Herramientas de gestión para la regeneración de la biodiversidad marina autóctona en litorales urbanizados
Abstract
La destrucción de hábitat se cuenta entre los cinco principales impactos que causan la pérdida de la biodiversidad en la naturaleza. En el entorno marino, esto se atribuye a la construcción de estructuras artificiales en la costa debido al desarrollo y a las necesidades de seguridad del ser humano. Esta tendencia está ganando velocidad debido al crecimiento de la población humana, así como por las oportunidades económicas que brindan las áreas costeras. Numerosos trabajos precedentes, han demostrado que las comunidades biológicas que se constituyen en estructuras artificiales son menos complejas y diversas que las del medio natural aledañas a éstas. Dichas estructuras artificiales afectan a la distribución de especies, la estructura de la comunidad y el funcionamiento de los ecosistemas. La presente tesis propone y justifica diversas herramientas de gestión que reducen el impacto producido en ciertos aspectos ecológicos causado por la construcción de defensas artificiales en los ecosistemas costeros. Entre los diversos estudios realizados, se ha constatado que también en el área del estrecho de Gibraltar en general y en la Ciudad de Ceuta en particular, la comunidad biológica del intermareal y submareal es notablemente menos diversa en estructuras artificiales en comparación con el entorno natural adyacente. Entre las diferentes medidas para mitigar esta situación, se ha comprobado que la creación de pozas intermareales en estructuras artificiales genera un microhábitat que atenúa las condiciones extremas del ambiente, lo que ha propiciado el aumento de la diversidad de especies y nichos ecológicos, e incluso ha favorecido el asentamiento de individuos de taxones que anteriormente no se encontraban en la estructura. Dado que la construcción de este tipo de diques tiene la finalidad de desarrollar y proteger los intereses humanos, suelen estar permanentemente custodiados. Este hecho ha provocado una situación paradójica, al asentarse en ellas poblaciones reproductoras de la lapa ferruginosa (Patella ferruginea) catalogada por la legislación vigente como ¨en peligro de extinción¨. Para favorecer los puentes genéticos entre poblaciones y el aumento de éstas en su área natural de distribución en el Mediterráneo Occidental, se ha propuesto y verificado la eficiencia de crear una ¨Red de Microrreservas Marinas Artificiales¨. Así mismo, se ha estudiado como la macro y micro rugosidad y la superficie del intermareal beneficia a la talla y densidad de adultos de esta especie, mientras que la inclinación vertical de la costa e impacto antrópico lo perjudica.
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ΗĂĚĂƵŶĂĚĞůĂƐŐƌĂŶĚĞƐĐŝĞŶĐŝĂƐŚĂĂƉŽƌƚĂĚŽƵŶŝŶŐƌĞĚŝĞŶƚĞĞƐĞŶĐŝĂůĞŶ ŶƵĞƐƚƌŽůĂƌŐŽƌĞƚƌŽĐĞƐŽĚĞƐĚĞůĂĐƌĞĞŶĐŝĂŝŶŝĐŝĂůĞŶŶƵĞƐƚƌĂƉƌŽƉŝĂŝŵƉŽƌƚĂŶĐŝĂ ĐſƐŵŝĐĂ>ĂĂƐƚƌŽŶŽŵşĂĚĞĨŝŶŝſŶƵĞƐƚƌŽŚŽŐĂƌĐŽŵŽƵŶƉĞƋƵĞŹŽƉůĂŶĞƚĂĞƐĐŽŶĚŝĚŽĞŶ ƵŶƌŝŶĐſŶĚĞƵŶĂŐĂůĂdžŝĂŵĞĚŝĂĞŶƚƌĞŵŝůůŽŶĞƐůĂďŝŽůŽŐşĂŶŽƐƋƵŝƚſŶƵĞƐƚƌŽĞƐƚĂƚƵƐĚĞ ƉĂƌĂŶŐŽŶĞƐĐƌĞĂĚŽƐĂŝŵĂŐĞŶĚĞŝŽƐůĂŐĞŽůŽŐşĂŶŽƐĚŝŽůĂŝŶŵĞŶƐŝĚĂĚĚĞůƚŝĞŵƉŽLJ ŶŽƐĞŶƐĞŹſůŽƉŽĐŽĚĞĠůƋƵĞŚĂŽĐƵƉĂĚŽŶƵĞƐƚƌĂƉƌŽƉŝĂĞƐƉĞĐŝĞΗ ĂĐŚŽĨƚŚĞŵĂũŽƌƐĐŝĞŶĐĞƐŚĂƐĐŽŶƚƌŝďƵƚĞĚĂŶĞƐƐĞŶƚŝĂůŝŶŐƌĞĚŝĞŶƚŝŶŽƵƌůŽŶŐ ƌĞƚƌĞĂƚĨƌŽŵĂŶŝŶŝƚŝĂůďĞůŝĞĨŝŶŽƵƌŽǁŶĐŽƐŵŝĐŝŵƉŽƌƚĂŶĐĞƐƚƌŽŶŽŵLJĚĞĨŝŶĞĚŽƵƌ ŚŽŵĞĂƐĂƐŵĂůůƉůĂŶĞƚƚƵĐŬĞĚĂǁĂLJŝŶŽŶĞĐŽƌŶĞƌŽĨĂŶĂǀĞƌĂŐĞŐĂůĂdžLJĂŵŽŶŐ ŵŝůůŝŽŶƐďŝŽůŽŐLJƚŽŽŬĂǁĂLJŽƵƌƐƚĂƚƵƐĂƐƉĂƌĂŐŽŶƐĐƌĞĂƚĞĚŝŶƚŚĞŝŵĂŐĞŽĨ'ŽĚ ŐĞŽůŽŐLJŐĂǀĞƵƐƚŚĞŝŵŵĞŶƐŝƚLJŽĨƚŝŵĞĂŶĚƚĂƵŐŚƚƵƐŚŽǁůŝƚƚůĞŽĨŝƚŽƵƌŽǁŶƐƉĞĐŝĞƐ ŚĂƐŽĐĐƵƉŝĞĚΗ ƌ^ƚĞƉŚĞŶ:ĂLJ'ŽƵůĚ ;ĞƐĚĞĂƌǁŝŶƌĞĨůĞdžŝŽŶĞƐƐŽďƌĞŚŝƐƚŽƌŝĂŶĂƚƵƌĂůͿ
RESUMEN La destrucción de hábitat se cuenta entre los cinco principales impactos que causan la pérdida de la biodiversidad en la naturaleza. En el entorno marino, esto se atribuye a la construcción de estructuras artificiales en la costa debido al desarrollo y a las necesidades de seguridad del ser humano. Esta tendencia está ganando velocidad debido al crecimiento de la población humana, así como por las oportunidades económicas que brindan las áreas costeras. Numerosos trabajos precedentes, han demostrado que las comunidades biológicas que se constituyen en estructuras artificiales son menos complejas y diversas que las del medio natural aledañas a éstas. Dichas estructuras artificiales afectan a la distribución de especies, la estructura de la comunidad y el funcionamiento de los ecosistemas. La presente tesis propone y justifica diversas herramientas de gestión que reducen el impacto producido en ciertos aspectos ecológicos causado por la construcción de defensas artificiales en los ecosistemas costeros. Entre los diversos estudios realizados, se ha constatado que también en el área del estrecho de Gibraltar en general y en la Ciudad de Ceuta en particular, la comunidad biológica del intermareal y submareal es notablemente menos diversa en estructuras artificiales en comparación con el entorno natural adyacente. Entre las diferentes medidas para mitigar esta situación, se ha comprobado que la creación de pozas intermareales en estructuras artificiales genera un microhábitat que atenúa las condiciones extremas del ambiente, lo que ha propiciado el aumento de la diversidad de especies y nichos ecológicos, e incluso ha favorecido el asentamiento de individuos de taxones que anteriormente no se encontraban en la estructura. Dado que la construcción de este tipo de diques tiene la finalidad de desarrollar y proteger los intereses humanos, suelen estar permanentemente custodiados. Este hecho ha provocado una situación paradójica, al asentarse en ellas poblaciones reproductoras de la lapa ferruginosa (Patella ferruginea) catalogada por la legislación vigente como ¨en peligro de extinción¨. Para favorecer los puentes genéticos entre poblaciones y el aumento de éstas en su área natural de distribución en el Mediterráneo Occidental, se ha propuesto y verificado la eficiencia de crear una ¨Red de Microrreservas Marinas Artificiales¨. Así mismo, se ha estudiado como la macro y micro rugosidad y la superficie del intermareal beneficia a la talla y densidad de adultos de esta especie, mientras que la inclinación vertical de la costa e impacto antrópico lo perjudica.
^dZd dŚĞĚĞƐƚƌƵĐƚŝŽŶŽĨŚĂďŝƚĂƚƌĂŶŬƐĂŵŽŶŐƚŚĞƚŽƉĨŝǀĞŝŵƉĂĐƚƐĐĂƵƐŝŶŐďŝŽĚŝǀĞƌƐŝƚLJ ůŽƐƐ ŝŶ ŶĂƚƵƌĞ /Ŷ ƚŚĞ ŵĂƌŝŶĞ ĞŶǀŝƌŽŶŵĞŶƚ ƚŚŝƐ ŝƐ ĂƚƚƌŝďƵƚĞĚ ƚŽ ƚŚĞ ĐŽŶƐƚƌƵĐƚŝŽŶ ŽĨ ĂƌƚŝĨŝĐŝĂůƐƚƌƵĐƚƵƌĞƐŽŶƚŚĞĐŽĂƐƚĚƵĞƚŽŚƵŵĂŶĚĞǀĞůŽƉŵĞŶƚĂŶĚƐĞĐƵƌŝƚLJŶĞĞĚƐdŚŝƐ ƚƌĞŶĚŝƐŐĂŝŶŝŶŐŵŽŵĞŶƚƵŵĚƵĞƚŽƚŚĞŐƌŽǁƚŚŽĨƚŚĞŚƵŵĂŶĂŶĚƵƌďĂŶƉŽƉƵůĂƚŝŽŶĂƐ ǁĞůůĂƐƚŚĞĞĐŽŶŽŵŝĐŽƉƉŽƌƚƵŶŝƚŝĞƐƉƌŽǀŝĚĞĚďLJĐŽĂƐƚĂůĂƌĞĂƐ EƵŵĞƌŽƵƐ ƉƌĞǀŝŽƵƐ ƐƚƵĚŝĞƐ ŚĂǀĞ ƐŚŽǁŶ ƚŚĂƚ ƚŚĞ ďŝŽůŽŐŝĐĂů ĐŽŵŵƵŶŝƚLJ ŝŶ ĂƌƚŝĨŝĐŝĂůƐƚƌƵĐƚƵƌĞƐĂƌĞůĞƐƐĐŽŵƉůĞdžĂŶĚĚŝǀĞƌƐĞƚŚĂŶƚŚŽƐĞŝŶƚŚĞƐƵƌƌŽƵŶĚŝŶŐŶĂƚƵƌĂů ĞŶǀŝƌŽŶŵĞŶƚ ĂŶĚ ƚŚĂƚ ƚŚĞLJ ĂĨĨĞĐƚ ƐƉĞĐŝĞƐ ĚŝƐƚƌŝďƵƚŝŽŶ ĐŽŵŵƵŶŝƚLJ ƐƚƌƵĐƚƵƌĞ ĂŶĚ ĞĐŽƐLJƐƚĞŵ ĨƵŶĐƚŝŽŶŝŶŐ dŚŝƐƚŚĞƐŝƐ ƉƌŽƉŽƐĞƐ ĂŶĚ ũƵƐƚŝĨŝĞƐ ǀĂƌŝŽƵƐ ŵĂŶĂŐĞŵĞŶƚ ƚŽŽůƐ ĂŝŵĞĚĂƚƌĞĚƵĐŝŶŐƚŚĞĞĐŽůŽŐŝĐĂůŝŵƉĂĐƚĐĂƵƐĞĚďLJƚŚĞĐŽŶƐƚƌƵĐƚŝŽŶŽĨĂƌƚŝĨŝĐŝĂůĚĞĨĞŶƐĞƐ ŝŶĐŽĂƐƚĂůĞĐŽƐLJƐƚĞŵƐ ŵŽŶŐƚŚĞǀĂƌŝŽƵƐƐƚƵĚŝĞƐĐŽŶĚƵĐƚĞĚŝƚŚĂƐďĞĞŶŽďƐĞƌǀĞĚƚŚĂƚŝŶƚŚĞĂƌĞĂŽĨ ƚŚĞ^ƚƌĂŝƚŽĨ'ŝďƌĂůƚĂƌŝŶŐĞŶĞƌĂůĂŶĚŝŶƚŚĞŝƚLJŽĨĞƵƚĂŝŶƉĂƌƚŝĐƵůĂƌƚŚĞďŝŽůŽŐŝĐĂů ĐŽŵŵƵŶŝƚLJŝŶƚŚĞŝŶƚĞƌƚŝĚĂůĂŶĚƐƵďƚŝĚĂůnjŽŶĞƐŝƐƐŝŐŶŝĨŝĐĂŶƚůLJůĞƐƐĂďƵŶĚĂŶƚŽŶĂƌƚŝĨŝĐŝĂů ƐƚƌƵĐƚƵƌĞƐ ĐŽŵƉĂƌĞĚ ƚŽ ƚŚĞ ĂĚũĂĐĞŶƚ ŶĂƚƵƌĂů ĞŶǀŝƌŽŶŵĞŶƚ ŵŽŶŐ ƚŚĞ ĚŝĨĨĞƌĞŶƚ ŵĞĂƐƵƌĞƐƚŽŵŝƚŝŐĂƚĞƚŚŝƐƐŝƚƵĂƚŝŽŶŝƚŚĂƐďĞĞŶĨŽƵŶĚƚŚĂƚƚŚĞĐƌĞĂƚŝŽŶŽĨŝŶƚĞƌƚŝĚĂůƉŽŽůƐ ŽŶĂƌƚŝĨŝĐŝĂůƐƚƌƵĐƚƵƌĞƐŐĞŶĞƌĂƚĞƐĂŵŝĐƌŽŚĂďŝƚĂƚƚŚĂƚĂƚƚĞŶƵĂƚĞƐƚŚĞĞdžƚƌĞŵĞĐŽŶĚŝƚŝŽŶƐ ŽĨƚŚĞĞŶǀŝƌŽŶŵĞŶƚdŚŝƐŚĂƐůĞĚƚŽĂŶŝŶĐƌĞĂƐĞŝŶƐƉĞĐŝĞƐĚŝǀĞƌƐŝƚLJĂŶĚĞĐŽůŽŐŝĐĂůŶŝĐŚĞƐ ĂŶĚ ĞǀĞŶ ĨĂĐŝůŝƚĂƚĞĚ ƚŚĞ ƐĞƚƚůĞŵĞŶƚ ŽĨ ŝŶĚŝǀŝĚƵĂůƐ ĨƌŽŵ ŽƚŚĞƌ ƚĂdžĂ ƚŚĂƚ ǁĞƌĞ ŶŽƚ ƉƌĞǀŝŽƵƐůLJĨŽƵŶĚŝŶƚŚĞƐƚƌƵĐƚƵƌĞ 'ŝǀĞŶƚŚĂƚƚŚĞĐŽŶƐƚƌƵĐƚŝŽŶŽĨƚŚĞƐĞƚLJƉĞƐŽĨƐƚƌƵĐƚƵƌĞƐĂŝŵƐƚŽĚĞǀĞůŽƉĂŶĚ ƉƌŽƚĞĐƚƐŽĐŝĞƚĂůŝŶƚĞƌĞƐƚƐƚŚĞLJĂƌĞƵƐƵĂůůLJĐŽŶƐƚĂŶƚůLJŐƵĂƌĚĞĚdŚŝƐĨĂĐƚŚĂƐůĞĚƚŽĂ ƉĂƌĂĚŽdžŝĐĂů ƐŝƚƵĂƚŝŽŶ ĂƐ ƌĞƉƌŽĚƵĐƚŝǀĞƉŽƉƵůĂƚŝŽŶƐ ŽĨ ƚŚĞ ĨĞƌƌƵŐŝŶŽƵƐ ůŝŵƉĞƚ ;WĂƚĞůůĂ ĨĞƌƌƵŐŝŶĞĂͿĐůĂƐƐŝĨŝĞĚďLJĐƵƌƌĞŶƚůĞŐŝƐůĂƚŝŽŶĂƐΗĞŶĚĂŶŐĞƌĞĚΗŚĂǀĞƐĞƚƚůĞĚŽŶƚŚĞŵdŽ ƉƌŽŵŽƚĞ ŐĞŶĞƚŝĐ ďƌŝĚŐĞƐ ďĞƚǁĞĞŶ ƉŽƉƵůĂƚŝŽŶƐ ĂŶĚ ƚŚĞŝƌ ŝŶĐƌĞĂƐĞ ŝŶ ƚŚĞŝƌ ŶĂƚƵƌĂů ĚŝƐƚƌŝďƵƚŝŽŶĂƌĞĂŝŶƚŚĞtĞƐƚĞƌŶDĞĚŝƚĞƌƌĂŶĞĂŶƚŚĞĞĨĨŝĐŝĞŶĐLJŽĨĐƌĞĂƚŝŶŐĂŶΗƌƚŝĨŝĐŝĂů DĂƌŝŶĞ DŝĐƌŽƌĞƐĞƌǀĞ EĞƚǁŽƌŬƐΗ ŚĂƐ ďĞĞŶ ƉƌŽƉŽƐĞĚ ĂŶĚ ǀĞƌŝĨŝĞĚ &ƵƌƚŚĞƌŵŽƌĞ ƚŚĞ ŵĂĐƌŽĂŶĚŵŝĐƌŽƌŽƵŐŚŶĞƐƐĂŶĚƚŚĞƐƵƌĨĂĐĞŽĨƚŚĞŝŶƚĞƌƚŝĚĂůnjŽŶĞŚĂǀĞďĞĞŶƐƚƵĚŝĞĚƚŽ ďĞŶĞĨŝƚƚŚĞƐŝnjĞĂŶĚĚĞŶƐŝƚLJŽĨĂĚƵůƚŝŶĚŝǀŝĚƵĂůƐŽĨƚŚŝƐƐƉĞĐŝĞƐǁŚĞƌĞĂƐƚŚĞǀĞƌƚŝĐĂůƐůŽƉĞ ŽĨƚŚĞĐŽĂƐƚĂŶĚĂŶƚŚƌŽƉŽŐĞŶŝĐŝŵƉĂĐƚĚĞƚƌŝŵĞŶƚĂůůLJĂĨĨĞĐƚŝƚ RESUMEN La destrucción de hábitat se cuenta entre los cinco principales impactos que causan la pérdida de la biodiversidad en la naturaleza. En el entorno marino, esto se atribuye a la construcción de estructuras artificiales en la costa debido al desarrollo y a las necesidades de seguridad del ser humano. Esta tendencia está ganando velocidad debido al crecimiento de la población humana, así como por las oportunidades económicas que brindan las áreas costeras. Numerosos trabajos precedentes, han demostrado que las comunidades biológicas que se constituyen en estructuras artificiales son menos complejas y diversas que las del medio natural aledañas a éstas. Dichas estructuras artificiales afectan a la distribución de especies, la estructura de la comunidad y el funcionamiento de los ecosistemas. La presente tesis propone y justifica diversas herramientas de gestión que reducen el impacto producido en ciertos aspectos ecológicos causado por la construcción de defensas artificiales en los ecosistemas costeros. Entre los diversos estudios realizados, se ha constatado que también en el área del estrecho de Gibraltar en general y en la Ciudad de Ceuta en particular, la comunidad biológica del intermareal y submareal es notablemente menos diversa en estructuras artificiales en comparación con el entorno natural adyacente. Entre las diferentes medidas para mitigar esta situación, se ha comprobado que la creación de pozas intermareales en estructuras artificiales genera un microhábitat que atenúa las condiciones extremas del ambiente, lo que ha propiciado el aumento de la diversidad de especies y nichos ecológicos, e incluso ha favorecido el asentamiento de individuos de taxones que anteriormente no se encontraban en la estructura. Dado que la construcción de este tipo de diques tiene la finalidad de desarrollar y proteger los intereses humanos, suelen estar permanentemente custodiados. Este hecho ha provocado una situación paradójica, al asentarse en ellas poblaciones reproductoras de la lapa ferruginosa (Patella ferruginea) catalogada por la legislación vigente como ¨en peligro de extinción¨. Para favorecer los puentes genéticos entre poblaciones y el aumento de éstas en su área natural de distribución en el Mediterráneo Occidental, se ha propuesto y verificado la eficiencia de crear una ¨Red de Microrreservas Marinas Artificiales¨. Así mismo, se ha estudiado como la macro y micro rugosidad y la superficie del intermareal beneficia a la talla y densidad de adultos de esta especie, mientras que la inclinación vertical de la costa e impacto antrópico lo perjudica.
1E/ ϭ d^/^WKZKDWE/KWh>//KE^ / Relación de publicaciones ………………………………………………………… // Informe de los directores de la tesis ….. /// /ŶĨŽƌŵĞĚĞƌĞůĞǀĂŶĐŝĂĐŝĞŶƚşĨŝĐa de las publicaciones …. /s Otras publicaciones como base formativa …. s /ŶĨŽƌŵĞĚĞůŽƐĚŝƌĞĐƚŽƌĞƐƐŽďƌĞůĂĐŽŶƚƌŝďƵĐŝſŶĚĞĐĂĚĂƵŶŽĚĞůŽƐĂƵƚŽƌĞƐ ĂůŽƐƚƌĂďĂũŽƐƉƵďůŝĐĂĚŽƐ………….. s/ /ŶĨŽƌŵĞĚĞůŽƐĐŽĂƵƚŽƌĞƐŶŽĚŽĐƚŽƌĞƐƐŽďƌĞůĂƌĞŶƵŶĐŝĂĚĞƉƌĞƐĞŶƚĂĞƐƚŽƐ ƚƌĂďĂũŽƐĐŽŵŽƉĂƌƚĞĚĞƵŶĂƚĞƐŝƐƉŽƌĐŽŵƉĞŶĚŝŽ………… Ϯ WZKzdKd^/^KdKZ> / Introducción general ………… // Objetivos e hipótesis ………… /// Wh>//ME ϭ ƌĞĂĐŝſŶ ĚĞ ŵŝĐƌŽŚĄďŝƚĂƚƐ ;ƉŽnjĂƐ ŝŶƚĞƌŵĂƌĞĂůĞƐͿ ĞŶ ĞƐĐŽůůĞƌĂƐĐŽŶĐŽŵƵŶŝĚĂĚĞƐďŝŽůſŐŝĐĂƐĞŶĞƚĂƉĂĐůşŵĂdžĚĞƐƵƐƵĐĞƐŝſŶ ĞĐŽůſŐŝĐĂ ĐŽŵŽ ĨŽƌŵĂ ĚĞ ŵŝƚŝŐĂƌ ůŽƐ ĞĨĞĐƚŽƐ ŶĞŐĂƚŝǀŽƐ ĚĞů ƐƵƐƚƌĂƚŽ ĂƌƚŝĨŝĐŝĂůƐŽďƌĞůĂďŝŽĚŝǀĞƌƐŝĚĂĚŵĂƌŝŶĂ…………… /s Wh>//MEϮ^ƵĐĞƐŝſŶĞĐŽůſŐŝĐĂĚĞůĂĐŽŵƵŶŝĚĂĚďŝŽůſŐŝĐĂĂƐĞŶƚĂĚĂ ĞŶƉŽnjĂƐŝŶƚĞƌŵĂƌĞĂůĞƐĐƌĞĂĚĂƐĞŶ ĞƐƚƌƵĐƚƵƌĂƐĚĞƉƌŽƚĞĐĐŝſŶĐŽƐƚĞƌĂƐ ;ϳϱĂŹŽƐĚĞŵŽŶŝƚŽƌŝnjĂĐŝſŶͿ………………… s Wh>//ME ϯ DŝĐƌŽƌƌĞƐĞƌǀĂƐ ŵĂƌŝŶĂƐ ĂƌƚŝĨŝĐŝĂůĞƐ ĐŽŵŽ ŶƵĞǀĂ ŚĞƌƌĂŵŝĞŶƚĂĚĞŐĞƐƚŝſŶĞĐŽƐŝƐƚĠŵŝĐĂƉĂƌĂůĂĐŽŶƐĞƌǀĂĐŝſŶŵĂƌŝŶĂĞůĐĂƐŽ ĚĞ W ĨĞƌƌƵŐŝŶĞĂ ;'ĂƐƚƌŽƉŽĚĂ WĂƚĞůůŝĚĂĞͿ ƵŶŽ ĚĞ ůŽƐ ŝŶǀĞƌƚĞďƌĂĚŽƐ ŵĂƌŝŶŽƐŵĄƐĂŵĞŶĂnjĂĚŽƐĚĞůDĞĚŝƚĞƌƌĄŶĞŽ………… s/ Wh>//MEϰƐƚƵĚŝŽĚĞůĂĚŝŶĄŵŝĐĂƉŽďůĂĐŝŽŶĂůLJĞĨĞĐƚŽƐĂďŝſƚŝĐŽƐ ƋƵĞ ŵŽĚĞůĂŶ ůĂ ĞƐƚƌƵĐƚƵƌĂ ƉŽďůĂĐŝŽŶĂů ĚĞů ŵŽůƵƐĐŽ ŐĂƐƚĞƌſƉŽĚŽ W ĨĞƌƌƵŐŝŶĞĂĂƐĞŶƚĂĚŽĞŶĞůůŝƚŽƌĂůĚĞĞƵƚĂ…………… s// ŝƐĐƵƐŝſŶŐĞŶĞƌĂů…………………… s/// ŽŶĐůƵƐŝŽŶĞƐ……
d^/^WKZKDWE/KWh>//KE^
21 d^/^WKZKDWE/KWh>//KE^ /Z>/MEWh>//KE^ >Ă ƉƌĞƐĞŶƚĞ ƚĞƐŝƐ ĚŽĐƚŽƌĂů ĚĞ ĂĐƵĞƌĚŽ ĐŽŶ Ğů ŝŶĨŽƌŵĞ ĐŽƌƌĞƐƉŽŶĚŝĞŶƚĞ ĂƵƚŽƌŝnjĂĚŽƉŽƌĞůŝƌĞĐƚŽƌĚĞdĞƐŝƐLJůĂŽŵŝƐŝſŶĚĞůWƌŽŐƌĂŵĂĚĞŽĐƚŽƌĂĚŽƐĞƉƌĞƐĞŶƚĂ ĐŽŵŽ ƵŶ ĐŽŵƉĞŶĚŝŽ ĚĞ ĐƵĂƚƌŽ ƚƌĂďĂũŽƐ ƉƌĞǀŝĂŵĞŶƚĞ ƉƵďůŝĐĂĚŽƐ >ĂƐ ƌĞĨĞƌĞŶĐŝĂƐ ĐŽŵƉůĞƚĂƐĚĞůŽƐĂƌƚşĐƵůŽƐƋƵĞĐŽŶƐƚŝƚƵLJĞŶĞůĐƵĞƌƉŽĚĞůĂƚĞƐŝƐƐŽŶůĂƐƐŝŐƵŝĞŶƚĞƐ ϭ KƐƚĂůĠͲsĂůƌŝďĞƌĂƐ ^ĞŵƉĞƌĞͲsĂůǀĞƌĚĞ : ŽƉƉĂ ^ 'ĂƌĐşĂͲ'ſŵĞnj : Θ ƐƉŝŶŽƐĂ & ;ϮϬϭϴͿ ƌĞĂƚŝŽŶ ŽĨ ŵŝĐƌŽŚĂďŝƚĂƚƐ ;ƚŝĚĞƉŽŽůƐͿ ŝŶ ƌŝƉƌĂƉƐ ǁŝƚŚ ĐůŝŵĂdž ĐŽŵŵƵŶŝƚŝĞƐĂƐĂǁĂLJƚŽŵŝƚŝŐĂƚĞŶĞŐĂƚŝǀĞĞĨĨĞĐƚƐŽĨĂƌƚŝĨŝĐŝĂůƐƵďƐƚƌĂƚĞŽŶŵĂƌŝŶĞ ďŝŽĚŝǀĞƌƐŝƚLJĐŽůŽŐŝĐĂůĞŶŐŝŶĞĞƌŝŶŐϭϮϬϱϮϮͲϱϯϭ ŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϭϲũĞĐŽůĞŶŐϮϬϭϴϬϲϬϮϯ Ϯ KƐƚĂůĠͲsĂůƌŝďĞƌĂƐDĂƌƚşŶͲŽƌƌŝůůĂ^ĞŵƉĞƌĞͲsĂůǀĞƌĚĞ:'ĂƌĐşĂͲ'ſŵĞnj: ΘƐƉŝŶŽƐĂ&;ϮϬϮϰͿĐŽůŽŐŝĐĂůƐƵĐĐĞƐƐŝŽŶǁŝƚŚŝŶŵŝĐƌŽŚĂďŝƚĂƚƐ;ƚŝĚĞƉŽŽůƐͿĐƌĞĂƚĞĚ ŝŶ ƌŝƉƌĂƉƐƚƌƵĐƚƵƌĞƐ ŚŽƐƚŝŶŐ ĐůŝŵĂdž ĐŽŵŵƵŶŝƚŝĞƐ Ŷ ĞĐŽŶŽŵŝĐĂů ƐƚƌĂƚĞŐLJ ĨŽƌŵŝƚŝŐĂƚŝŶŐ ƚŚĞ ŶĞŐĂƚŝǀĞ ĞĨĨĞĐƚƐ ŽĨ ĐŽĂƐƚĂů ĚĞĨĞŶĐĞ ƐƚƌƵĐƚƵƌĞ ŽŶ ŵĂƌŝŶĞ ďŝŽĚŝǀĞƌƐŝƚLJĐŽůŽŐŝĐĂůĞŶŐŝŶĞĞƌŝŶŐϮϬϬϭϬϳͲϭϴϳ ŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϭϲũĞĐŽůĞŶŐϮϬϮϰϭϬϳϭϴϳ ϯ KƐƚĂůĠͲsĂůƌŝďĞƌĂƐ ^ĞŵƉĞƌĞͲsĂůǀĞƌĚĞ : WĂǀſŶͲWĂŶĞƋƵĞ ŽƉƉĂ ^ ƐƉŝŶŽƐĂ&Θ'ĂƌĐşĂͲ'ſŵĞnj:;ϮϬϮϮͿƌƚŝĨŝĐŝĂůŵĂƌŝŶĞŵŝĐƌŽͲƌĞƐĞƌǀĞƐĂƐĂŶĞǁ ĞĐŽƐLJƐƚĞŵͲďĂƐĞĚŵĂŶĂŐĞŵĞŶƚƚŽŽůĨŽƌŵĂƌŝŶĞĐŽŶƐĞƌǀĂƚŝŽŶdŚĞĐĂƐĞŽĨWĂƚĞůůĂ ĨĞƌƌƵŐŝŶĞĂ ;'ĂƐƚƌŽƉŽĚĂ WĂƚĞůůŝĚĂĞͿ ŽŶĞ ŽĨ ƚŚĞ ŵŽƐƚ ĞŶĚĂŶŐĞƌĞĚ ŵĂƌŝŶĞ ŝŶǀĞƌƚĞďƌĂƚĞƐŽĨƚŚĞDĞĚŝƚĞƌƌĂŶĞĂŶDĂƌŝŶĞWŽůŝĐLJϭϯϲϭϬϰϵϭϳ ŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϭϲũŵĂƌƉŽůϮϬϮϭϭϬϰϵϭϳ ϰ KƐƚĂůĠͲsĂůƌŝďĞƌĂƐ ^ĂďŝŶŽͲ>ŽƌĞŶnjŽ ůŝͲŚŵĞĚ WĂǀſŶͲWĂŶĞƋƵĞ ^ĞŵƉĞƌĞͲsĂůǀĞƌĚĞ : ƐƉŝŶŽƐĂ & Θ 'ĂƌĐşĂͲ'ſŵĞnj : ;ϮϬϮϯͿ tŚĞŶ ƚŚĞ ƉŽƉƵůĂƚŝŽŶŽĨĂŶĞŶĚĂŶŐĞƌĞĚŵĂƌŝŶĞŵŽůůƵƐĐ;WĂƚĞůůĂĨĞƌƌƵŐŝŶĞĂͿŝŶĐƌĞĂƐĞƐĂůŵŽƐƚ ƚŚƌĞĞͲĨŽůĚŝŶƚĞŶLJĞĂƌƐZĞĂůŝƚLJŽƌĨŝĐƚŝŽŶ&ƌŽŶƚŝĞƌƐŝŶDĂƌŝŶĞ^ĐŝĞŶĐĞϭϬϭϭϮϳϲϯϬ ŚƚƚƉƐĚŽŝŽƌŐϭϬϯϯϴϵĨŵĂƌƐϮϬϮϯϭϭϮϳϲϯϬ
23 ///E&KZD/ZdKZ^d^/^ /E&KZD/ZdKZ^^KZ>d^/^KdKZ>EZ/YhK^d>s>Z/Z^ ƌ&ƌĞĞƐƉŝŶŽƐĂdŽƌƌĞLJƌ:ŽƐĠĂƌůŽƐ'ĂƌĐşĂ'ſŵĞnj ĞƌƚŝĨŝĐĂŶ YƵĞŶƌŝƋƵĞKƐƚĂůĠsĂůƌŝďĞƌĂƐůŝĐĞŶĐŝĂĚŽĞŶŝĞŶĐŝĂƐĚĞůDĂƌƉŽƌůĂhŶŝǀĞƌƐŝĚĂĚĚĞ ĄĚŝnj ŚĂƌĞĂůŝnjĂĚo la tesis doctoral titulada: “HERRAMIENTAS DE GESTIÓN PARA LA Z'EZ/ME > /K/sZ^/ DZ/E hdMdKE E >/dKZ>^ URBANIZADOS”ĚĞŶƚƌŽĚĞůWƌŽŐƌĂŵĂĚĞŽĐƚŽƌĂĚŽĞŶŝŽůŽŐşĂ/ŶƚĞŐƌĂĚĂĞŶůĂůşŶĞĂĚĞ ŝŶǀĞƐƚŝŐĂĐŝſŶĚĞŝŽůŽŐşĂŶŝŵĂů&ŝƐŝŽůŽŐşĂŝŽƚĞĐŶŽůŽŐşĂŝŽĚŝǀĞƌƐŝĚĂĚǀŽůƵĐŝſŶLJ ŽŶƐĞƌǀĂĐŝſŶ ŝĐŚĂ ƚĞƐŝƐ ĚŽĐƚŽƌĂů ĨŽƌŵĂĚĂ ƉŽƌ ƵŶ ĐŽŶũƵŶƚŽ ĚĞ ĐƵĂƚƌŽ ƉƵďůŝĐĂĐŝŽŶĞƐ ĐŝĞŶƚşĨŝĐĂƐ ;ĐŽŵƉĞŶĚŝŽĚĞƉƵďůŝĐĂĐŝŽŶĞƐͿĐƵŵƉůĞŶĐŽŶůŽƐŽďũĞƚŝǀŽƐLJĐƌŝƚĞƌŝŽƐĚĞĐĂůŝĚĂĚĞdžŝŐŝĚŽƐ ƉĂƌĂŽƉƚĂƌĂůƚşƚƵůŽĚĞĚŽĐƚŽƌƉŽƌůĂhŶŝǀĞƌƐŝĚĂĚĚĞ^ĞǀŝůůĂĚĞŶƚƌŽĚĞƐƵƉƌŽŐƌĂŵĂĚĞ ŝŽůŽŐşĂ/ŶƚĞŐƌĂĚĂ ^ĞǀŝůůĂĂďƌŝůĚĞϮϬϮϰ /E&KZD/ZdKZ^^KZ>d^/^KdKZ>EZ/YhK^d>s>Z/Z^ ƌ&ƌĞĞƐƉŝŶŽƐĂdŽƌƌĞLJƌ:ŽƐĠĂƌůŽƐ'ĂƌĐşĂ'ſŵĞnj ĞƌƚŝĨŝĐĂŶ YƵĞŶƌŝƋƵĞKƐƚĂůĠsĂůƌŝďĞƌĂƐůŝĐĞŶĐŝĂĚŽĞŶŝĞŶĐŝĂƐĚĞůDĂƌƉŽƌůĂhŶŝǀĞƌƐŝĚĂĚĚĞ ĄĚŝnj ŚĂƌĞĂůŝnjĂĚo la tesis doctoral titulada: “HERRAMIENTAS DE GESTIÓN PARA LA Z'EZ/ME > /K/sZ^/ DZ/E hdMdKE E >/dKZ>^ URBANIZADOS”ĚĞŶƚƌŽĚĞůWƌŽŐƌĂŵĂĚĞŽĐƚŽƌĂĚŽĞŶŝŽůŽŐşĂ/ŶƚĞŐƌĂĚĂĞŶůĂůşŶĞĂĚĞ ŝŶǀĞƐƚŝŐĂĐŝſŶĚĞŝŽůŽŐşĂŶŝŵĂů&ŝƐŝŽůŽŐşĂŝŽƚĞĐŶŽůŽŐşĂŝŽĚŝǀĞƌƐŝĚĂĚǀŽůƵĐŝſŶLJ ŽŶƐĞƌǀĂĐŝſŶ ŝĐŚĂ ƚĞƐŝƐ ĚŽĐƚŽƌĂů ĨŽƌŵĂĚĂ ƉŽƌ ƵŶ ĐŽŶũƵŶƚŽ ĚĞ ĐƵĂƚƌŽ ƉƵďůŝĐĂĐŝŽŶĞƐ ĐŝĞŶƚşĨŝĐĂƐ ;ĐŽŵƉĞŶĚŝŽĚĞƉƵďůŝĐĂĐŝŽŶĞƐͿĐƵŵƉůĞŶĐŽŶůŽƐŽďũĞƚŝǀŽƐLJĐƌŝƚĞƌŝŽƐĚĞĐĂůŝĚĂĚĞdžŝŐŝĚŽƐ ƉĂƌĂŽƉƚĂƌĂůƚşƚƵůŽĚĞĚŽĐƚŽƌƉŽƌůĂhŶŝǀĞƌƐŝĚĂĚĚĞ^ĞǀŝůůĂĚĞŶƚƌŽĚĞƐƵƉƌŽŐƌĂŵĂĚĞ ŝŽůŽŐşĂ/ŶƚĞŐƌĂĚĂ ^ĞǀŝůůĂĂďƌŝůĚĞϮϬϮϰ sǑǑĚĞůŽƐĚŝƌĞĐƚŽƌĞƐ &ĚŽ&ƌĞĞƐƉŝŶŽƐĂdŽƌƌĞ &ĚŽ:ŽƐĠĂƌůŽƐ'ĂƌĐşĂ'ſŵĞnj ůŝŶƚĞƌĞƐĂĚŽ &ĚŽŶƌŝƋƵĞKƐƚĂůĠsĂůƌŝďĞƌĂƐ sǑǑĚĞůŽƐĚŝƌĞĐƚŽƌĞƐ &ĚŽ&ƌĞĞƐƉŝŶŽƐĂdŽƌƌĞ &ĚŽ:ŽƐĠĂƌůŽƐ'ĂƌĐşĂ'ſŵĞnj ůŝŶƚĞƌĞƐĂĚŽ &ĚŽŶƌŝƋƵĞKƐƚĂůĠsĂůƌŝďĞƌĂƐ sǑǑĚĞůŽƐĚŝƌĞĐƚŽƌĞƐ &ĚŽ&ƌĞĞƐƉŝŶŽƐĂdŽƌƌĞ&ĚŽ:ŽƐĠĂƌůŽƐ'ĂƌĐşĂ'ſŵĞnj ůŝŶƚĞƌĞƐĂĚŽ &ĚŽŶƌŝƋƵĞKƐƚĂůĠsĂůƌŝďĞƌĂƐ
25 ////E&KZDZ>sE//Ed1&/>^Wh>//KE^ ĐŽŶƚŝŶƵĂĐŝſŶƐĞŵĞŶĐŝŽŶĂĞůŝŵƉĂĐƚŽĚĞĐĂĚĂĄƌĞĂƚĞŵĄƚŝĐĂĚĞůĂƐƌĞǀŝƐƚĂƐĞŶůĂƋƵĞ ƐĞŚĂŶƉƵďůŝĐĂĚŽůŽƐĂƌƚşĐƵůŽƐƋƵĞĐŽŶƐƚŝƚƵLJĞŶůĂƉƌĞƐĞŶƚĞƚĞƐŝƐůĨĂĐƚŽƌĚĞŝŵƉĂĐƚŽƐĞ ŚĂŝŶĚŝĐĂĚŽƐĞŐƷŶĞůşŶĚŝĐĞ:ŽƵƌŶĂůŝƚĂƚŝŽŶZĞƉŽƌƚ;:ZͿLJ^ĐŝŵĂŐŽ:ŽƵƌŶĂůZĂŶŬ;^:ZͿ ϭ KƐƚĂůĠͲsĂůƌŝďĞƌĂƐ ^ĞŵƉĞƌĞͲsĂůǀĞƌĚĞ : ŽƉƉĂ ^ 'ĂƌĐşĂͲ'ſŵĞnj : Θ ƐƉŝŶŽƐĂ & ;ϮϬϭϴͿ ƌĞĂƚŝŽŶ ŽĨ ŵŝĐƌŽŚĂďŝƚĂƚƐ ;ƚŝĚĞƉŽŽůƐͿ ŝŶ ƌŝƉƌĂƉƐ ǁŝƚŚ ĐůŝŵĂdž ĐŽŵŵƵŶŝƚŝĞƐĂƐĂǁĂLJƚŽŵŝƚŝŐĂƚĞŶĞŐĂƚŝǀĞĞĨĨĞĐƚƐŽĨĂƌƚŝĨŝĐŝĂůƐƵďƐƚƌĂƚĞŽŶŵĂƌŝŶĞ ďŝŽĚŝǀĞƌƐŝƚLJĐŽůŽŐŝĐĂůĞŶŐŝŶĞĞƌŝŶŐϭϮϬϱϮϮͲϱϯϭ ŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϭϲũĞĐŽůĞŶŐϮϬϭϴϬϲϬϮϯ &ĂĐƚŽƌĚĞŝŵƉĂĐƚŽLJĄƌĞĂƚĞŵĄƚŝĐĂĚĞůĂƌĞǀŝƐƚĂ &ĂĐƚŽƌĚĞŝŵƉĂĐƚŽĞŶ:ZͲϮϬϭϳ;ĂŹŽĚĞĂĐĞƉƚĂĐŝſŶͿ ϯϬϮϯ ůĂƐŝĨŝĐĂĐŝſŶƉŽƌ ĐĂƚĞŐŽƌşĂ /ŶŐĞŶŝĞƌşĂŵĞĚŝŽĂŵďŝĞŶƚĞ ϮϬϱϬ;ϮǑƵĂƌƚŝůͿ ŝĞŶĐŝĂƐŵĞĚŝŽĂŵďŝĞŶƚĞƐ ϳϮϮϰϭ;ϮǑƵĂƌƚŝůͿ ĐŽůŽŐşĂ ϰϳϭϱϴ;ϮǑƵĂƌƚŝůͿ &ĂĐƚŽƌĚĞŝŵƉĂĐƚŽĞŶ^:ZͲϮϬϭϳ;ĂŹŽĚĞĂĐĞƉƚĂĐŝſŶͿ ϭϬϰϮ;ϭǑƵĂƌƚŝůͿ ůĂƐŝĨŝĐĂĐŝſŶƉŽƌ ĐĂƚĞŐŽƌşĂ /ŶŐĞŶŝĞƌşĂŵĞĚŝŽĂŵďŝĞŶƚĂů ϮϯϮϵϭ;ϭǑƵĂƌƚŝůͿ 'ĞƐƚŝſŶĐŽŶƚƌŽůƉŽůşƚŝĐĂLJ ůĞŐŝƐůĂĐŝſŶ ϰϵϯϳϳ;ϭǑƵĂƌƚŝůͿ ŽŶƐĞƌǀĂĐŝſŶĚĞůĂŶĂƚƵƌĂůĞnjĂLJĞů ƉĂŝƐĂũĞ ϮϴϭϳϮ;ϭǑƵĂƌƚŝůͿ
32 ZĞůĞǀĂŶĐŝĂĚĞůĂĂƉŽƌƚĂĐŝſŶĞŶĞůĐŽŶƚĞdžƚŽĐŝĞŶƚşĨŝĐŽĚĞůĂƚĞŵĄƚŝĐĂ ŶƚƌĞ ůŽƐ ĂŹŽƐ ϮϬϭϭ LJ ϮϬϮϭ Ğů ƚĂŵĂŹŽ ĞƐƚŝŵĂĚŽ ĚĞ ůĂ ƉŽďůĂĐŝſŶ ĚĞ W ĨĞƌƌƵŐŝŶĞĂŚĂĂƵŵĞŶƚĂĚŽƵŶϮϬϬйƉĂƐĂŶĚŽĚĞϱϱϵϬϮĂϭϲϴϰϲϯŝŶĚŝǀŝĚƵŽƐ ;ĚĞůŽƐĐƵĂůĞƐϭϯϭϳϳϲƐŽŶĂĚƵůƚŽƐͿ >ŽƐƌĞƐƵůƚĂĚŽƐĚĞůƉƌĞƐĞŶƚĞĞƐƚƵĚŝŽŝŶĚŝĐĂŶƋƵĞĞůůŝƚŽƌĂůĚĞĞƵƚĂĂůďĞƌŐĂůĂ ƉƌŝŶĐŝƉĂů ƉŽďůĂĐŝſŶ ĚĞ ĞƐƚĂ ĞƐƉĞĐŝĞ ĂŵĞŶĂnjĂĚĂ Ă ůŽ ůĂƌŐŽ ĚĞ ƐƵ ĄƌĞĂ ĚĞ ĚŝƐƚƌŝďƵĐŝſŶĞŶĞůDĞĚŝƚĞƌƌĄŶĞŽKĐĐŝĚĞŶƚĂůƐŝĞŶĚŽƵŶĂƉŽďůĂĐŝſŶĨƵĞŶƚĞĞŶ ĞůƐƵƌĚĞůĂWĞŶşŶƐƵůĂ/ďĠƌŝĐĂĐƵLJĂƉƌĞƐĞƌǀĂĐŝſŶĚĞďĞƐĞƌƉƌŝŽƌŝƚĂƌŝĂ ůĂƵŵĞŶƚŽĞdžƉĞƌŝŵĞŶƚĂĚŽƉŽƌůĂƉŽďůĂĐŝſŶǀĂůŝĚĂůŽƐƌĞƐƵůƚĂĚŽƐĚĞůŵĠƚŽĚŽ ĚĞƉƌĞĚŝĐĐŝſŶΗƉŽƉƵůĂƚŝŽŶǀŝĂďŝůŝƚLJĂŶĂůLJƐŝƐΗ;WsͿůůĞǀĂĚŽĂĐĂďŽƉŽƌƐƉŝŶŽƐĂ ĞƚĂů;ϮϬϭϴͿƉĂƌĂůĂƉŽďůĂĐŝſŶĚĞWĨĞƌƌƵŐŝŶĞĂĞŶĞƵƚĂ >ĂĚĞŶƐŝĚĂĚĚĞĂĚƵůƚŽƐĚĞWĨĞƌƌƵŐŝŶĞĂĞƐƚĄŝŶĨůƵĞŶĐŝĂĚĂƉŽƐŝƚŝǀĂŵĞŶƚĞƉŽƌ ůĂŚĞƚĞƌŽŐĞŶĞŝĚĂĚĐŽƐƚĞƌĂůĂƐƵƉĞƌĨŝĐŝĞĚĞůŚĄďŝƚĂƚLJůĂƌƵŐŽƐŝĚĂĚĚĞůƐƵƐƚƌĂƚŽ ƉĞƌŽŶĞŐĂƚŝǀĂŵĞŶƚĞƉŽƌůĂŝŶĐůŝŶĂĐŝſŶǀĞƌƚŝĐĂůůĂĐŽŶĐĞŶƚƌĂĐŝſŶĚĞĐůŽƌŽĨŝůĂͲĂ LJ Ğů ŝŵƉĂĐƚŽ ĂŶƚƌŽƉŽŐĠŶŝĐŽ ƐƚŽƐ ƉĂƌĄŵĞƚƌŽƐ ĂŵďŝĞŶƚĂůĞƐ ĚĞďĞŶ ƐĞƌ ĐŽŶƐŝĚĞƌĂĚŽƐ ĞŶ Ğů ĐĂƐŽ ƋƵĞ ƐĞ ŶĞĐĞƐŝƚĞ ůŽĐĂůŝnjĂƌ ƵŶĂ njŽŶĂ ƌĞĐĞƉƚŽƌĂ ĚĞ ŝŶĚŝǀŝĚƵŽƐƚƌĂƐůĂĚĂĚŽƐ >ŽƐƌĞƐƵůƚĂĚŽƐĂƉŽLJĂŶƋƵĞůĂĐƌĞĂĐŝſŶĚĞƵŶĂZĞĚĚĞDŝĐƌŽƌƌĞƐĞƌǀĂƐDĂƌŝŶĂƐ ƌƚŝĨŝĐŝĂůĞƐĐŽŶƚƌŝďƵLJĞĂĞƐƚĂďůĞĐĞƌĐŽŶĞdžŝŽŶĞƐĞŶƚƌĞȇƉŽďůĂĐŝŽŶĞƐĨƵĞŶƚĞƐȇ ĚĞWĨĞƌƌƵŐŝŶĞĂĐŽŶůŽƋƵĞƐĞƉƌŽŵƵĞǀĞĞůĨůƵũŽŐĞŶĠƚŝĐŽĞŶƚƌĞƉŽďůĂĐŝŽŶĞƐ ĂƐş ĐŽŵŽ ůĂ ƌĞĐŽůŽŶŝnjĂĐŝſŶ ĚĞů ŵĞĚŝŽ ŶĂƚƵƌĂů Ă ůŽ ůĂƌŐŽ ĚĞ ƐƵ ĄƌĞĂ ĚĞ ĚŝƐƚƌŝďƵĐŝſŶŽƌŝŐŝŶĂů /sKdZ^Wh>//KE^KDK^&KZDd/s ĐŽŶƚŝŶƵĂĐŝſŶƐĞĐŝƚĂŶĚŝƐƚŝŶƚŽƐĂƌƚşĐƵůŽƐĐŝĞŶƚşĨŝĐŽƐƋƵĞŚĂŶĐŽŶƐƚŝƚƵŝĚŽƉĂƌƚĞĚĞůĂ ďĂƐĞĨŽƌŵĂƚŝǀĂĚĞůĚŽĐƚŽƌĂŶĚŽLJĞŶůŽƐĐƵĂůĞƐƉĂƌƚŝĐŝƉĂĐŽŵŽĐŽĂƵƚŽƌ ϮϬϭϴ ^ĞŵƉĞƌĞͲsĂůǀĞƌĚĞ : KƐƚĂůĠͲsĂůƌŝďĞƌĂƐ &ĂƌĨĄŶ ' D Θ ƐƉŝŶŽƐĂ & ;ϮϬϭϴͿ ^ƵďƐƚƌĂƚƵŵ ƚLJƉĞ ĂĨĨĞĐƚƐ ƌĞĐƌƵŝƚŵĞŶƚ ĂŶĚ ĚĞǀĞůŽƉŵĞŶƚ ŽĨ ŵĂƌŝŶĞ ĂƐƐĞŵďůĂŐĞƐŽǀĞƌĂƌƚŝĨŝĐŝĂůƐƵďƐƚƌĂƚĂĐĂƐĞƐƚƵĚLJŝŶƚŚĞůďŽƌĂŶ^ĞĂƐƚƵĂƌŝŶĞ ŽĂƐƚĂůĂŶĚ^ŚĞůĨ^ĐŝĞŶĐĞϮϬϰϱϲͲϲϱ ϮϬϭϴEspinosa, F., Rivera‐Ingraham, G. A., Ostalé‐Valriberas, E., & García‐Gómez, J. ;ϮϬϭϴͿWƌĞĚŝĐƚŝŶŐƚŚĞĨĂƚĞŽĨƚŚĞŵŽƐƚĞŶĚĂŶŐĞƌĞĚŵĂƌŝŶĞŝŶǀĞƌƚĞďƌĂƚĞŽĨ the Mediterranean: The power of long‐term monitoring in conservation ďŝŽůŽŐLJ ƋƵĂƚŝĐ ŽŶƐĞƌǀĂƚŝŽŶ DĂƌŝŶĞ ĂŶĚ &ƌĞƐŚǁĂƚĞƌ ĐŽƐLJƐƚĞŵƐ Ϯϴ;ϲͿ ϭϮϴϯͲϭϮϵϯ ϮϬϭϴ 'ĂƌĐşĂ'ſŵĞnj:^ĞŵƉĞƌĞsĂůǀĞƌĚĞ:KƐƚĂůĠsĂůƌŝďĞƌĂƐDĂƌƚşŶĞnjD KůĂLJĂWŽŶnjŽŶĞ>ZŽŝ'ŽŶnjĄůĞnjƐƉŝŶŽƐĂ&^ĄŶĐŚĞnjͲDŽLJĂŶŽDĞŐŝŶĂ ΘWĂƌĂĚĂ:;ϮϬϭϴͿZƵŐƵůŽƉƚĞƌLJdžŽŬĂŵƵƌĂĞ;zĂǁƐŽŶͿ/<,ǁĂŶŐt: Lee & HS Kim (Dictyotales, Ochrophyta), alga exótica “explosiva” en el estrecho ĚĞ 'ŝďƌĂůƚĂƌ KďƐĞƌǀĂĐŝŽŶĞƐ ƉƌĞůŝŵŝŶĂƌĞƐ ĚĞ ƐƵ ĚŝƐƚƌŝďƵĐŝſŶ Ğ ŝŵƉĂĐƚŽ ůŵŽƌĂŝŵĂZĞǀŝƐƚĂĚĞƐƚƵĚŝŽƐĂŵƉŽŐŝďƌĂůƚĂƌĞŹŽƐϰϵϵϳͲϭϭϯ ϮϬϭϵ EĂǀĂƌƌŽͲĂƌƌĂŶĐŽDƵŹŽnjͲ'ſŵĞnj^ĂŝnjZŽƐD'ƵĞƌƌĂͲ'ĂƌĐşĂ:D ůƚĂŵŝƌĂŶŽDKƐƚĂůĠsĂůƌŝďĞƌĂƐΘDŽƌĞŝƌĂ:;ϮϬϭϵͿĂŶŝŶǀĂƐŝǀĞŚĂďŝƚĂƚͲ ĨŽƌŵŝŶŐ ƐƉĞĐŝĞƐ ƉůĂLJ ƚŚĞ ƐĂŵĞ ƌŽůĞ ĂƐ ŶĂƚŝǀĞ ŽŶĞƐ dŚĞ ĐĂƐĞ ŽĨ ƚŚĞ ĞdžŽƚŝĐ ŵĂƌŝŶĞŵĂĐƌŽĂůŐĂZƵŐƵůŽƉƚĞƌLJdžŽŬĂŵƵƌĂĞŝŶƚŚĞ^ƚƌĂŝƚŽĨ'ŝďƌĂůƚĂƌŝŽůŽŐŝĐĂů /ŶǀĂƐŝŽŶƐϮϭϯϯϭϵͲϯϯϯϰ ϮϬϭϵ ƐƉŝŶŽƐĂ&KƐƚĂůĠͲsĂůƌŝďĞƌĂƐDĂĞƐƚƌĞD'ŽŶnjĄůĞnjZKƵĞƌŐŚŝ ^ŐŚĂŝĞƌzZΘĂnjĂŝƌŝ,;ϮϬϭϵͿ^ŝŐŚƚŝŶŐŽĨĂƌĞĚĐŽƌĂůŽƌĂůůŝƵŵƌƵďƌƵŵ ;>ŝŶŶĂĞƵƐ ϭϳϱϴͿ ƉŽƉƵůĂƚŝŽŶ ůŝǀŝŶŐ Ăƚ 'ŝďƌĂůƚĂƌ ^ƚƌĂŝƚ ZĞŐŝŽŶĂů ^ƚƵĚŝĞƐ ŝŶ DĂƌŝŶĞ^ĐŝĞŶĐĞϮϵϭϬϬϲϰϭ ϮϬϮϬ 'ĂƌĐşĂͲ'ſŵĞnj:^ĞŵƉĞƌĞͲsĂůǀĞƌĚĞ:'ŽŶnjĄůĞnjZDĂƌƚşŶĞnjͲŚĂĐſŶ DKůĂLJĂͲWŽŶnjŽŶĞ>^ĄŶĐŚĞnjͲDŽLJĂŶŽKƐƚĂůĠͲsĂůƌŝďĞƌĂƐΘDĞŐŝŶĂ ;ϮϬϮϬͿ &ƌŽŵ ĞdžŽƚŝĐ ƚŽ ŝŶǀĂƐŝǀĞ ŝŶ ƌĞĐŽƌĚ ƚŝŵĞ dŚĞ ĞdžƚƌĞŵĞ ŝŵƉĂĐƚ ŽĨ ZƵŐƵůŽƉƚĞƌLJdž ŽŬĂŵƵƌĂĞ ;ŝĐƚLJŽƚĂůĞƐ KĐŚƌŽƉŚLJƚĂͿ ŝŶ ƚŚĞ ƐƚƌĂŝƚ ŽĨ 'ŝďƌĂůƚĂƌ ^ĐŝĞŶĐĞŽĨdŚĞdŽƚĂůŶǀŝƌŽŶŵĞŶƚϳϬϰϭϯϱϰϬϴ ϮϬϮϬ ZŽƐ D EĂǀĂƌƌŽͲĂƌƌĂŶĐŽ 'ŽŶnjĄůĞnjͲ^ĄŶĐŚĞnj D KƐƚĂůĠͲsĂůƌŝďĞƌĂƐ ĞƌǀĞƌĂͲƵƌƌĂĚŽ > Θ 'ƵĞƌƌĂͲ'Ăƌкà : D ;ϮϬϮϬͿ ^ƚĂƌƚŝŶŐ ƚŚĞ ƐƚŽǁĂǁĂLJ
33 ZĞůĞǀĂŶĐŝĂĚĞůĂĂƉŽƌƚĂĐŝſŶĞŶĞůĐŽŶƚĞdžƚŽĐŝĞŶƚşĨŝĐŽĚĞůĂƚĞŵĄƚŝĐĂ ŶƚƌĞ ůŽƐ ĂŹŽƐ ϮϬϭϭ LJ ϮϬϮϭ Ğů ƚĂŵĂŹŽ ĞƐƚŝŵĂĚŽ ĚĞ ůĂ ƉŽďůĂĐŝſŶ ĚĞ W ĨĞƌƌƵŐŝŶĞĂŚĂĂƵŵĞŶƚĂĚŽƵŶϮϬϬйƉĂƐĂŶĚŽĚĞϱϱϵϬϮĂϭϲϴϰϲϯŝŶĚŝǀŝĚƵŽƐ ;ĚĞůŽƐĐƵĂůĞƐϭϯϭϳϳϲƐŽŶĂĚƵůƚŽƐͿ >ŽƐƌĞƐƵůƚĂĚŽƐĚĞůƉƌĞƐĞŶƚĞĞƐƚƵĚŝŽŝŶĚŝĐĂŶƋƵĞĞůůŝƚŽƌĂůĚĞĞƵƚĂĂůďĞƌŐĂůĂ ƉƌŝŶĐŝƉĂů ƉŽďůĂĐŝſŶ ĚĞ ĞƐƚĂ ĞƐƉĞĐŝĞ ĂŵĞŶĂnjĂĚĂ Ă ůŽ ůĂƌŐŽ ĚĞ ƐƵ ĄƌĞĂ ĚĞ ĚŝƐƚƌŝďƵĐŝſŶĞŶĞůDĞĚŝƚĞƌƌĄŶĞŽKĐĐŝĚĞŶƚĂůƐŝĞŶĚŽƵŶĂƉŽďůĂĐŝſŶĨƵĞŶƚĞĞŶ ĞůƐƵƌĚĞůĂWĞŶşŶƐƵůĂ/ďĠƌŝĐĂĐƵLJĂƉƌĞƐĞƌǀĂĐŝſŶĚĞďĞƐĞƌƉƌŝŽƌŝƚĂƌŝĂ ůĂƵŵĞŶƚŽĞdžƉĞƌŝŵĞŶƚĂĚŽƉŽƌůĂƉŽďůĂĐŝſŶǀĂůŝĚĂůŽƐƌĞƐƵůƚĂĚŽƐĚĞůŵĠƚŽĚŽ ĚĞƉƌĞĚŝĐĐŝſŶΗƉŽƉƵůĂƚŝŽŶǀŝĂďŝůŝƚLJĂŶĂůLJƐŝƐΗ;WsͿůůĞǀĂĚŽĂĐĂďŽƉŽƌƐƉŝŶŽƐĂ ĞƚĂů;ϮϬϭϴͿƉĂƌĂůĂƉŽďůĂĐŝſŶĚĞWĨĞƌƌƵŐŝŶĞĂĞŶĞƵƚĂ >ĂĚĞŶƐŝĚĂĚĚĞĂĚƵůƚŽƐĚĞWĨĞƌƌƵŐŝŶĞĂĞƐƚĄŝŶĨůƵĞŶĐŝĂĚĂƉŽƐŝƚŝǀĂŵĞŶƚĞƉŽƌ ůĂŚĞƚĞƌŽŐĞŶĞŝĚĂĚĐŽƐƚĞƌĂůĂƐƵƉĞƌĨŝĐŝĞĚĞůŚĄďŝƚĂƚLJůĂƌƵŐŽƐŝĚĂĚĚĞůƐƵƐƚƌĂƚŽ ƉĞƌŽŶĞŐĂƚŝǀĂŵĞŶƚĞƉŽƌůĂŝŶĐůŝŶĂĐŝſŶǀĞƌƚŝĐĂůůĂĐŽŶĐĞŶƚƌĂĐŝſŶĚĞĐůŽƌŽĨŝůĂͲĂ LJ Ğů ŝŵƉĂĐƚŽ ĂŶƚƌŽƉŽŐĠŶŝĐŽ ƐƚŽƐ ƉĂƌĄŵĞƚƌŽƐ ĂŵďŝĞŶƚĂůĞƐ ĚĞďĞŶ ƐĞƌ ĐŽŶƐŝĚĞƌĂĚŽƐ ĞŶ Ğů ĐĂƐŽ ƋƵĞ ƐĞ ŶĞĐĞƐŝƚĞ ůŽĐĂůŝnjĂƌ ƵŶĂ njŽŶĂ ƌĞĐĞƉƚŽƌĂ ĚĞ ŝŶĚŝǀŝĚƵŽƐƚƌĂƐůĂĚĂĚŽƐ >ŽƐƌĞƐƵůƚĂĚŽƐĂƉŽLJĂŶƋƵĞůĂĐƌĞĂĐŝſŶĚĞƵŶĂZĞĚĚĞDŝĐƌŽƌƌĞƐĞƌǀĂƐDĂƌŝŶĂƐ ƌƚŝĨŝĐŝĂůĞƐĐŽŶƚƌŝďƵLJĞĂĞƐƚĂďůĞĐĞƌĐŽŶĞdžŝŽŶĞƐĞŶƚƌĞȇƉŽďůĂĐŝŽŶĞƐĨƵĞŶƚĞƐȇ ĚĞWĨĞƌƌƵŐŝŶĞĂĐŽŶůŽƋƵĞƐĞƉƌŽŵƵĞǀĞĞůĨůƵũŽŐĞŶĠƚŝĐŽĞŶƚƌĞƉŽďůĂĐŝŽŶĞƐ ĂƐş ĐŽŵŽ ůĂ ƌĞĐŽůŽŶŝnjĂĐŝſŶ ĚĞů ŵĞĚŝŽ ŶĂƚƵƌĂů Ă ůŽ ůĂƌŐŽ ĚĞ ƐƵ ĄƌĞĂ ĚĞ ĚŝƐƚƌŝďƵĐŝſŶŽƌŝŐŝŶĂů /sKdZ^Wh>//KE^KDK^&KZDd/s ĐŽŶƚŝŶƵĂĐŝſŶƐĞĐŝƚĂŶĚŝƐƚŝŶƚŽƐĂƌƚşĐƵůŽƐĐŝĞŶƚşĨŝĐŽƐƋƵĞŚĂŶĐŽŶƐƚŝƚƵŝĚŽƉĂƌƚĞĚĞůĂ ďĂƐĞĨŽƌŵĂƚŝǀĂĚĞůĚŽĐƚŽƌĂŶĚŽLJĞŶůŽƐĐƵĂůĞƐƉĂƌƚŝĐŝƉĂĐŽŵŽĐŽĂƵƚŽƌ ϮϬϭϴ ^ĞŵƉĞƌĞͲsĂůǀĞƌĚĞ : KƐƚĂůĠͲsĂůƌŝďĞƌĂƐ &ĂƌĨĄŶ ' D Θ ƐƉŝŶŽƐĂ & ;ϮϬϭϴͿ ^ƵďƐƚƌĂƚƵŵ ƚLJƉĞ ĂĨĨĞĐƚƐ ƌĞĐƌƵŝƚŵĞŶƚ ĂŶĚ ĚĞǀĞůŽƉŵĞŶƚ ŽĨ ŵĂƌŝŶĞ ĂƐƐĞŵďůĂŐĞƐŽǀĞƌĂƌƚŝĨŝĐŝĂůƐƵďƐƚƌĂƚĂĐĂƐĞƐƚƵĚLJŝŶƚŚĞůďŽƌĂŶ^ĞĂƐƚƵĂƌŝŶĞ ŽĂƐƚĂůĂŶĚ^ŚĞůĨ^ĐŝĞŶĐĞϮϬϰϱϲͲϲϱ ϮϬϭϴEspinosa, F., Rivera‐Ingraham, G. A., Ostalé‐Valriberas, E., & García‐Gómez, J. ;ϮϬϭϴͿWƌĞĚŝĐƚŝŶŐƚŚĞĨĂƚĞŽĨƚŚĞŵŽƐƚĞŶĚĂŶŐĞƌĞĚŵĂƌŝŶĞŝŶǀĞƌƚĞďƌĂƚĞŽĨ the Mediterranean: The power of long‐term monitoring in conservation ďŝŽůŽŐLJ ƋƵĂƚŝĐ ŽŶƐĞƌǀĂƚŝŽŶ DĂƌŝŶĞ ĂŶĚ &ƌĞƐŚǁĂƚĞƌ ĐŽƐLJƐƚĞŵƐ Ϯϴ;ϲͿ ϭϮϴϯͲϭϮϵϯ ϮϬϭϴ 'ĂƌĐşĂ'ſŵĞnj:^ĞŵƉĞƌĞsĂůǀĞƌĚĞ:KƐƚĂůĠsĂůƌŝďĞƌĂƐDĂƌƚşŶĞnjD KůĂLJĂWŽŶnjŽŶĞ>ZŽŝ'ŽŶnjĄůĞnjƐƉŝŶŽƐĂ&^ĄŶĐŚĞnjͲDŽLJĂŶŽDĞŐŝŶĂ ΘWĂƌĂĚĂ:;ϮϬϭϴͿZƵŐƵůŽƉƚĞƌLJdžŽŬĂŵƵƌĂĞ;zĂǁƐŽŶͿ/<,ǁĂŶŐt: Lee & HS Kim (Dictyotales, Ochrophyta), alga exótica “explosiva” en el estrecho ĚĞ 'ŝďƌĂůƚĂƌ KďƐĞƌǀĂĐŝŽŶĞƐ ƉƌĞůŝŵŝŶĂƌĞƐ ĚĞ ƐƵ ĚŝƐƚƌŝďƵĐŝſŶ Ğ ŝŵƉĂĐƚŽ ůŵŽƌĂŝŵĂZĞǀŝƐƚĂĚĞƐƚƵĚŝŽƐĂŵƉŽŐŝďƌĂůƚĂƌĞŹŽƐϰϵϵϳͲϭϭϯ ϮϬϭϵ EĂǀĂƌƌŽͲĂƌƌĂŶĐŽDƵŹŽnjͲ'ſŵĞnj^ĂŝnjZŽƐD'ƵĞƌƌĂͲ'ĂƌĐşĂ:D ůƚĂŵŝƌĂŶŽDKƐƚĂůĠsĂůƌŝďĞƌĂƐΘDŽƌĞŝƌĂ:;ϮϬϭϵͿĂŶŝŶǀĂƐŝǀĞŚĂďŝƚĂƚͲ ĨŽƌŵŝŶŐ ƐƉĞĐŝĞƐ ƉůĂLJ ƚŚĞ ƐĂŵĞ ƌŽůĞ ĂƐ ŶĂƚŝǀĞ ŽŶĞƐ dŚĞ ĐĂƐĞ ŽĨ ƚŚĞ ĞdžŽƚŝĐ ŵĂƌŝŶĞŵĂĐƌŽĂůŐĂZƵŐƵůŽƉƚĞƌLJdžŽŬĂŵƵƌĂĞŝŶƚŚĞ^ƚƌĂŝƚŽĨ'ŝďƌĂůƚĂƌŝŽůŽŐŝĐĂů /ŶǀĂƐŝŽŶƐϮϭϯϯϭϵͲϯϯϯϰ ϮϬϭϵ ƐƉŝŶŽƐĂ&KƐƚĂůĠͲsĂůƌŝďĞƌĂƐDĂĞƐƚƌĞD'ŽŶnjĄůĞnjZKƵĞƌŐŚŝ ^ŐŚĂŝĞƌzZΘĂnjĂŝƌŝ,;ϮϬϭϵͿ^ŝŐŚƚŝŶŐŽĨĂƌĞĚĐŽƌĂůŽƌĂůůŝƵŵƌƵďƌƵŵ ;>ŝŶŶĂĞƵƐ ϭϳϱϴͿ ƉŽƉƵůĂƚŝŽŶ ůŝǀŝŶŐ Ăƚ 'ŝďƌĂůƚĂƌ ^ƚƌĂŝƚ ZĞŐŝŽŶĂů ^ƚƵĚŝĞƐ ŝŶ DĂƌŝŶĞ^ĐŝĞŶĐĞϮϵϭϬϬϲϰϭ ϮϬϮϬ 'ĂƌĐşĂͲ'ſŵĞnj:^ĞŵƉĞƌĞͲsĂůǀĞƌĚĞ:'ŽŶnjĄůĞnjZDĂƌƚşŶĞnjͲŚĂĐſŶ DKůĂLJĂͲWŽŶnjŽŶĞ>^ĄŶĐŚĞnjͲDŽLJĂŶŽKƐƚĂůĠͲsĂůƌŝďĞƌĂƐΘDĞŐŝŶĂ ;ϮϬϮϬͿ &ƌŽŵ ĞdžŽƚŝĐ ƚŽ ŝŶǀĂƐŝǀĞ ŝŶ ƌĞĐŽƌĚ ƚŝŵĞ dŚĞ ĞdžƚƌĞŵĞ ŝŵƉĂĐƚ ŽĨ ZƵŐƵůŽƉƚĞƌLJdž ŽŬĂŵƵƌĂĞ ;ŝĐƚLJŽƚĂůĞƐ KĐŚƌŽƉŚLJƚĂͿ ŝŶ ƚŚĞ ƐƚƌĂŝƚ ŽĨ 'ŝďƌĂůƚĂƌ ^ĐŝĞŶĐĞŽĨdŚĞdŽƚĂůŶǀŝƌŽŶŵĞŶƚϳϬϰϭϯϱϰϬϴ ϮϬϮϬ ZŽƐ D EĂǀĂƌƌŽͲĂƌƌĂŶĐŽ 'ŽŶnjĄůĞnjͲ^ĄŶĐŚĞnj D KƐƚĂůĠͲsĂůƌŝďĞƌĂƐ ĞƌǀĞƌĂͲƵƌƌĂĚŽ > Θ 'ƵĞƌƌĂͲ'Ăƌкà : D ;ϮϬϮϬͿ ^ƚĂƌƚŝŶŐ ƚŚĞ ƐƚŽǁĂǁĂLJ
34 ƉĂƚŚǁĂLJƚŚĞƌŽůĞŽĨĚŝƐƉĞƌƐĂůďĞŚĂǀŝŽƌŝŶƚŚĞŝŶǀĂƐŝŽŶƐƵĐĐĞƐƐŽĨůŽǁͲŵŽďŝůĞ ŵĂƌŝŶĞƐƉĞĐŝĞƐŝŽůŽŐŝĐĂů/ŶǀĂƐŝŽŶƐϮϮϮϳϵϳͲϮϴϭϮ ϮϬϮϬ ĂůĚĞƌĂ:tŚŝƚŶĞLJ:>ELJĞŐĂĂƌĚDKƐƚĂůĠͲsĂůƌŝďĞƌĂƐ<ƵďŝĐĞŬ>Θ dŚLJƐdD;ϮϬϮϬͿ'ĞŶĞƚŝĐŝŶƐŝŐŚƚƐƌĞŐĂƌĚŝŶŐƚŚĞƚĂdžŽŶŽŵLJƉŚLJůŽŐĞŽŐƌĂƉŚLJ ĂŶĚ ĞǀŽůƵƚŝŽŶ ŽĨ ŽĐĞĂŶ ƐƵŶĨŝƐŚĞƐ ;DŽůŝĚĂĞ dĞƚƌĂŽĚŽŶƚŝĨŽƌŵĞƐͿ dŚĞ ŽĐĞĂŶ ƐƵŶĨŝƐŚĞƐĞǀŽůƵƚŝŽŶďŝŽůŽŐLJĂŶĚĐŽŶƐĞƌǀĂƚŝŽŶZWƌĞƐƐŽĐĂZĂƚŽŶϯϳͲϱϰ ϮϬϮϭ ^ĞŵƉĞƌĞͲsĂůǀĞƌĚĞ:KƐƚĂůĠͲsĂůƌŝďĞƌĂƐDĂĞƐƚƌĞDƌĂŶĚĂZ'ĂnjĂŝƌŝ ,ΘƐƉŝŶŽƐĂ&;ϮϬϮϭͿ/ŵƉĂĐƚƐŽĨƚŚĞŶŽŶͲŝŶĚŝŐĞŶŽƵƐƐĞĂǁĞĞĚZƵŐƵůŽƉƚĞƌLJdž ŽŬĂŵƵƌĂĞŽŶĂDĞĚŝƚĞƌƌĂŶĞĂŶĐŽƌĂůůŝŐĞŶŽƵƐĐŽŵŵƵŶŝƚLJ;^ƚƌĂŝƚŽĨ'ŝďƌĂůƚĂƌͿ dŚĞƌŽůĞŽĨůŽŶŐͲƚĞƌŵŵŽŶŝƚŽƌŝŶŐĐŽůŽŐŝĐĂů/ŶĚŝĐĂƚŽƌƐϭϮϭϭϬϳϭϯϱ ϮϬϮϭNavarro‐Barranco, C., Moreira, J., Espinosa, F., Ros, M., RalliƐ, I., SemperesĂůǀĞƌĚĞ : KƐƚĂůĠͲsĂůƌŝďĞƌĂƐ ůƚĂŵŝƌĂŶŽ D & Guerra‐García, J. M. ;ϮϬϮϭͿ ǀĂůƵĂƚŝŶŐ ƚŚĞ ǀƵůŶĞƌĂďŝůŝƚLJ ŽĨ ĐŽƌĂůůŝŐĞŶŽƵƐ ĞƉŝĨĂƵŶĂ ƚŽ ŵĂĐƌŽĂůŐĂů ŝŶǀĂƐŝŽŶƐ ƋƵĂƚŝĐ ŽŶƐĞƌǀĂƚŝŽŶ DĂƌŝŶĞ ĂŶĚ &ƌĞƐŚǁĂƚĞƌ ĐŽƐLJƐƚĞŵƐ ϯϭ;ϵͿ ϮϯϬϱͲϮϯϭϵ ϮϬϮϯ 'ĂƌĐşĂͲ'ſŵĞnj:ŝĚͲ/ƚƵƌďĞKƐƚĂůĠͲsĂůƌŝďĞƌĂƐƐƉĂĚĂZĂƌďĂůůŽ: > &Ă 'ĂƌĐşĂͲKůĂLJĂ Θ ůĂŶĐĂͲ^ƷũĂƌ Z ;ϮϬϮϯͿ ĚǀĂŶĐĞƐ ŝŶ ƚŚĞ ŵĂŶĂŐĞŵĞŶƚ ĂŶĚ ƚƌĂŶƐůŽĐĂƚŝŽŶ ŵĞƚŚŽĚŽůŽŐLJ ŽĨ ƚŚĞ ĞŶĚĂŶŐĞƌĞĚ ŵŽůůƵƐŬ WĂƚĞůůĂĨĞƌƌƵŐŝŶĞĂŝŶĂƌƚŝĨŝĐŝĂůŚĂďŝƚĂƚƐŽĨƉŽƌƚŝŶĨƌĂƐƚƌƵĐƚƵƌĞƐŝŵƉůŝĐĂƚŝŽŶƐĨŽƌ ŝƚƐĐŽŶƐĞƌǀĂƚŝŽŶ&ƌŽŶƚŝĞƌƐŝŶDĂƌŝŶĞ^ĐŝĞŶĐĞϭϬϭϭϲϲϵϯϳ ϮϬϮϰ Pavón‐Paneque, A., Ostalé‐Valriberas, E., Sempere‐Valverde, J., Sedano, F., Espinosa, F., & García‐Gómez, J. C. (202ϰͿƌƚŝĨŝĐŝĂůƉŽƌƚĂďůĞƉůĂƚĞƐďƌĂŶĚ ŶĞǁŵĞƚŚŽĚĨŽƌĂƐƐŝƐƚĞĚĐŽůŽŶŝnjĂƚŝŽŶŽĨĂŶĞŶĚĂŶŐĞƌĞĚŵĂƌŝŶĞŝŶǀĞƌƚĞďƌĂƚĞ WĂƚĞůůĂĨĞƌƌƵŐŝŶĞĂƋƵĂƚŝĐŽŶƐĞƌǀĂƚŝŽŶDĂƌŝŶĞĂŶĚ&ƌĞƐŚǁĂƚĞƌĐŽƐLJƐƚĞŵƐ ϮϬϮϰ ^ĞŵƉĞƌĞͲsĂůǀĞƌĚĞ:KƐƚĂůĠͲsĂůƌŝďĞƌĂƐƐƉŝŶŽƐĂ&ΘDĄƌƋƵĞnj&;ϮϬϮϰͿ DŽƌƉŚŽŵĞƚƌŝĐǀĂƌŝĂƚŝŽŶƐŽĨƚǁŽƉĂƚĞůůŝĚůŝŵƉĞƚƐďĞƚǁĞĞŶĂƌƚŝĨŝĐŝĂůďƌĞĂŬǁĂƚĞƌƐ ĂŶĚŶĂƚƵƌĂůƌĞĞĨƐƐƚƵĂƌŝŶĞŽĂƐƚĂůĂŶĚ^ŚĞůĨ^ĐŝĞŶĐĞϭϬϴϲϭϳ s/E&KZD>K^/ZdKZ^^KZ>KEdZ/h/MEhEK>K^ hdKZ^>K^dZ:K^Wh>/K^ >ŽƐ ĚŝƐƚŝŶƚŽƐ ĞƐƚƵĚŝŽƐ ƉƌĞƐĞŶƚĂĚŽƐ ŚĂŶ ƌĞƋƵĞƌŝĚŽ ĚĞ ƵŶĂ ůĂďŽƌ ŝŶƚĞŶƐĂ ĚĞ ŵƵĞƐƚƌĞŽ;ƚĂŶƚŽĞƐƉĂĐŝĂůĐŽŵŽƚĞŵƉŽƌĂůŵĞŶƚĞͿůŽƋƵĞŚĂŵŽƚŝǀĂĚŽĞůĐŽŶĐƵƌƐŽĚĞ ŽƚƌŽƐŝŶǀĞƐƚŝŐĂĚŽƌĞƐĞŶůĂƚŽŵĂĚĞĚĂƚŽƐŶƚŽĚŽƐĞůůŽƐĞůĚŽĐƚŽƌĂŶĚŽŚĂĂĐƚƵĂĚŽĐŽŵŽ ƉƌŝŵĞƌĂƵƚŽƌƌĞƐƉŽŶƐĂďŝůŝnjĄŶĚŽƐĞĚĞůĂĐŽŽƌĚŝŶĂĐŝſŶƉůĂŶŝĨŝĐĂĐŝſŶLJĞũĞĐƵĐŝſŶĚĞůŽƐ ŵƵĞƐƚƌĞŽƐ ĂƐş ĐŽŵŽ ĚĞ ůĂ ŵĂLJŽƌ ƉĂƌƚĞ ĚĞ ůŽƐ ĂŶĄůŝƐŝƐ ĚĞ ĚĂƚŽƐ LJ ƌĞĚĂĐƚĂŶĚŽ ůŽƐ ďŽƌƌĂĚŽƌĞƐ ĚĞ ĐĂĚĂ ĂƌƚşĐƵůŽ ƉƵďůŝĐĂĚŽ Ŷ ĂůŐƷŶ ĐĂƐŽ ŽƚƌŽƐ ĂƵƚŽƌĞƐ ƚĂŵďŝĠŶ ŚĂŶ ĐŽŶƚƌŝďƵŝĚŽĞŶĞůĂŶĄůŝƐŝƐĚĞůĂŝŶĨŽƌŵĂĐŝſŶĚĞďŝĚŽĂƐƵĐŽŶŽĐŝŵŝĞŶƚŽĞŶĚĞƚĞƌŵŝŶĂĚĂƐ ŚĞƌƌĂŵŝĞŶƚĂƐ ĂŶĂůşƚŝĐĂƐ >ŽƐ ĚŽƐ ƷůƚŝŵŽƐ ĨŝƌŵĂŶƚĞƐ ĐŽƌƌĞƐƉŽŶĚĞŶ Ă ůŽƐ ĚŝƌĞĐƚŽƌĞƐ ĚĞ ƚĞƐŝƐƋƵĞŚĂŶƐƵƉĞƌǀŝƐĂĚŽLJĐŽƌƌĞŐŝĚŽĞůƚƌĂďĂũŽ >ĂƐĨƵŶĐŝŽŶĞƐƋƵĞŚĂŶĚĞƐĞŵƉĞŹĂĚŽůŽƐĐŽůĂďŽƌĂĚŽƌĞƐĞŶůŽƐƌĞƐƵůƚĂĚŽƐĚĞůĂƐ ŝŶǀĞƐƚŝŐĂĐŝŽŶĞƐƐĞ ƌĞĂůŝnjĂ ƐĞŐƷŶ ůĂ ĐĂƚĞŐŽƌŝnjĂĐŝſŶ ĚĞ ZĞĚĚŝd ;ŽŶƚƌŝďƵƚŽƌ ZŽůĞƐ dĂdžŽŶŽŵLJͿ ϭ KƐƚĂůĠͲsĂůƌŝďĞƌĂƐ ^ĞŵƉĞƌĞͲsĂůǀĞƌĚĞ : ŽƉƉĂ ^ 'ĂƌĐşĂͲ'ſŵĞnj : Θ ƐƉŝŶŽƐĂ & ;ϮϬϭϴͿ ƌĞĂƚŝŽŶ ŽĨ ŵŝĐƌŽŚĂďŝƚĂƚƐ ;ƚŝĚĞƉŽŽůƐͿ ŝŶ ƌŝƉƌĂƉƐ ǁŝƚŚ ĐůŝŵĂdž ĐŽŵŵƵŶŝƚŝĞƐĂƐĂǁĂLJƚŽŵŝƚŝŐĂƚĞŶĞŐĂƚŝǀĞĞĨĨĞĐƚƐŽĨĂƌƚŝĨŝĐŝĂůƐƵďƐƚƌĂƚĞŽŶŵĂƌŝŶĞ ďŝŽĚŝǀĞƌƐŝƚLJĐŽůŽŐŝĐĂůĞŶŐŝŶĞĞƌŝŶŐϭϮϬϱϮϮͲϱϯϭ KƐƚĂůĠͲsĂůƌŝďĞƌĂƐ ĐŽŶƐĞƌǀĂĐŝſŶ ĚĞ ĚĂƚŽƐ ĂŶĄůŝƐŝƐ ĨŽƌŵĂů ŝŶǀĞƐƚŝŐĂĐŝſŶ ĂĚŵŝŶŝƐƚƌĂĐŝſŶ ĚĞů ƉƌŽLJĞĐƚŽ ƐƵƉĞƌǀŝƐŝſŶ ǀŝƐƵĂůŝnjĂĐŝſŶ ƌĞĚĂĐĐŝſŶͲďŽƌƌĂĚŽƌ ŽƌŝŐŝŶĂůƌĞĚĂĐĐŝſŶͲƌĞǀŝƐŝſŶLJĞĚŝĐŝſŶ ^ĞŵƉĞƌĞͲsĂůǀĞƌĚĞ:ĐŽŶƐĞƌǀĂĐŝſŶĚĞĚĂƚŽƐĂŶĄůŝƐŝƐĨŽƌŵĂůŝŶǀĞƐƚŝŐĂĐŝſŶ ǀŝƐƵĂůŝnjĂĐŝſŶƌĞĚĂĐĐŝſŶͲƌĞǀŝƐŝſŶLJĞĚŝĐŝſŶ ŽƉƉĂ ^ ĐŽŶƐĞƌǀĂĐŝſŶ ĚĞ ĚĂƚŽƐ ŝŶǀĞƐƚŝŐĂĐŝſŶ ǀŝƐƵĂůŝnjĂĐŝſŶ ƌĞĚĂĐĐŝſŶͲ ƌĞǀŝƐŝſŶLJĞĚŝĐŝſŶ 'ĂƌĐşĂͲ'ſŵĞnj:ĂĚƋƵŝƐŝĐŝſŶĚĞĨŝŶĂŶĐŝĂĐŝſŶƌĞĐƵƌƐŽƐƌĞĚĂĐĐŝſŶͲƌĞǀŝƐŝſŶ LJĞĚŝĐŝſŶ ƐƉŝŶŽƐĂ & ĐŽŶĐĞƉƚƵĂůŝnjĂĐŝſŶ ĐŽŶƐĞƌǀĂĐŝſŶ ĚĞ ĚĂƚŽƐ ĂĚƋƵŝƐŝĐŝſŶ ĚĞ ĨŝŶĂŶĐŝĂĐŝſŶ ŝŶǀĞƐƚŝŐĂĐŝſŶ ŵĞƚŽĚŽůŽŐşĂ ĂĚŵŝŶŝƐƚƌĂĐŝſŶ ĚĞů ƉƌŽLJĞĐƚŽ ƌĞĐƵƌƐŽƐƐƵƉĞƌǀŝƐŝſŶǀĂůŝĚĂĐŝſŶǀŝƐƵĂůŝnjĂĐŝſŶƌĞĚĂĐĐŝſŶͲƌĞǀŝƐŝſŶLJĞĚŝĐŝſŶ
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36 Ϯ KƐƚĂůĠͲsĂůƌŝďĞƌĂƐDĂƌƚşŶͲŽƌƌŝůůĂ^ĞŵƉĞƌĞͲsĂůǀĞƌĚĞ:'ĂƌĐşĂͲ'ſŵĞnj: ΘƐƉŝŶŽƐĂ&;ϮϬϮϰͿĐŽůŽŐŝĐĂůƐƵĐĐĞƐƐŝŽŶǁŝƚŚŝŶŵŝĐƌŽŚĂďŝƚĂƚƐ;ƚŝĚĞƉŽŽůƐͿĐƌĞĂƚĞĚ ŝŶ ƌŝƉƌĂƉƐƚƌƵĐƚƵƌĞƐ ŚŽƐƚŝŶŐ ĐůŝŵĂdž ĐŽŵŵƵŶŝƚŝĞƐ Ŷ ĞĐŽŶŽŵŝĐĂů ƐƚƌĂƚĞŐLJ ĨŽƌŵŝƚŝŐĂƚŝŶŐ ƚŚĞ ŶĞŐĂƚŝǀĞ ĞĨĨĞĐƚƐ ŽĨ ĐŽĂƐƚĂů ĚĞĨĞŶĐĞ ƐƚƌƵĐƚƵƌĞ ŽŶ ŵĂƌŝŶĞ ďŝŽĚŝǀĞƌƐŝƚLJĐŽůŽŐŝĐĂůĞŶŐŝŶĞĞƌŝŶŐϮϬϬϭϬϳͲϭϴϳ KƐƚĂůĠͲsĂůƌŝďĞƌĂƐ ĐŽŶĐĞƉƚƵĂůŝnjĂĐŝſŶ ĐŽŶƐĞƌǀĂĐŝſŶ ĚĞ ĚĂƚŽƐ ĂŶĄůŝƐŝƐ ĨŽƌŵĂů ŝŶǀĞƐƚŝŐĂĐŝſŶ ŵĞƚŽĚŽůŽŐşĂ ĂĚŵŝŶŝƐƚƌĂĐŝſŶ ĚĞů ƉƌŽLJĞĐƚŽ ƌĞĐƵƌƐŽƐ ƐƵƉĞƌǀŝƐŝſŶǀĂůŝĚĂĐŝſŶǀŝƐƵĂůŝnjĂĐŝſŶƌĞĚĂĐĐŝſŶͲďŽƌƌĂĚŽƌŽƌŝŐŝŶĂůƌĞĚĂĐĐŝſŶͲ ƌĞǀŝƐŝſŶLJĞĚŝĐŝſŶ DĂƌƚşŶͲŽƌƌŝůůĂ ĐŽŶƐĞƌǀĂĐŝſŶ ĚĞ ĚĂƚŽƐ ĂŶĄůŝƐŝƐ ĨŽƌŵĂů ŝŶǀĞƐƚŝŐĂĐŝſŶ ǀŝƐƵĂůŝnjĂĐŝſŶƌĞĚĂĐĐŝſŶͲďŽƌƌĂĚŽƌŽƌŝŐŝŶĂůƌĞĚĂĐĐŝſŶͲƌĞǀŝƐŝſŶLJĞĚŝĐŝſŶ ^ĞŵƉĞƌĞͲsĂůǀĞƌĚĞ:ĂŶĄůŝƐŝƐĨŽƌŵĂůŝŶǀĞƐƚŝŐĂĐŝſŶǀŝƐƵĂůŝnjĂĐŝſŶƌĞĚĂĐĐŝſŶͲ ƌĞǀŝƐŝſŶLJĞĚŝĐŝſŶ 'ĂƌĐşĂͲ'ſŵĞnj:ĂĚƋƵŝƐŝĐŝſŶĚĞĨŝŶĂŶĐŝĂĐŝſŶƌĞĐƵƌƐŽƐƌĞĚĂĐĐŝſŶͲƌĞǀŝƐŝſŶ LJĞĚŝĐŝſŶ ƐƉŝŶŽƐĂ & ĐŽŶĐĞƉƚƵĂůŝnjĂĐŝſŶ ŵĞƚŽĚŽůŽŐşĂ ƐƵƉĞƌǀŝƐŝſŶ ǀĂůŝĚĂĐŝſŶ ǀŝƐƵĂůŝnjĂĐŝſŶƌĞĚĂĐĐŝſŶͲƌĞǀŝƐŝſŶLJĞĚŝĐŝſŶ ϯ KƐƚĂůĠͲsĂůƌŝďĞƌĂƐ ^ĞŵƉĞƌĞͲsĂůǀĞƌĚĞ : WĂǀſŶͲWĂŶĞƋƵĞ ŽƉƉĂ ^ ƐƉŝŶŽƐĂ&Θ'ĂƌĐşĂͲ'ſŵĞnj:;ϮϬϮϮͿƌƚŝĨŝĐŝĂůŵĂƌŝŶĞŵŝĐƌŽͲƌĞƐĞƌǀĞƐĂƐĂŶĞǁ ĞĐŽƐLJƐƚĞŵͲďĂƐĞĚŵĂŶĂŐĞŵĞŶƚƚŽŽůĨŽƌŵĂƌŝŶĞĐŽŶƐĞƌǀĂƚŝŽŶdŚĞĐĂƐĞŽĨWĂƚĞůůĂ ĨĞƌƌƵŐŝŶĞĂ ;'ĂƐƚƌŽƉŽĚĂ WĂƚĞůůŝĚĂĞͿ ŽŶĞ ŽĨ ƚŚĞ ŵŽƐƚ ĞŶĚĂŶŐĞƌĞĚ ŵĂƌŝŶĞ ŝŶǀĞƌƚĞďƌĂƚĞƐŽĨƚŚĞDĞĚŝƚĞƌƌĂŶĞĂŶDĂƌŝŶĞWŽůŝĐLJϭϯϲϭϬϰϵϭϳ KƐƚĂůĠͲsĂůƌŝďĞƌĂƐĐŽŶƐĞƌǀĂĐŝſŶĚĞĚĂƚŽƐĂŶĄůŝƐŝƐĨŽƌŵĂůĂŶĄůŝƐŝƐĨŽƌŵĂů ŝŶǀĞƐƚŝŐĂĐŝſŶ ĂĚŵŝŶŝƐƚƌĂĐŝſŶ ĚĞů ƉƌŽLJĞĐƚŽ ƐƵƉĞƌǀŝƐŝſŶ ǀŝƐƵĂůŝnjĂĐŝſŶ ƌĞĚĂĐĐŝſŶͲďŽƌƌĂĚŽƌŽƌŝŐŝŶĂůƌĞĚĂĐĐŝſŶͲƌĞǀŝƐŝſŶLJĞĚŝĐŝſŶ ^ĞŵƉĞƌĞͲsĂůǀĞƌĚĞ:ĐŽŶƐĞƌǀĂĐŝſŶĚĞĚĂƚŽƐĂŶĄůŝƐŝƐĨŽƌŵĂůĂŶĄůŝƐŝƐĨŽƌŵĂů ŝŶǀĞƐƚŝŐĂĐŝſŶǀŝƐƵĂůŝnjĂĐŝſŶƌĞĚĂĐĐŝſŶͲƌĞǀŝƐŝſŶLJĞĚŝĐŝſŶ WĂǀſŶͲWĂŶĞƋƵĞĐŽŶƐĞƌǀĂĐŝſŶĚĞĚĂƚŽƐŝŶǀĞƐƚŝŐĂĐŝſŶƌĞĚĂĐĐŝſŶͲƌĞǀŝƐŝſŶ LJĞĚŝĐŝſŶ ŽƉƉĂ ^ ĐŽŶƐĞƌǀĂĐŝſŶ ĚĞ ĚĂƚŽƐ ŝŶǀĞƐƚŝŐĂĐŝſŶ ǀŝƐƵĂůŝnjĂĐŝſŶ ƌĞĚĂĐĐŝſŶͲ ƌĞǀŝƐŝſŶLJĞĚŝĐŝſŶ ƐƉŝŶŽƐĂ & ŵĞƚŽĚŽůŽŐşĂ ǀĂůŝĚĂĐŝſŶ ǀŝƐƵĂůŝnjĂĐŝſŶ ƌĞĚĂĐĐŝſŶͲƌĞǀŝƐŝſŶ LJ ĞĚŝĐŝſŶ 'ĂƌĐşĂͲ'ſŵĞnj : ĐŽŶĐĞƉƚƵĂůŝnjĂĐŝſŶ ĂĚƋƵŝƐŝĐŝſŶ ĚĞ ĨŝŶĂŶĐŝĂĐŝſŶ ŵĞƚŽĚŽůŽŐşĂ ƌĞĐƵƌƐŽƐ ƐƵƉĞƌǀŝƐŝſŶ ǀĂůŝĚĂĐŝſŶ ǀŝƐƵĂůŝnjĂĐŝſŶ ƌĞĚĂĐĐŝſŶͲ ƌĞǀŝƐŝſŶLJĞĚŝĐŝſŶ
37 Ϯ KƐƚĂůĠͲsĂůƌŝďĞƌĂƐDĂƌƚşŶͲŽƌƌŝůůĂ^ĞŵƉĞƌĞͲsĂůǀĞƌĚĞ:'ĂƌĐşĂͲ'ſŵĞnj: ΘƐƉŝŶŽƐĂ&;ϮϬϮϰͿĐŽůŽŐŝĐĂůƐƵĐĐĞƐƐŝŽŶǁŝƚŚŝŶŵŝĐƌŽŚĂďŝƚĂƚƐ;ƚŝĚĞƉŽŽůƐͿĐƌĞĂƚĞĚ ŝŶ ƌŝƉƌĂƉƐƚƌƵĐƚƵƌĞƐ ŚŽƐƚŝŶŐ ĐůŝŵĂdž ĐŽŵŵƵŶŝƚŝĞƐ Ŷ ĞĐŽŶŽŵŝĐĂů ƐƚƌĂƚĞŐLJ ĨŽƌŵŝƚŝŐĂƚŝŶŐ ƚŚĞ ŶĞŐĂƚŝǀĞ ĞĨĨĞĐƚƐ ŽĨ ĐŽĂƐƚĂů ĚĞĨĞŶĐĞ ƐƚƌƵĐƚƵƌĞ ŽŶ ŵĂƌŝŶĞ ďŝŽĚŝǀĞƌƐŝƚLJĐŽůŽŐŝĐĂůĞŶŐŝŶĞĞƌŝŶŐϮϬϬϭϬϳͲϭϴϳ KƐƚĂůĠͲsĂůƌŝďĞƌĂƐ ĐŽŶĐĞƉƚƵĂůŝnjĂĐŝſŶ ĐŽŶƐĞƌǀĂĐŝſŶ ĚĞ ĚĂƚŽƐ ĂŶĄůŝƐŝƐ ĨŽƌŵĂů ŝŶǀĞƐƚŝŐĂĐŝſŶ ŵĞƚŽĚŽůŽŐşĂ ĂĚŵŝŶŝƐƚƌĂĐŝſŶ ĚĞů ƉƌŽLJĞĐƚŽ ƌĞĐƵƌƐŽƐ ƐƵƉĞƌǀŝƐŝſŶǀĂůŝĚĂĐŝſŶǀŝƐƵĂůŝnjĂĐŝſŶƌĞĚĂĐĐŝſŶͲďŽƌƌĂĚŽƌŽƌŝŐŝŶĂůƌĞĚĂĐĐŝſŶͲ ƌĞǀŝƐŝſŶLJĞĚŝĐŝſŶ DĂƌƚşŶͲŽƌƌŝůůĂ ĐŽŶƐĞƌǀĂĐŝſŶ ĚĞ ĚĂƚŽƐ ĂŶĄůŝƐŝƐ ĨŽƌŵĂů ŝŶǀĞƐƚŝŐĂĐŝſŶ ǀŝƐƵĂůŝnjĂĐŝſŶƌĞĚĂĐĐŝſŶͲďŽƌƌĂĚŽƌŽƌŝŐŝŶĂůƌĞĚĂĐĐŝſŶͲƌĞǀŝƐŝſŶLJĞĚŝĐŝſŶ ^ĞŵƉĞƌĞͲsĂůǀĞƌĚĞ:ĂŶĄůŝƐŝƐĨŽƌŵĂůŝŶǀĞƐƚŝŐĂĐŝſŶǀŝƐƵĂůŝnjĂĐŝſŶƌĞĚĂĐĐŝſŶͲ ƌĞǀŝƐŝſŶLJĞĚŝĐŝſŶ 'ĂƌĐşĂͲ'ſŵĞnj:ĂĚƋƵŝƐŝĐŝſŶĚĞĨŝŶĂŶĐŝĂĐŝſŶƌĞĐƵƌƐŽƐƌĞĚĂĐĐŝſŶͲƌĞǀŝƐŝſŶ LJĞĚŝĐŝſŶ ƐƉŝŶŽƐĂ & ĐŽŶĐĞƉƚƵĂůŝnjĂĐŝſŶ ŵĞƚŽĚŽůŽŐşĂ ƐƵƉĞƌǀŝƐŝſŶ ǀĂůŝĚĂĐŝſŶ ǀŝƐƵĂůŝnjĂĐŝſŶƌĞĚĂĐĐŝſŶͲƌĞǀŝƐŝſŶLJĞĚŝĐŝſŶ ϯ KƐƚĂůĠͲsĂůƌŝďĞƌĂƐ ^ĞŵƉĞƌĞͲsĂůǀĞƌĚĞ : WĂǀſŶͲWĂŶĞƋƵĞ ŽƉƉĂ ^ ƐƉŝŶŽƐĂ&Θ'ĂƌĐşĂͲ'ſŵĞnj:;ϮϬϮϮͿƌƚŝĨŝĐŝĂůŵĂƌŝŶĞŵŝĐƌŽͲƌĞƐĞƌǀĞƐĂƐĂŶĞǁ ĞĐŽƐLJƐƚĞŵͲďĂƐĞĚŵĂŶĂŐĞŵĞŶƚƚŽŽůĨŽƌŵĂƌŝŶĞĐŽŶƐĞƌǀĂƚŝŽŶdŚĞĐĂƐĞŽĨWĂƚĞůůĂ ĨĞƌƌƵŐŝŶĞĂ ;'ĂƐƚƌŽƉŽĚĂ WĂƚĞůůŝĚĂĞͿ ŽŶĞ ŽĨ ƚŚĞ ŵŽƐƚ ĞŶĚĂŶŐĞƌĞĚ ŵĂƌŝŶĞ ŝŶǀĞƌƚĞďƌĂƚĞƐŽĨƚŚĞDĞĚŝƚĞƌƌĂŶĞĂŶDĂƌŝŶĞWŽůŝĐLJϭϯϲϭϬϰϵϭϳ KƐƚĂůĠͲsĂůƌŝďĞƌĂƐĐŽŶƐĞƌǀĂĐŝſŶĚĞĚĂƚŽƐĂŶĄůŝƐŝƐĨŽƌŵĂůĂŶĄůŝƐŝƐĨŽƌŵĂů ŝŶǀĞƐƚŝŐĂĐŝſŶ ĂĚŵŝŶŝƐƚƌĂĐŝſŶ ĚĞů ƉƌŽLJĞĐƚŽ ƐƵƉĞƌǀŝƐŝſŶ ǀŝƐƵĂůŝnjĂĐŝſŶ ƌĞĚĂĐĐŝſŶͲďŽƌƌĂĚŽƌŽƌŝŐŝŶĂůƌĞĚĂĐĐŝſŶͲƌĞǀŝƐŝſŶLJĞĚŝĐŝſŶ ^ĞŵƉĞƌĞͲsĂůǀĞƌĚĞ:ĐŽŶƐĞƌǀĂĐŝſŶĚĞĚĂƚŽƐĂŶĄůŝƐŝƐĨŽƌŵĂůĂŶĄůŝƐŝƐĨŽƌŵĂů ŝŶǀĞƐƚŝŐĂĐŝſŶǀŝƐƵĂůŝnjĂĐŝſŶƌĞĚĂĐĐŝſŶͲƌĞǀŝƐŝſŶLJĞĚŝĐŝſŶ WĂǀſŶͲWĂŶĞƋƵĞĐŽŶƐĞƌǀĂĐŝſŶĚĞĚĂƚŽƐŝŶǀĞƐƚŝŐĂĐŝſŶƌĞĚĂĐĐŝſŶͲƌĞǀŝƐŝſŶ LJĞĚŝĐŝſŶ ŽƉƉĂ ^ ĐŽŶƐĞƌǀĂĐŝſŶ ĚĞ ĚĂƚŽƐ ŝŶǀĞƐƚŝŐĂĐŝſŶ ǀŝƐƵĂůŝnjĂĐŝſŶ ƌĞĚĂĐĐŝſŶͲ ƌĞǀŝƐŝſŶLJĞĚŝĐŝſŶ ƐƉŝŶŽƐĂ & ŵĞƚŽĚŽůŽŐşĂ ǀĂůŝĚĂĐŝſŶ ǀŝƐƵĂůŝnjĂĐŝſŶ ƌĞĚĂĐĐŝſŶͲƌĞǀŝƐŝſŶ LJ ĞĚŝĐŝſŶ 'ĂƌĐşĂͲ'ſŵĞnj : ĐŽŶĐĞƉƚƵĂůŝnjĂĐŝſŶ ĂĚƋƵŝƐŝĐŝſŶ ĚĞ ĨŝŶĂŶĐŝĂĐŝſŶ ŵĞƚŽĚŽůŽŐşĂ ƌĞĐƵƌƐŽƐ ƐƵƉĞƌǀŝƐŝſŶ ǀĂůŝĚĂĐŝſŶ ǀŝƐƵĂůŝnjĂĐŝſŶ ƌĞĚĂĐĐŝſŶͲ ƌĞǀŝƐŝſŶLJĞĚŝĐŝſŶ ϰ KƐƚĂůĠͲsĂůƌŝďĞƌĂƐ ^ĂďŝŶŽͲ>ŽƌĞŶnjŽ ůŝͲŚŵĞĚ WĂǀſŶͲWĂŶĞƋƵĞ ^ĞŵƉĞƌĞͲsĂůǀĞƌĚĞ : ƐƉŝŶŽƐĂ & Θ 'ĂƌĐşĂͲ'ſŵĞnj : ;ϮϬϮϯͿ tŚĞŶ ƚŚĞ ƉŽƉƵůĂƚŝŽŶŽĨĂŶĞŶĚĂŶŐĞƌĞĚŵĂƌŝŶĞŵŽůůƵƐĐ;WĂƚĞůůĂĨĞƌƌƵŐŝŶĞĂͿŝŶĐƌĞĂƐĞƐĂůŵŽƐƚ ƚŚƌĞĞͲĨŽůĚŝŶƚĞŶLJĞĂƌƐZĞĂůŝƚLJŽƌĨŝĐƚŝŽŶ&ƌŽŶƚŝĞƌƐŝŶDĂƌŝŶĞ^ĐŝĞŶĐĞ KƐƚĂůĠͲsĂůƌŝďĞƌĂƐ ĐŽŶĐĞƉƚƵĂůŝnjĂĐŝſŶ ĂŶĄůŝƐŝƐ ĨŽƌŵĂů ĂĚƋƵŝƐŝĐŝſŶ ĚĞ ĨŝŶĂŶĐŝĂĐŝſŶ ŝŶǀĞƐƚŝŐĂĐŝſŶ ŵĞƚŽĚŽůŽŐşĂ ĂĚŵŝŶŝƐƚƌĂĐŝſŶ ĚĞů ƉƌŽLJĞĐƚŽ ƌĞĐƵƌƐŽƐƐƵƉĞƌǀŝƐŝſŶǀĂůŝĚĂĐŝſŶǀŝƐƵĂůŝnjĂĐŝſŶƌĞĚĂĐĐŝſŶͲďŽƌƌĂĚŽƌŽƌŝŐŝŶĂů ƌĞĚĂĐĐŝſŶͲƌĞǀŝƐŝſŶLJĞĚŝĐŝſŶ ^ĂďŝŶŽͲ>ŽƌĞŶnjŽ ĐŽŶƐĞƌǀĂĐŝſŶ ĚĞ ĚĂƚŽƐ ĂŶĄůŝƐŝƐ ĨŽƌŵĂů ŝŶǀĞƐƚŝŐĂĐŝſŶ ƌĞĚĂĐĐŝſŶͲƌĞǀŝƐŝſŶLJĞĚŝĐŝſŶ ůŝͲŚŵĞĚĐŽŶƐĞƌǀĂĐŝſŶĚĞĚĂƚŽƐŝŶǀĞƐƚŝŐĂĐŝſŶ WĂǀſŶͲWĂŶĞƋƵĞĐŽŶƐĞƌǀĂĐŝſŶĚĞĚĂƚŽƐŝŶǀĞƐƚŝŐĂĐŝſŶƌĞĚĂĐĐŝſŶͲƌĞǀŝƐŝſŶ LJĞĚŝĐŝſŶ ^ĞŵƉĞƌĞͲsĂůǀĞƌĚĞ : ĐŽŶƐĞƌǀĂĐŝſŶ ĚĞ ĚĂƚŽƐ ŝŶǀĞƐƚŝŐĂĐŝſŶ ŵĞƚŽĚŽůŽŐşĂ ǀŝƐƵĂůŝnjĂĐŝſŶƌĞĚĂĐĐŝſŶͲƌĞǀŝƐŝſŶLJĞĚŝĐŝſŶ ƐƉŝŶŽƐĂ &ŵĞƚŽĚŽůŽŐşĂƐƵƉĞƌǀŝƐŝſŶǀĂůŝĚĂĐŝſŶǀŝƐƵĂůŝnjĂĐŝſŶƌĞĚĂĐĐŝſŶͲ ƌĞǀŝƐŝſŶLJĞĚŝĐŝſŶ 'ĂƌĐşĂͲ'ſŵĞnj : ĂĚƋƵŝƐŝĐŝſŶ ĚĞ ĨŝŶĂŶĐŝĂĐŝſŶ ŵĞƚŽĚŽůŽŐşĂ ƌĞĐƵƌƐŽƐ ƐƵƉĞƌǀŝƐŝſŶǀĂůŝĚĂĐŝſŶǀŝƐƵĂůŝnjĂĐŝſŶƌĞĚĂĐĐŝſŶͲƌĞǀŝƐŝſŶLJĞĚŝĐŝſŶ
38 /E&KZD/ZdKZ^^KZ>KEdZ/h/MEhEK>K^hdKZ^ >K^dZ:K^Wh>/K^ ƌ&ƌĞĞƐƉŝŶŽƐĂdŽƌƌĞLJƌ:ŽƐĠĂƌůŽƐ'ĂƌĐşĂ'ſŵĞnj ĞƌƚŝĨŝĐĂŶ YƵĞůĂƐĨƵŶĐŝŽŶĞƐƋƵĞŚĂŶĚĞƐĞŵƉĞŹĂĚŽůŽƐĚŝƐƚŝŶƚŽƐĐŽůĂďŽƌĂĚŽƌĞƐĞŶůŽƐĐƵĂƚƌŽ ĂƌƚşĐƵůŽƐƋƵĞĐŽŶĨŽƌŵĂŶůĂƉƌĞƐĞŶƚĞƚĞƐŝƐĚŽĐƚŽƌĂůƐĞŚĂĞdžƉƵĞƐƚŽĐŽƌƌĞĐƚĂŵĞŶƚĞĞŶĞů ĂƉĂƌƚĂĚŽȇs/ŶĨŽƌŵĞĚĞůŽƐĚŝƌĞĐƚŽƌĞƐƐŽďƌĞůĂĐŽŶƚƌŝďƵĐŝſŶĚĞĐĂĚĂƵŶŽĚĞůŽƐĂƵƚŽƌĞƐ Ă ůŽƐ ƚƌĂďĂũŽƐ ƉƵďůŝĐĂĚŽƐ ƐĞŐƷŶ ůĂ ĐĂƚĞŐŽƌŝnjĂĐŝſŶ ĚĞ ZĞĚĚŝd ;ŽŶƚƌŝďƵƚŽƌ ZŽůĞƐ dĂdžŽŶŽŵLJͿ sǑǑĚĞůŽƐĚŝƌĞĐƚŽƌĞƐ &ĚŽ&ƌĞĞƐƉŝŶŽƐĂdŽƌƌĞ&ĚŽ:ŽƐĠĂƌůŽƐ'ĂƌĐşĂ'ſŵĞnj /E&KZD>K^KhdKZ^EKKdKZ^^KZ>ZEhE/WZ^EdZ ^dK^dZ:K^KDKWZdhEd^/^WKZKDWE/K ůƚĂŝWĂǀſŶͲWĂŶĞƋƵĞůǀĂƌŽ^ĂďŝŶŽͲ>ŽƌĞŶnjŽďĚĞƌƌĂŚŵĂŶůŝ ŚŵĞĚLJŶƚŽŶŝŽDĂƌƚşŶŽƌƌŝůůĂ ĞƌƚŝĨŝĐĂŶ YƵĞƌĞŶƵŶĐŝĂŶĂĚĞƐƚŝŶĂƌůĂƐƉƵďůŝĐĂĐŝŽŶĞƐƋƵĞĐŽŶƐƚŝƚƵLJĞŶůĂƚĞƐŝƐĚŽĐƚŽƌĂůƚŝƚƵůĂĚĂ “HERRAMIENTAS DE GESTIÓN PARA LA REGENERACIÓN DE LA BIODIVERSIDAD MARINA AUTÓCTONA EN LITORALES URBANIZADOS”, del Programa de Doctorado en Biología /ŶƚĞŐƌĂĚĂ ĞŶ ůĂ ůşŶĞĂ ĚĞ ŝŶǀĞƐƚŝŐĂĐŝſŶ ĚĞ ŝŽůŽŐşĂ ŶŝŵĂů &ŝƐŝŽůŽŐşĂ ŝŽƚĞĐŶŽůŽŐşĂ ŝŽĚŝǀĞƌƐŝĚĂĚǀŽůƵĐŝſŶLJŽŶƐĞƌǀĂĐŝſŶĚĞůĂhŶŝǀĞƌƐŝĚĂĚĚĞ^ĞǀŝůůĂĐŽŵŽƉĂƌƚĞĚĞƵŶĂ ĨƵƚƵƌĂƚĞƐŝƐĚŽĐƚŽƌĂůƉŽƌĐŽŵƉĞŶĚŝŽĚĞƉƵďůŝĐĂĐŝŽŶĞƐ ^ĞǀŝůůĂĂďƌŝůĚĞϮϬϮϰ
39 s/ /E&KZD >K^ KhdKZ^ EK KdKZ^ ^KZ > ZEhE/ WZ^Ed^dK^dZ:K^KDKWZdhEd^/^WKZKDWE/K /E&KZD>K^KhdKZ^EKKdKZ^^KZ>ZEhE/WZ^EdZ ^dK^dZ:K^KDKWZdhEd^/^WKZKDWE/K ůƚĂŝWĂǀſŶͲWĂŶĞƋƵĞůǀĂƌŽ^ĂďŝŶŽͲ>ŽƌĞŶnjŽďĚĞƌƌĂŚŵĂŶůŝ ŚŵĞĚLJŶƚŽŶŝŽDĂƌƚşŶŽƌƌŝůůĂ ĞƌƚŝĨŝĐĂŶ YƵĞƌĞŶƵŶĐŝĂŶĂĚĞƐƚŝŶĂƌůĂƐƉƵďůŝĐĂĐŝŽŶĞƐƋƵĞĐŽŶƐƚŝƚƵLJĞŶůĂƚĞƐŝƐĚŽĐƚŽƌĂůƚŝƚƵůĂĚĂ “HERRAMIENTAS DE GESTIÓN PARA LA REGENERACIÓN DE LA BIODIVERSIDAD MARINA AUTÓCTONA EN LITORALES URBANIZADOS”, del Programa de Doctorado en Biología /ŶƚĞŐƌĂĚĂ ĞŶ ůĂ ůşŶĞĂ ĚĞ ŝŶǀĞƐƚŝŐĂĐŝſŶ ĚĞ ŝŽůŽŐşĂ ŶŝŵĂů &ŝƐŝŽůŽŐşĂ ŝŽƚĞĐŶŽůŽŐşĂ ŝŽĚŝǀĞƌƐŝĚĂĚǀŽůƵĐŝſŶLJŽŶƐĞƌǀĂĐŝſŶĚĞůĂhŶŝǀĞƌƐŝĚĂĚĚĞ^ĞǀŝůůĂĐŽŵŽƉĂƌƚĞĚĞƵŶĂ ĨƵƚƵƌĂƚĞƐŝƐĚŽĐƚŽƌĂůƉŽƌĐŽŵƉĞŶĚŝŽĚĞƉƵďůŝĐĂĐŝŽŶĞƐ ^ĞǀŝůůĂĂďƌŝůĚĞϮϬϮϰ sǑǑĚĞůŽƐĐŽĂƵƚŽƌĞƐ &ĚŽůƚŝĂWĂǀſŶWĂŶĞƋƵĞ &ĚŽůǀĂƌŽ^ĂďŝŶŽͲ>ŽƌĞŶnjŽ &ĚŽďĚĞƌƌĂŚŵĂŶůŝŚŵĞĚ &ĚŽŶƚŽŶŝŽDĂƌƚşŶŽƌƌŝůůĂ ůŝŶƚĞƌĞƐĂĚŽ &ĚŽŶƌŝƋƵĞKƐƚĂůĠsĂůƌŝďĞƌĂƐ sǑǑĚĞůŽƐĐŽĂƵƚŽƌĞƐ &ĚŽůƚŝĂWĂǀſŶWĂŶĞƋƵĞ&ĚŽůǀĂƌŽ^ĂďŝŶŽͲ>ŽƌĞŶnjŽ &ĚŽďĚĞƌƌĂŚŵĂŶůŝŚŵĞĚ &ĚŽŶƚŽŶŝŽDĂƌƚşŶŽƌƌŝůůĂ ůŝŶƚĞƌĞƐĂĚŽ &ĚŽŶƌŝƋƵĞKƐƚĂůĠsĂůƌŝďĞƌĂƐ sǑǑĚĞůŽƐĐŽĂƵƚŽƌĞƐ &ĚŽůƚŝĂWĂǀſŶWĂŶĞƋƵĞ&ĚŽůǀĂƌŽ^ĂďŝŶŽͲ>ŽƌĞŶnjŽ &ĚŽďĚĞƌƌĂŚŵĂŶůŝŚŵĞĚ&ĚŽŶƚŽŶŝŽDĂƌƚşŶŽƌƌŝůůĂ ůŝŶƚĞƌĞƐĂĚŽ &ĚŽŶƌŝƋƵĞKƐƚĂůĠsĂůƌŝďĞƌĂƐ
40 WZKzdKd^/^KdKZ>
41 WZKzdKd^/^KdKZ> //EdZKh/ME'EZ> ůȇ,ŽůŽĐĞŶŽȇ(del griego holos, todo, y kainos, reciente) ĞƐĞůƚĠƌŵŝŶŽĐŽŶĞůƋƵĞ ƐĞ ĚĞƐŝŐŶĂ ůĂ ƷůƚŝŵĂ LJ ĂĐƚƵĂů ĠƉŽĐĂ ŐĞŽůſŐŝĐĂ ĚĞů ƉůĂŶĞƚĂ dŝĞƌƌĂ ƉŽƌ ůĂ ĐŽŵƵŶŝĚĂĚ ĐŝĞŶƚşĨŝĐĂĚĞůĂŽŵŝƐŝſŶ/ŶƚĞƌŶĂĐŝŽŶĂůĚĞƐƚƌĂƚŝŐƌĂĨşĂ;Ž/ŶƚĞƌŶĂƚŝŽŶĂůŽŵŵŝƐƐŝŽŶŽŶ ^ƚƌĂƚŝŐƌĂƉŚLJ/^ͿůƚĠƌŵŝŶŽĨƵĞĂĐƵŹĂĚŽƉŽƌŚĂƌůĞƐ>LJĞůůĞŶϭϴϯϯƉĂƌĂƌĞĨĞƌŝƌƐĞĂů ĂĐƚƵĂůƉĞƌŝŽĚŽĐĄůŝĚŽƚƌĂƐůĂƷůƚŝŵĂŐůĂĐŝĂĐŝſŶLJĨƵĞĂĚŽƉƚĂĚŽĐŽŵŽƵŶŝĚĂĚĚĞůĂĞƐĐĂůĂ ŝŶƚĞƌŶĂĐŝŽŶĂů ĚĞ ƚŝĞŵƉŽ ŐĞŽůſŐŝĐŽ ƉŽƌ Ğů ŽŶŐƌĞƐŽ 'ĞŽůſŐŝĐŽ /ŶƚĞƌŶĂĐŝŽŶĂů ĚĞ ϭϴϴϱ ;ĂůďLJϮϬϭϲͿ ŶůĂƐƷůƚŝŵĂƐĚĠĐĂĚĂƐƉĂƌƚĞĚĞůĂĐŽŵƵŶŝĚĂĚĐŝĞŶƚşĨŝĐĂŚĂƉƌŽƉƵĞƐƚŽůĂĐƌĞĂĐŝſŶ ĚĞ ƵŶĂ ŶƵĞǀĂ ĠƉŽĐĂ ŐĞŽůſŐŝĐĂ ƉĂƌĂ ƐƵĐĞĚĞƌ Ă ůĂ ƐĞƌŝĞ Ž ĠƉŽĐĂ ĚĞů ,ŽůŽĐĞŶŽ Ğů ȇŶƚƌŽƉŽĐĞŶŽȇ(del griego ἄνθρωπος anthropos, 'ser humano', y καινός kainos, 'nuevo') ƐƚĂ ƉƌŽƉƵĞƐƚĂ ƐĞ ĨŽĐĂůŝnjĂ ĞŶ Ğů ŝŵƉĂĐƚŽ ŐůŽďĂů ƋƵĞ ůĂƐ ĂĐƚŝǀŝĚĂĚĞƐ ŚƵŵĂŶĂƐ ĞƐƚĄŶ ƚĞŶŝĞŶĚŽ ĞŶ ůĂ ŐĞŽůŽŐşĂ LJ ĞĐŽůŽŐşĂ ƚĞƌƌĞƐƚƌĞ ƉƌŽǀŽĐĂŶĚŽ ůĂĚĞŶŽŵŝŶĂĚĂ ȇĞdžƚŝŶĐŝſŶ ŵĂƐŝǀĂĚĞů,ŽůŽĐĞŶŽȇŽȇƐĞdžƚĂĞdžƚŝŶĐŝſŶŵĂƐŝǀĂȇĚĞĞƐƉĞĐŝĞƐ;ƌƵƚnjĞŶLJ^ƚŽĞƌŵĞƌϮϬϬϬ <ŽůďĞƌƚϮϬϭϰͿ ĞŶƚƌĂŶĚŽ ůŽƐ ŝŵƉĂĐƚŽƐ ŚƵŵĂŶŽƐ ĞŶ ůŽƐ ĞĐŽƐŝƐƚĞŵĂƐ ĐŽƐƚĞƌŽƐ ƐĞ ŚĂŶ ŝĚĞŶƚŝĨŝĐĂĚŽůĂƐŽďƌĞĞdžƉůŽƚĂĐŝſŶůĂĐŽŶƚĂŵŝŶĂĐŝſŶůĂĚĞƐƚƌƵĐĐŝſŶĐŽƐƚĞƌĂůĂƐŝŶǀĂƐŝŽŶĞƐ ďŝŽůſŐŝĐĂƐ LJ Ğů ĐĂŵďŝŽ ĐůŝŵĄƚŝĐŽ ĐŽŵŽ ůŽƐ ĐŝŶĐŽ ĞĨĞĐƚŽƐ ĚĞ ŵĂLJŽƌ ĚĞŐĞŶĞƌĂĐŝſŶ LJ ĚĞƚĞƌŝŽƌŽĞŶůĂƐnjŽŶĂƐůŝƚŽƌĂůĞƐ;:ĂĐŬƐŽŶĞƚĂůϮϬϬϭWƌŽďĞƌƚϮϬϭϳͿůůŽƐĞĞŶƚŝĞŶĚĞĐŽŶ ĚĂƚŽƐĐŽŵŽƋƵĞůĂƐŝƵĚĂĚĞƐLJŐůŽŵĞƌĂĐŝŽŶĞƐŽƐƚĞƌĂƐ;ͿĞŶƚŽĚŽĞůŵƵŶĚŽƐĞŚĂŶ ŵƵůƚŝƉůŝĐĂĚŽ ƉŽƌ ϰϱ ĚĞƐĚĞ ϭϵϰϱ ;ĂƌƌĂŐĄŶ LJ ĚĞ ŶĚƌĠƐ ϮϬϭϱͿ >ĂƐ njŽŶĂƐ ĐŽƐƚĞƌĂƐ ĂůďĞƌŐĂŶůĂŵŝƚĂĚĚĞůĂƐĐŝƵĚĂĚĞƐĚĞůŵƵŶĚŽLJŵĄƐĚĞůĂŵŝƚĂĚĚĞůĂƉŽďůĂĐŝſŶŵƵŶĚŝĂů ĐŽŶƵŶĂĚĞŶƐŝĚĂĚĚĞƉŽďůĂĐŝſŶĐĞƌĐĂĚĞůĂĐŽƐƚĂƚƌĞƐǀĞĐĞƐƐƵƉĞƌŝŽƌĂůĂŵĞĚŝĂŵƵŶĚŝĂů ;ƌĞĞůϮϬϬϯ^ŵĂůůLJEŝĐŚŽůůƐϮϬϬϯ'ŝďƐŽŶĞƚĂůϮϬϬϳͿ ŶnjŽŶĂƐĚĞůůŝƚŽƌĂůĚĞŶƐĂŵĞŶƚĞƉŽďůĂĚĂƐĞůƐƵƐƚƌĂƚŽĂƌƚŝĨŝĐŝĂůĞŶůĂĐŽƐƚĂƉƵĞĚĞ ƌĞƉƌĞƐĞŶƚĂƌŵĄƐĚĞůϱϬйĚĞůůŝƚŽƌĂů;ĞŶĐŝŶŝϭϵϵϴĂĨĨŽƌŶĞƚĂůϮϬϭϱĂͿŶŝǀĞůŵƵŶĚŝĂů ƐĞŽďƐĞƌǀĂŶĐŝĞƌƚĂƐnjŽŶĂƐŐĞŽŐƌĄĨŝĐĂƐĐŽŶĐŽƐƚĂƐĂŵƉůŝĂŵĞŶƚĞƵƌďĂŶŝnjĂĚĂƐĐŽŵŽƉƵĞĚĞ ƐĞƌ Ğů ĐĂƐŽ ĚĞ ƐƚĂĚŽƐ hŶŝĚŽƐ ĞŶ Ğů ƋƵĞ Ğů ϭϰй ĚĞƐƵ ůŝƚŽƌĂů ĞƐƚĄ ĐŽŶƐƚƌƵŝĚŽ ĐŽŶ ĞƐƚƌƵĐƚƵƌĂƐĂƌƚŝĨŝĐŝĂůĞƐ;'ŝƚƚŵĂŶĞƚĂůϮϬϭϱͿŽĞůŵĂƌDĞĚŝƚĞƌƌĄŶĞŽƋƵĞƉƵĞĚĞůůĞŐĂƌĂů ϱϬйĚĞƐƵůŝƚŽƌĂů;^ĞůůĂΘWĞƌŬŽůͲ&ŝŶŬĞůϮϬϭϱͿŶƚƌĞůŽƐĚŝƐƚŝŶƚŽƐĂĐĐŝĚĞŶƚĞƐŐĞŽŐƌĄĨŝĐŽƐ ĐŽƐƚĞƌŽƐ ůĂƐ ůĂŐƵŶĂƐ ĐŽƐƚĞƌĂƐ ůŽƐ ĞƐƚƵĂƌŝŽƐ LJ ůĂƐ ďĂŚşĂƐ ƐŽŶ ůŽƐ ŵĄƐ ƵƌďĂŶŝnjĂĚŽƐ ƌĞƉƌĞƐĞŶƚĂŶĚŽĂƉƌŽdžŝŵĂĚĂŵĞŶƚĞĞůϯϬйŵŝĞŶƚƌĂƐƋƵĞůŽƐĂĐĂŶƚŝůĂĚŽƐLJůŽƐŐůĂĐŝĂƌĞƐ ƐŽŶůŽƐƋƵĞƚŝĞŶĞŶůĂŵĞŶŽƌĐŽďĞƌƚƵƌĂĚĞƐƵƐƚƌĂƚŽĂƌƚŝĨŝĐŝĂůƐĞŐƷŶ^ĞŵƉĞƌĞͲsĂůǀĞƌĚĞĞƚ Ăů;ϮϬϮϯͿƚĞŶĚŝĞŶĚŽĂůĂƌŝƋƵĞnjĂĚĞůŽƐĚŝƐƚŝŶƚŽƐƉĂşƐĞƐƐĞŚĂĚĞŵŽƐƚƌĂĚŽƋƵĞĂƋƵĞůůŽƐ ĐŽŶƌĞŶƚĂĂůƚĂLJŵĞĚŝĂͲĂůƚĂƚŝĞŶĞŶƵŶĂĐŽďĞƌƚƵƌĂĂƌƚŝĨŝĐŝĂůƐƵƉĞƌŝŽƌĂůĂĚĞůŽƐƉĂşƐĞƐĚĞ ƌĞŶƚĂďĂũĂLJŵĞĚŝĂͲďĂũĂ;^ĞŵƉĞƌĞͲsĂůǀĞƌĚĞĞƚĂůϮϬϮϯͿ
48 //K:d/sK^,/WMd^/^ WƵďůŝĐĂĐŝſŶ ϭ ƌĞĂĐŝſŶ ĚĞ ŵŝĐƌŽŚĄďŝƚĂƚƐ ;ƉŽnjĂƐ ŝŶƚĞƌŵĂƌĞĂůĞƐͿ ĞŶ ĞƐĐŽůůĞƌĂƐ ĐŽŶ ĐŽŵƵŶŝĚĂĚĞƐďŝŽůſŐŝĐĂƐĞŶĞƚĂƉĂĐůşŵĂdžĚĞƐƵƐƵĐĞƐŝſŶĞĐŽůſŐŝĐĂĐŽŵŽĨŽƌŵĂĚĞŵŝƚŝŐĂƌ ůŽƐĞĨĞĐƚŽƐŶĞŐĂƚŝǀŽƐĚĞůƐƵƐƚƌĂƚŽĂƌƚŝĨŝĐŝĂůƐŽďƌĞůĂďŝŽĚŝǀĞƌƐŝĚĂĚŵĂƌŝŶĂ ĂĚĂ ůĂ ĚŝƐŵŝŶƵĐŝſŶ ĚĞ ŚĄďŝƚĂƚƐ ĐŽƐƚĞƌŽƐ ŽĐĂƐŝŽŶĂĚĂ ƉŽƌ ůĂ ĐŽŶƐƚƌƵĐĐŝſŶ ĚĞ ĞƐƚƌƵĐƚƵƌĂƐĂƌƚŝĨŝĐŝĂůĞƐƉĂƌĂƐĂƚŝƐĨĂĐĞƌůĂƐĚĞŵĂŶĚĂƐĚĞůĚĞƐĂƌƌŽůůŽƵƌďĂŶŽĞƐŝŵƉĞƌĂƚŝǀŽ ĚŝƐĞŹĂƌ ĞƐƚĂƐ ĞƐƚƌƵĐƚƵƌĂƐ ƚĞŶŝĞŶĚŽ ĞŶ ĐƵĞŶƚĂ ƉƌŝŶĐŝƉŝŽƐ ĞĐŽůſŐŝĐŽƐ ĐŽŶ Ğů ĨŝŶ ĚĞ ŵŝŶŝŵŝnjĂƌƐƵŝŵƉĂĐƚŽĞŶĞůĞŶƚŽƌŶŽŶĂƚƵƌĂůĂƐşĐŽŵŽĞǀĂůƵĂƌĐŽŵƉƌĞŶĚĞƌLJĐƵĂŶƚŝĨŝĐĂƌ ĞůĞƐƚĂĚŽĚĞĞƐƚŽƐŚĄďŝƚĂƚƐWŽƌůŽƚĂŶƚŽůŽƐŽďũĞƚŝǀŽƐĚĞůĂƉƌĞƐĞŶƚĞŝŶǀĞƐƚŝŐĂĐŝſŶƐŽŶ ŝͿĞǀĂůƵĂƌƐŝůĂĐƌĞĂĐŝſŶĚĞƉŽnjĂƐŝŶƚĞƌŵĂƌĞĂůĞƐĞŶĞƐƚƌƵĐƚƵƌĂƐĚĞĚĞĨĞŶƐĂĐŽƐƚĞƌĂĚĞ ĞƐĐŽůůĞƌĂƐ ĚŽůŽŵşƚŝĐĂƐ ĐŽŶ ĐŽŵƵŶŝĚĂĚĞƐ ĐůşŵĂdž ĐŽŶƚƌŝďƵLJĞ Ăů ĂƵŵĞŶƚŽ ĚĞ ůĂ ďŝŽĚŝǀĞƌƐŝĚĂĚůŽĐĂůŝŝͿĂŶĂůŝnjĂƌĞůĞĨĞĐƚŽƐŽďƌĞĞůŚĂůŽƉĞƌŝŵĞƚƌĂůĂĚLJĂĐĞŶƚĞĂůĂƉŽnjĂŝŝŝͿ ǀĞƌŝĨŝĐĂƌ ĐŽŶĨŽƌŵĞ Ă ŝŶǀĞƐƚŝŐĂĐŝŽŶĞƐ ƉƌĞǀŝĂƐ ĞŶ ŽƚƌĂƐ ƌĞŐŝŽŶĞƐ ĚĞů ŵƵŶĚŽ Ɛŝ ůĂƐ ĞƐƚƌƵĐƚƵƌĂƐĂƌƚŝĨŝĐŝĂůĞƐĞŶĞƵƚĂĂůďĞƌŐĂŶĐŽŵƵŶŝĚĂĚĞƐŵĞŶŽƐĚŝǀĞƌƐĂƐƋƵĞůĂƐĄƌĞĂƐ ŶĂƚƵƌĂůĞƐ ĐŝƌĐƵŶĚĂŶƚĞƐ ĞŶ Ğů ŵĞĚŝŽ ŝŶƚĞƌŵĂƌĞĂů ŝǀͿ ĞdžƉůŽƌĂƌ ƋƵĠ ĞƐƉĞĐŝĞƐ ƐĞ ďĞŶĞĨŝĐŝĂƌŽŶ ĚŝƌĞĐƚĂŵĞŶƚĞ ĚĞů ŶƵĞǀŽ ŵŝĐƌŽŚĄďŝƚĂƚ ĐƌĞĂĚŽ LJ ǀͿ ĚĞƐĐƌŝďŝƌ ůĂƐ ĐŽŵƵŶŝĚĂĚĞƐďŝŽůſŐŝĐĂƐĚĞĞƐƚĞƚŝƉŽĚĞŵŝĐƌŽŚĄďŝƚĂƚƐĚĞŶƚƌŽĚĞůŵĞĚŝŽŶĂƚƵƌĂů WƵďůŝĐĂĐŝſŶ Ϯ ^ƵĐĞƐŝſŶ ĞĐŽůſŐŝĐĂ ĚĞ ůĂ ĐŽŵƵŶŝĚĂĚ ďŝŽůſŐŝĐĂ ĂƐĞŶƚĂĚĂ ĞŶ ƉŽnjĂƐ ŝŶƚĞƌŵĂƌĞĂůĞƐ ĐƌĞĂĚĂƐ ĞŶ ĞƐƚƌƵĐƚƵƌĂƐ ĚĞ ƉƌŽƚĞĐĐŝſŶ ĐŽƐƚĞƌĂƐ ;ϳϱ ĂŹŽƐ ĚĞ ŵŽŶŝƚŽƌŝnjĂĐŝſŶͿ ůŽďũĞƚŝǀŽĚĞůƉƌĞƐĞŶƚĞĞƐƚƵĚŝŽĞƐĂŶĂůŝnjĂƌůĂƐĚŝƐƚŝŶƚĂƐĞƚĂƉĂƐĚĞůĂƐƵĐĞƐŝſŶ ĞĐŽůſŐŝĐĂƋƵĞŚĂĞdžƉĞƌŝŵĞŶƚĂĚŽĞůďŝŽƚŽƉŽĚĞůĂƐƉŽnjĂƐŝŶƚĞƌŵĂƌĞĂůĞƐĐƌĞĂĚĂƐĞŶůĂƐ ĞƐƚƌƵĐƚƵƌĂƐĚĞƉƌŽƚĞĐĐŝſŶĐŽƐƚĞƌĂƐĂƐşĐŽŵŽǀĂůŽƌĂƌƐŝĞůŵŝĐƌŽŚĄďŝƚĂƚĐŽŶƚƌŝďƵLJĞĂů ĂƵŵĞŶƚŽĚĞůĂďŝŽĚŝǀĞƌƐŝĚĂĚůŽĐĂůĚĞƐƉƵĠƐĚĞϳϱĂŹŽƐĚĞƐĚĞƐƵĐŽŶƐƚƌƵĐĐŝſŶŽŶĞů ƉƌŽƉſƐŝƚŽĚĞĂďŽƌĚĂƌĞƐƚĂƐƉƌĞŐƵŶƚĂƐůŽƐŽďũĞƚŝǀŽƐĚĞĞƐƚĞĞƐƚƵĚŝŽƐŽŶůŽƐƐŝŐƵŝĞŶƚĞƐ ŝͿĞǀĂůƵĂƌƐŝůĂĐƌĞĂĐŝſŶĚĞƉŽnjĂƐŝŶƚĞƌŵĂƌĞĂůĞƐĞŶĞƐƚƌƵĐƚƵƌĂƐĂƌƚŝĨŝĐŝĂůĞƐĚĞƉƌŽƚĞĐĐŝſŶ ĐŽƐƚĞƌĂĚŽŶĚĞůĂĐŽŵƵŶŝĚĂĚďŝŽůſŐŝĐĂLJĂŚĂĂůĐĂŶnjĂĚŽƐƵĞƐƚĂĚŽĐůşŵĂdžĐŽŶƚƌŝďƵLJĞĂů ĂƵŵĞŶƚŽ ĚĞ ůĂ ďŝŽĚŝǀĞƌƐŝĚĂĚ ůŽĐĂů ŝŝͿ ĚĞƚĞƌŵŝŶĂƌ Ɛŝ Ğů ŝŶĐƌĞŵĞŶƚŽ ĚĞ ůĂ ĚŝǀĞƌƐŝĚĂĚ ĐĂƵƐĂĚŽƉŽƌůĂƐƉŽnjĂƐŝŶƚĞƌŵĂƌĞĂůĞƐĞƐŵĂLJŽƌĞŶĞůŶŝǀĞůƐƵƉĞƌŝŽƌƋƵĞĞŶĞůŝŶĨĞƌŝŽƌĚĞ ůĂ njŽŶĂ ŝŶƚĞƌŵĂƌĞĂů ŝŝŝͿ ĂŶĂůŝnjĂƌ ůĂ ƐƵĐĞƐŝſŶ ĚĞ ůĂ ĐŽŵƵŶŝĚĂĚ ďŝŽůſŐŝĐĂ ĞŶ Ğů ŶƵĞǀŽ ŵŝĐƌŽŚĄďŝƚĂƚĐƌĞĂĚŽĞŝǀͿŝĚĞŶƚŝĨŝĐĂƌůĂƐĞƐƉĞĐŝĞƐƋƵĞƐĞŚĂŶďĞŶĞĨŝĐŝĂĚŽĚŝƌĞĐƚĂŵĞŶƚĞ ĚĞůĂƐƉŽnjĂƐĐŽŶƐƚƌƵŝĚĂƐ WƵďůŝĐĂĐŝſŶϯDŝĐƌŽƌƌĞƐĞƌǀĂƐŵĂƌŝŶĂƐĂƌƚŝĨŝĐŝĂůĞƐĐŽŵŽŶƵĞǀĂŚĞƌƌĂŵŝĞŶƚĂĚĞŐĞƐƚŝſŶ ĞĐŽƐŝƐƚĠŵŝĐĂ ƉĂƌĂ ůĂ ĐŽŶƐĞƌǀĂĐŝſŶ ŵĂƌŝŶĂ Ğů ĐĂƐŽ ĚĞ W ĨĞƌƌƵŐŝŶĞĂ ;'ĂƐƚƌŽƉŽĚĂ WĂƚĞůůŝĚĂĞͿƵŶŽĚĞůŽƐŝŶǀĞƌƚĞďƌĂĚŽƐŵĂƌŝŶŽƐŵĄƐĂŵĞŶĂnjĂĚŽƐĚĞůDĞĚŝƚĞƌƌĄŶĞŽ
49 //K:d/sK^,/WMd^/^ WƵďůŝĐĂĐŝſŶ ϭ ƌĞĂĐŝſŶ ĚĞ ŵŝĐƌŽŚĄďŝƚĂƚƐ ;ƉŽnjĂƐ ŝŶƚĞƌŵĂƌĞĂůĞƐͿ ĞŶ ĞƐĐŽůůĞƌĂƐ ĐŽŶ ĐŽŵƵŶŝĚĂĚĞƐďŝŽůſŐŝĐĂƐĞŶĞƚĂƉĂĐůşŵĂdžĚĞƐƵƐƵĐĞƐŝſŶĞĐŽůſŐŝĐĂĐŽŵŽĨŽƌŵĂĚĞŵŝƚŝŐĂƌ ůŽƐĞĨĞĐƚŽƐŶĞŐĂƚŝǀŽƐĚĞůƐƵƐƚƌĂƚŽĂƌƚŝĨŝĐŝĂůƐŽďƌĞůĂďŝŽĚŝǀĞƌƐŝĚĂĚŵĂƌŝŶĂ ĂĚĂ ůĂ ĚŝƐŵŝŶƵĐŝſŶ ĚĞ ŚĄďŝƚĂƚƐ ĐŽƐƚĞƌŽƐ ŽĐĂƐŝŽŶĂĚĂ ƉŽƌ ůĂ ĐŽŶƐƚƌƵĐĐŝſŶ ĚĞ ĞƐƚƌƵĐƚƵƌĂƐĂƌƚŝĨŝĐŝĂůĞƐƉĂƌĂƐĂƚŝƐĨĂĐĞƌůĂƐĚĞŵĂŶĚĂƐĚĞůĚĞƐĂƌƌŽůůŽƵƌďĂŶŽĞƐŝŵƉĞƌĂƚŝǀŽ ĚŝƐĞŹĂƌ ĞƐƚĂƐ ĞƐƚƌƵĐƚƵƌĂƐ ƚĞŶŝĞŶĚŽ ĞŶ ĐƵĞŶƚĂ ƉƌŝŶĐŝƉŝŽƐ ĞĐŽůſŐŝĐŽƐ ĐŽŶ Ğů ĨŝŶ ĚĞ ŵŝŶŝŵŝnjĂƌƐƵŝŵƉĂĐƚŽĞŶĞůĞŶƚŽƌŶŽŶĂƚƵƌĂůĂƐşĐŽŵŽĞǀĂůƵĂƌĐŽŵƉƌĞŶĚĞƌLJĐƵĂŶƚŝĨŝĐĂƌ ĞůĞƐƚĂĚŽĚĞĞƐƚŽƐŚĄďŝƚĂƚƐWŽƌůŽƚĂŶƚŽůŽƐŽďũĞƚŝǀŽƐĚĞůĂƉƌĞƐĞŶƚĞŝŶǀĞƐƚŝŐĂĐŝſŶƐŽŶ ŝͿĞǀĂůƵĂƌƐŝůĂĐƌĞĂĐŝſŶĚĞƉŽnjĂƐŝŶƚĞƌŵĂƌĞĂůĞƐĞŶĞƐƚƌƵĐƚƵƌĂƐĚĞĚĞĨĞŶƐĂĐŽƐƚĞƌĂĚĞ ĞƐĐŽůůĞƌĂƐ ĚŽůŽŵşƚŝĐĂƐ ĐŽŶ ĐŽŵƵŶŝĚĂĚĞƐ ĐůşŵĂdž ĐŽŶƚƌŝďƵLJĞ Ăů ĂƵŵĞŶƚŽ ĚĞ ůĂ ďŝŽĚŝǀĞƌƐŝĚĂĚůŽĐĂůŝŝͿĂŶĂůŝnjĂƌĞůĞĨĞĐƚŽƐŽďƌĞĞůŚĂůŽƉĞƌŝŵĞƚƌĂůĂĚLJĂĐĞŶƚĞĂůĂƉŽnjĂŝŝŝͿ ǀĞƌŝĨŝĐĂƌ ĐŽŶĨŽƌŵĞ Ă ŝŶǀĞƐƚŝŐĂĐŝŽŶĞƐ ƉƌĞǀŝĂƐ ĞŶ ŽƚƌĂƐ ƌĞŐŝŽŶĞƐ ĚĞů ŵƵŶĚŽ Ɛŝ ůĂƐ ĞƐƚƌƵĐƚƵƌĂƐĂƌƚŝĨŝĐŝĂůĞƐĞŶĞƵƚĂĂůďĞƌŐĂŶĐŽŵƵŶŝĚĂĚĞƐŵĞŶŽƐĚŝǀĞƌƐĂƐƋƵĞůĂƐĄƌĞĂƐ ŶĂƚƵƌĂůĞƐ ĐŝƌĐƵŶĚĂŶƚĞƐ ĞŶ Ğů ŵĞĚŝŽ ŝŶƚĞƌŵĂƌĞĂů ŝǀͿ ĞdžƉůŽƌĂƌ ƋƵĠ ĞƐƉĞĐŝĞƐ ƐĞ ďĞŶĞĨŝĐŝĂƌŽŶ ĚŝƌĞĐƚĂŵĞŶƚĞ ĚĞů ŶƵĞǀŽ ŵŝĐƌŽŚĄďŝƚĂƚ ĐƌĞĂĚŽ LJ ǀͿ ĚĞƐĐƌŝďŝƌ ůĂƐ ĐŽŵƵŶŝĚĂĚĞƐďŝŽůſŐŝĐĂƐĚĞĞƐƚĞƚŝƉŽĚĞŵŝĐƌŽŚĄďŝƚĂƚƐĚĞŶƚƌŽĚĞůŵĞĚŝŽŶĂƚƵƌĂů WƵďůŝĐĂĐŝſŶ Ϯ ^ƵĐĞƐŝſŶ ĞĐŽůſŐŝĐĂ ĚĞ ůĂ ĐŽŵƵŶŝĚĂĚ ďŝŽůſŐŝĐĂ ĂƐĞŶƚĂĚĂ ĞŶ ƉŽnjĂƐ ŝŶƚĞƌŵĂƌĞĂůĞƐ ĐƌĞĂĚĂƐ ĞŶ ĞƐƚƌƵĐƚƵƌĂƐ ĚĞ ƉƌŽƚĞĐĐŝſŶ ĐŽƐƚĞƌĂƐ ;ϳϱ ĂŹŽƐ ĚĞ ŵŽŶŝƚŽƌŝnjĂĐŝſŶͿ ůŽďũĞƚŝǀŽĚĞůƉƌĞƐĞŶƚĞĞƐƚƵĚŝŽĞƐĂŶĂůŝnjĂƌůĂƐĚŝƐƚŝŶƚĂƐĞƚĂƉĂƐĚĞůĂƐƵĐĞƐŝſŶ ĞĐŽůſŐŝĐĂƋƵĞŚĂĞdžƉĞƌŝŵĞŶƚĂĚŽĞůďŝŽƚŽƉŽĚĞůĂƐƉŽnjĂƐŝŶƚĞƌŵĂƌĞĂůĞƐĐƌĞĂĚĂƐĞŶůĂƐ ĞƐƚƌƵĐƚƵƌĂƐĚĞƉƌŽƚĞĐĐŝſŶĐŽƐƚĞƌĂƐĂƐşĐŽŵŽǀĂůŽƌĂƌƐŝĞůŵŝĐƌŽŚĄďŝƚĂƚĐŽŶƚƌŝďƵLJĞĂů ĂƵŵĞŶƚŽĚĞůĂďŝŽĚŝǀĞƌƐŝĚĂĚůŽĐĂůĚĞƐƉƵĠƐĚĞϳϱĂŹŽƐĚĞƐĚĞƐƵĐŽŶƐƚƌƵĐĐŝſŶŽŶĞů ƉƌŽƉſƐŝƚŽĚĞĂďŽƌĚĂƌĞƐƚĂƐƉƌĞŐƵŶƚĂƐůŽƐŽďũĞƚŝǀŽƐĚĞĞƐƚĞĞƐƚƵĚŝŽƐŽŶůŽƐƐŝŐƵŝĞŶƚĞƐ ŝͿĞǀĂůƵĂƌƐŝůĂĐƌĞĂĐŝſŶĚĞƉŽnjĂƐŝŶƚĞƌŵĂƌĞĂůĞƐĞŶĞƐƚƌƵĐƚƵƌĂƐĂƌƚŝĨŝĐŝĂůĞƐĚĞƉƌŽƚĞĐĐŝſŶ ĐŽƐƚĞƌĂĚŽŶĚĞůĂĐŽŵƵŶŝĚĂĚďŝŽůſŐŝĐĂLJĂŚĂĂůĐĂŶnjĂĚŽƐƵĞƐƚĂĚŽĐůşŵĂdžĐŽŶƚƌŝďƵLJĞĂů ĂƵŵĞŶƚŽ ĚĞ ůĂ ďŝŽĚŝǀĞƌƐŝĚĂĚ ůŽĐĂů ŝŝͿ ĚĞƚĞƌŵŝŶĂƌ Ɛŝ Ğů ŝŶĐƌĞŵĞŶƚŽ ĚĞ ůĂ ĚŝǀĞƌƐŝĚĂĚ ĐĂƵƐĂĚŽƉŽƌůĂƐƉŽnjĂƐŝŶƚĞƌŵĂƌĞĂůĞƐĞƐŵĂLJŽƌĞŶĞůŶŝǀĞůƐƵƉĞƌŝŽƌƋƵĞĞŶĞůŝŶĨĞƌŝŽƌĚĞ ůĂ njŽŶĂ ŝŶƚĞƌŵĂƌĞĂů ŝŝŝͿ ĂŶĂůŝnjĂƌ ůĂ ƐƵĐĞƐŝſŶ ĚĞ ůĂ ĐŽŵƵŶŝĚĂĚ ďŝŽůſŐŝĐĂ ĞŶ Ğů ŶƵĞǀŽ ŵŝĐƌŽŚĄďŝƚĂƚĐƌĞĂĚŽĞŝǀͿŝĚĞŶƚŝĨŝĐĂƌůĂƐĞƐƉĞĐŝĞƐƋƵĞƐĞŚĂŶďĞŶĞĨŝĐŝĂĚŽĚŝƌĞĐƚĂŵĞŶƚĞ ĚĞůĂƐƉŽnjĂƐĐŽŶƐƚƌƵŝĚĂƐ WƵďůŝĐĂĐŝſŶϯDŝĐƌŽƌƌĞƐĞƌǀĂƐŵĂƌŝŶĂƐĂƌƚŝĨŝĐŝĂůĞƐĐŽŵŽŶƵĞǀĂŚĞƌƌĂŵŝĞŶƚĂĚĞŐĞƐƚŝſŶ ĞĐŽƐŝƐƚĠŵŝĐĂ ƉĂƌĂ ůĂ ĐŽŶƐĞƌǀĂĐŝſŶ ŵĂƌŝŶĂ Ğů ĐĂƐŽ ĚĞ W ĨĞƌƌƵŐŝŶĞĂ ;'ĂƐƚƌŽƉŽĚĂ WĂƚĞůůŝĚĂĞͿƵŶŽĚĞůŽƐŝŶǀĞƌƚĞďƌĂĚŽƐŵĂƌŝŶŽƐŵĄƐĂŵĞŶĂnjĂĚŽƐĚĞůDĞĚŝƚĞƌƌĄŶĞŽ dƌĂƐǀĂůŽƌĂƌůĂƉƌŽƉƵĞƐƚĂĚĞĐƌĞĂƌȇDŝĐƌŽƌƌĞƐĞƌǀĂƐDĂƌŝŶĂƐƌƚŝĨŝĐŝĂůĞƐȇĐŽŵŽ ƵŶĂ ŶƵĞǀĂ ŚĞƌƌĂŵŝĞŶƚĂĚĞ ŐĞƐƚŝſŶ ĞĐŽƐŝƐƚĠŵŝĐĂ ƉĂƌĂ ůĂ ĐŽŶƐĞƌǀĂĐŝſŶ ŵĞĚŝŽ ŵĂƌŝŶŽ ;'ĂƌĐşĂͲ'ſŵĞnjĞƚĂůϮϬϭϮϬϭϱͿĞůƉƌĞƐĞŶƚĞƚƌĂďĂũŽƉƌĞƚĞŶĚĞĂƉŽƌƚĂƌĚĂƚŽƐĞŵƉşƌŝĐŽƐ ĚĞƵŶĐĂƐŽƌĞĂůLJƚĂŶŐŝďůĞĂƐşĐŽŵŽǀĂůŽƌĂƌůĂĞĨŝĐŝĞŶĐŝĂLJǀŝĂďŝůŝĚĂĚĚĞůĂƉƌŽƉŽƐŝĐŝſŶ Ŷ ĐŽŶƐĞĐƵĞŶĐŝĂ ůŽƐ ŽďũĞƚŝǀŽƐ ĚĞ ĞƐƚĞ ĞƐƚƵĚŝŽ ƐŽŶ ŝͿ ĚĞƚĞƌŵŝŶĂƌ Ɛŝ ůĂƐ ĞƐƚƌƵĐƚƵƌĂƐ ĂƌƚŝĨŝĐŝĂůĞƐ ĚĞ ĚĞĨĞŶƐĂ ĐŽƐƚĞƌĂ ĚĞ ĞƵƚĂ ;ĞƐƚƌĞĐŚŽ ĚĞ 'ŝďƌĂůƚĂƌͿ ĐƵŵƉůĞŶ ĐŽŶ ůŽƐ ƌĞƋƵŝƐŝƚŽƐ ƉĂƌĂ ůĂ ŝŵƉůĞŵĞŶƚĂĐŝſŶ ĚĞ ƵŶĂ DD Ğ ŝĚĞŶƚŝĨŝĐĂƌ ƋƵĠ ĞƐƉĞĐŝĞƐ ƉŽĚƌşĂŶ ďĞŶĞĨŝĐŝĂƌƐĞĚĞĚŝĐŚĂƉƌŽƚĞĐĐŝſŶLJ;ŝŝͿĞǀĂůƵĂƌĞůĞĨĞĐƚŽĞƐƉĞƌĂĚŽƐŽďƌĞůĂƉŽďůĂĐŝſŶĚĞů ŵŽůƵƐĐŽ ĞŶƉĞůŝŐƌŽ ĚĞĞdžƚŝŶĐŝſŶ W ĨĞƌƌƵŐŝŶĞĂ ƋƵĞĂĐƚƷĂ ĐŽŵŽƵŶĂ ĞƐƉĞĐŝĞ ŵŽĚĞůŽ ďĞŶĞĨŝĐŝĂƌŝĂĚĞĞƐƚĞŝŶŶŽǀĂĚŽƌĞŶĨŽƋƵĞ WƵďůŝĐĂĐŝſŶϰƐƚƵĚŝŽĚĞůĂĚŝŶĄŵŝĐĂƉŽďůĂĐŝŽŶĂůLJĞĨĞĐƚŽƐĂďŝſƚŝĐŽƐƋƵĞŵŽĚĞůĂŶůĂ ĞƐƚƌƵĐƚƵƌĂƉŽďůĂĐŝŽŶĂůĚĞůŵŽůƵƐĐŽŐĂƐƚĞƌſƉŽĚŽWĨĞƌƌƵŐŝŶĞĂĂƐĞŶƚĂĚŽĞŶĞůůŝƚŽƌĂůĚĞ ĞƵƚĂ ŶƚƌĞůŽƐĚŝƐƚŝŶƚŽƐŽďũĞƚŝǀŽƐĚĞůƉƌĞƐĞŶƚĞĞƐƚƵĚŝŽƐĞŚĂĞdžĂŵŝŶĂĚŽĞůƉĂƉĞůƋƵĞ ůĂƐƐƵďƉŽďůĂĐŝŽŶĞƐĚĞWĨĞƌƌƵŐŝŶĞĂĂƐĞŶƚĂĚĂƐĞŶƐƵƐƚƌĂƚŽƐĂƌƚŝĨŝĐŝĂůĞƐũƵĞŐĂŶƌĞƐƉĞĐƚŽ ĂĂƋƵĞůůĂƐĂƐĞŶƚĂĚĂƐĞŶĞůŵĞĚŝŽŶĂƚƵƌĂůĞƐƉĞĐŝĂůŵĞŶƚĞĞŶůĂƐĚĞůƐƉĂĐŝŽWƌŽƚĞŐŝĚŽ ZĞĚEĂƚƵƌĂϮϬϬϬůŽĐĂůŝnjĂĚŽĞŶůĂŝƵĚĂĚĚĞĞƵƚĂWĂƌĂĞůůŽƐĞŚĂĞƐƚƵĚŝĂĚŽůĂĚŝŶĄŵŝĐĂ ƉŽďůĂĐŝŽŶĂů ƋƵĞ ŚĂ ĞdžƉĞƌŝŵĞŶƚĂĚŽ ůĂ ƉŽďůĂĐŝſŶ ĞŶ ůŽƐ ƷůƚŝŵŽƐ ϭϬ ĂŹŽƐ ĂƐş ĐŽŵŽ ŝĚĞŶƚŝĨŝĐĂĚŽLJĐƵĂŶƚŝĨŝĐĂĚŽůŽƐĨĂĐƚŽƌĞƐĂďŝſƚŝĐŽƐƋƵĞŵŽĚĞůĂŶƐƵĞƐƚƌƵĐƚƵƌĂƉŽďůĂĐŝŽŶĂů ŶĐŽŶƐĞĐƵĞŶĐŝĂůŽƐŽďũĞƚŝǀŽƐĚĞůƉƌĞƐĞŶƚĞĞƐƚƵĚŝŽƐŽŶŝͿĚĞƚĞƌŵŝŶĂƌĞůĞƐƚĂĚŽĂĐƚƵĂů ĚĞ ůĂ ƉŽďůĂĐŝſŶ ĚĞ W ĨĞƌƌƵŐŝŶĞĂ ŝŝͿ ĞƐƚƵĚŝĂƌ Ğů ĐĂŵďŝŽ ƋƵĞ ŚĂ ĞdžƉĞƌŝŵĞŶƚĂĚŽ ůĂ ƉŽďůĂĐŝſŶĞŶůŽƐƷůƚŝŵŽƐϭϬĂŹŽƐŝŝŝͿǀĂůŝĚĂƌůŽƐƌĞƐƵůƚĂĚŽƐĚĞůŵĠƚŽĚŽĚĞƉƌĞĚŝĐĐŝſŶ ΗƉŽƉƵůĂƚŝŽŶǀŝĂďŝůŝƚLJĂŶĂůLJƐŝƐΗ;WsͿůůĞǀĂĚŽĂĐĂďŽƉŽƌƐƉŝŶŽƐĂĞƚĂů;ϮϬϭϴͿƉĂƌĂůĂ ƉŽďůĂĐŝſŶĚĞWĨĞƌƌƵŐŝŶĞĂĞŶĞƵƚĂLJŝǀͿĞdžƉůŽƌĂƌůŽƐĨĂĐƚŽƌĞƐĂŵďŝĞŶƚĂůĞƐLJďŝŽůſŐŝĐŽƐ ƋƵĞĂĨĞĐƚĂŶĂůĂĞƐƚƌƵĐƚƵƌĂĚĞůĂƐƉŽďůĂĐŝŽŶĞƐĚĞWĨĞƌƌƵŐŝŶĞĂ
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51 /ŶŽĂƐƚĂůĨůƵdžĞƐŝŶƚŚĞŶƚŚƌŽƉŽĐĞŶĞƚŚĞůĂŶĚͲŽĐĞĂŶŝŶƚĞƌĂĐƚŝŽŶƐŝŶƚŚĞĐŽĂƐƚĂů njŽŶĞ ƉƌŽũĞĐƚ ŽĨ ƚŚĞ /ŶƚĞƌŶĂƚŝŽŶĂů 'ĞŽƐƉŚĞƌĞͲŝŽƐƉŚĞƌĞ WƌŽŐƌĂŵŵĞ ;ƉƉ ϭͲϯϳͿ ĞƌůŝŶ ,ĞŝĚĞůďĞƌŐ ^ƉƌŝŶŐĞƌ ĞƌůŝŶ ,ĞŝĚĞůďĞƌŐ ŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϬϳϯͲϱϰϬͲ ϮϳϴϱϭͲϲͺϭ Crutzen, P., & Stoermer, E. (2000). The ‘Anthropocene’. 'ůŽďĂůŚĂŶŐĞEĞǁƐůĞƚƚĞƌϰϭ ŽŵŝƐŝſŶ /ŶƚĞƌŶĂĐŝŽŶĂů ĚĞ ƐƚƌĂƚŝŐƌĂĨşĂ dĂďůĂ ĐƌŽŶŽĞƐƚƌĂƚŝŐƌĄĨŝĐĂ ŝŶƚĞƌŶĂĐŝŽŶĂů ŽŶƐƵůƚĂĚŽ Ğů Ϯϭ ĚĞ ŶŽǀŝĞŵďƌĞ ĚĞ ϮϬϭϴ ;ŚƚƚƉƐƐƚƌĂƚŝŐƌĂƉŚLJŽƌŐ/^ĐŚĂƌƚŚƌŽŶŽƐƚƌĂƚŚĂƌƚϮϬϭϴͲϬϴ^ƉĂŶŝƐŚƉĚĨͿ ĂĨĨŽƌŶ<DĂLJĞƌͲWŝŶƚŽDDŽƌƌŝƐZ>ΘtĂůƚŚĂŵE:;ϮϬϭϱĂͿƉƉůŝĐĂƚŝŽŶŽĨ ŵĂŶĂŐĞŵĞŶƚ ƚŽŽůƐ ƚŽ ŝŶƚĞŐƌĂƚĞ ĞĐŽůŽŐŝĐĂů ƉƌŝŶĐŝƉůĞƐ ǁŝƚŚ ƚŚĞ ĚĞƐŝŐŶ ŽĨ ŵĂƌŝŶĞ ŝŶĨƌĂƐƚƌƵĐƚƵƌĞ :ŽƵƌŶĂů ŽĨ ŶǀŝƌŽŶŵĞŶƚĂů DĂŶĂŐĞŵĞŶƚ ϭϱϴ ϲϭͲϳϯ ŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϭϲũũĞŶǀŵĂŶϮϬϭϱϬϱϬϬϭ ĂĨĨŽƌŶ<'ůĂƐďLJdDŝƌŽůĚŝ>ZŝǀĞƌŽE<DĂLJĞƌͲWŝŶƚŽDΘ:ŽŚŶƐƚŽŶ> ;ϮϬϭϱďͿ DĂƌŝŶĞ ƵƌďĂŶŝnjĂƚŝŽŶ ĂŶ ĞĐŽůŽŐŝĐĂů ĨƌĂŵĞǁŽƌŬ ĨŽƌ ĚĞƐŝŐŶŝŶŐ ŵƵůƚŝĨƵŶĐƚŝŽŶĂůĂƌƚŝĨŝĐŝĂůƐƚƌƵĐƚƵƌĞƐ&ƌŽŶƚŝĞƌƐŝŶĐŽůŽŐLJĂŶĚƚŚĞŶǀŝƌŽŶŵĞŶƚϭϯ;ϮͿ ϴϮͲϵϬŚƚƚƉƐĚŽŝŽƌŐϭϬϭϴϵϬϭϰϬϬϱϬ ĂůďLJ ^ ;ϮϬϭϲͿ ZĞͲĞǀĂůƵĂƚŝŶŐ ƚŚĞ ŶƚŚƌŽƉŽĐĞŶĞ ŶƚŝƋƵŝƚLJ WƵďůŝĐĂƚŝŽŶƐ ŚƚƚƉƐĚŽŝŽƌŐϭϬϭϱϭϴϰĂƋLJϮϬϭϲϯϲ ƵŐĂŶ:ŝƌŽůĚŝ>ŚĂƉŵĂŶD'tĂůŬĞƌ^:^ĐŚůĂĐŚĞƌdtŽůĂŶƐŬŝΘ DĐ>ƵƐŬLJ;ϮϬϭϭͿϴϬϮͲƐƚƵĂƌŝŶĞĂŶĚĐŽĂƐƚĂůƐƚƌƵĐƚƵƌĞƐĞŶǀŝƌŽŶŵĞŶƚĂůĞĨĨĞĐƚƐĂ ĨŽĐƵƐŽŶƐŚŽƌĞĂŶĚŶĞĂƌƐŚŽƌĞƐƚƌƵĐƚƵƌĞƐdƌĞĂƚŝƐĞŽŶĞƐƚƵĂƌŝŶĞĂŶĚĐŽĂƐƚĂůƐĐŝĞŶĐĞ ϴϭϳͲϰϭŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϭϲϵϳϴͲϬͲϭϮͲϯϳϰϳϭϭͲϮϬϬϴϬϮͲϬ ƐƉŝŶŽƐĂ dŽƌƌĞ & ;ϮϬϬϲͿ ĂƌĂĐƚĞƌŝnjĂĐŝſŶ ďŝŽůſŐŝĐĂ ĚĞů ŵŽůƵƐĐŽ ƉƌŽƚĞŐŝĚŽ WĂƚĞůůĂ &ĞƌƌƌƵŐŝŶĞĂ 'ŵĞůŝŶ ϭϳϵϭ ;'ĂƐƚƌŽƉŽĚĂ WĂƚĞůůŝĚĂĞͿ ĂƐĞƐ ƉĂƌĂ ƐƵ ŐĞƐƚŝſŶ LJ ĐŽŶƐĞƌǀĂĐŝſŶϯϬͲϰϱŚƚƚƉƐŚĚůŚĂŶĚůĞŶĞƚϭϭϰϰϭϳϮϰϮϯ ƐƉŝŶŽƐĂ&'ƵĞƌƌĂͲ'ĂƌĐşĂ:DΘ'ĂƌĐşĂͲ'ſŵĞnj:;ϮϬϬϳͿ^ĞǁĂŐĞƉŽůůƵƚŝŽŶĂŶĚ ĞdžƚŝŶĐƚŝŽŶ ƌŝƐŬ ĂŶ ĞŶĚĂŶŐĞƌĞĚ ůŝŵƉĞƚ ĂƐ Ă ďŝŽŝŶĚŝĐĂƚŽƌ ŝŽĚŝǀĞƌƐŝƚLJ ĂŶĚ ĐŽŶƐĞƌǀĂƚŝŽŶϭϲϯϳϳͲϯϵϳŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϬϳƐϭϬϱϯϭͲϬϬϱͲϯϬϭϰͲϯ ƐƉŝŶŽƐĂ&ZŝǀĞƌĂͲ/ŶŐƌĂŚĂŵ'&ĂΘ'ĂƌĐşĂͲ'ſŵĞnj:;ϮϬϬϵͿĨĨĞĐƚŽĨŚƵŵĂŶ ƉƌĞƐƐƵƌĞ ŽŶ ƉŽƉƵůĂƚŝŽŶ ƐŝnjĞ ƐƚƌƵĐƚƵƌĞƐ ŽĨ ƚŚĞ ĞŶĚĂŶŐĞƌĞĚ ĨĞƌƌƵŐŝŶĞĂŶ ůŝŵƉĞƚ ƚŽǁĂƌĚĨƵƚƵƌĞŵĂŶĂŐĞŵĞŶƚŵĞĂƐƵƌĞƐ:ŽƵƌŶĂůŽĨŽĂƐƚĂůZĞƐĞĂƌĐŚϮϱ;ϰͿϴϱϳͲϴϲϯ ŚƚƚƉƐĚŽŝŽƌŐϭϬϮϭϭϮϬϴͲϭϬϬϱϭ ƐƉŝŶŽƐĂ&ΘZŝǀĞƌĂͲ/ŶŐƌĂŚĂŵ';ϮϬϭϳͿŝŽůŽŐŝĐĂůĐŽŶƐĞƌǀĂƚŝŽŶŽĨŐŝĂŶƚůŝŵƉĞƚƐ ƚŚĞ ŝŵƉůŝĐĂƚŝŽŶƐ ŽĨ ůĂƌŐĞ ƐŝnjĞ ĚǀĂŶĐĞƐ ŝŶ ŵĂƌŝŶĞ ďŝŽůŽŐLJ ϳϲ ϭϬϱͲϭϱϱ ŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϭϲďƐĂŵďϮϬϭϲϭϬϬϬϮ
52 ƐƉŝŶŽƐĂ&ΘĂnjĂŝƌŝ,;ϮϬϮϯͿ/ŵƉĂĐƚƐĞǀŽůƵƚŝŽŶĂŶĚĐŚĂŶŐĞƐŽĨƉƌĞƐƐƵƌĞŽŶŵĂƌŝŶĞ ĞĐŽƐLJƐƚĞŵƐŝŶƌĞĐĞŶƚƚŝŵĞƐdŽǁĂƌĚŶĞǁĞŵĞƌŐŝŶŐĂŶĚƵŶĨŽƌĞƐĞĞŶŝŵƉĂĐƚƐǁŝƚŚŝŶ Ă ĐŚĂŶŐŝŶŐ ǁŽƌůĚ /Ŷ ŽĂƐƚĂů ,ĂďŝƚĂƚ ŽŶƐĞƌǀĂƚŝŽŶ ;ƉƉ ϭͲϭϲͿ ĐĂĚĞŵŝĐ WƌĞƐƐ ŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϭϲϵϳϴͲϬͲϯϮϯͲϴϱϲϭϯͲϯϬϬϬϬϰͲϵ ǀĂŶƐ:>ĂǁƌĞŶĐĞW:EĂƚĂŶnjŝ^DŽŽƌĞW:ĂǀŝĞƐ:ƌŽǁĞdWΘ ƌŽŽŬƐWZ;ϮϬϮϭͿZĞƉůŝĐĂƚŝŶŐŶĂƚƵƌĂůƚŽƉŽŐƌĂƉŚLJŽŶŵĂƌŝŶĞĂƌƚŝĨŝĐŝĂůƐƚƌƵĐƚƵƌĞƐ– ŶŽǀĞů ĂƉƉƌŽĂĐŚ ƚŽ ĞĐŽͲĞŶŐŝŶĞĞƌŝŶŐ ĐŽůŽŐŝĐĂů ŶŐŝŶĞĞƌŝŶŐ ϭϲϬ ϭϬϲϭϰϰ ŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϭϲũĞĐŽůĞŶŐϮϬϮϬϭϬϲϭϰϰ &ŝƌƚŚ>dŚŽŵƉƐŽŶZŽŚŶ<ďďŝĂƚŝDŝƌŽůĚŝ>ŽƵŵĂd:Θ,ĂǁŬŝŶƐ ^ : ;ϮϬϭϰͿ ĞƚǁĞĞŶ Ă ƌŽĐŬ ĂŶĚ Ă ŚĂƌĚ ƉůĂĐĞ ĞŶǀŝƌŽŶŵĞŶƚĂů ĂŶĚ ĞŶŐŝŶĞĞƌŝŶŐ ĐŽŶƐŝĚĞƌĂƚŝŽŶƐǁŚĞŶĚĞƐŝŐŶŝŶŐĐŽĂƐƚĂůĚĞĨĞŶĐĞƐƚƌƵĐƚƵƌĞƐŽĂƐƚĂůŶŐŝŶĞĞƌŝŶŐϴϳ ϭϮϮͲϭϯϱŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϭϲũĐŽĂƐƚĂůĞŶŐϮϬϭϯϭϬϬϭϱ &ŝƌƚŚ><ŶŝŐŚƚƐDƌŝĚŐĞƌǀĂŶƐDŝĞƐŬŽǁƐŬĂEDŽŽƌĞW:Θ ,ĂǁŬŝŶƐ^:;ϮϬϭϲͿKĐĞĂŶƐƉƌĂǁůĐŚĂůůĞŶŐĞƐĂŶĚŽƉƉŽƌƚƵŶŝƚŝĞƐĨŽƌďŝŽĚŝǀĞƌƐŝƚLJ ŵĂŶĂŐĞŵĞŶƚŝŶĂĐŚĂŶŐŝŶŐǁŽƌůĚŚƚƚƉƐĚŽŝŽƌŐϭϬϭϮϬϭϵϳϴϭϯϭϱϯϲϴϱϵϳ &ŝƌƚŚ>ŽŶĞ:ĂƌƚŚŽůŽŵĞǁŝƐŚŽƉD:ƵŐŶŽƚƵůůĞƌŝ&Θ<ŶŝŐŚƚƐ D;ϮϬϮϰ&ĞďƌƵĂƌLJͿŽĂƐƚĂůŐƌĞĞŶŝŶŐŽĨŐƌĞLJŝŶĨƌĂƐƚƌƵĐƚƵƌĞĂŶƵƉĚĂƚĞŽŶƚŚĞ ƐƚĂƚĞͲŽĨͲƚŚĞͲĂƌƚ /Ŷ WƌŽĐĞĞĚŝŶŐƐ ŽĨ ƚŚĞ /ŶƐƚŝƚƵƚŝŽŶ ŽĨ ŝǀŝů ŶŐŝŶĞĞƌƐͲDĂƌŝƚŝŵĞ ŶŐŝŶĞĞƌŝŶŐ;ƉƉϭͲϲϵͿŵĞƌĂůĚWƵďůŝƐŚŝŶŐ>ŝŵŝƚĞĚ &ƌĞŶŬŝĞů>;ϭϵϳϱͿŽŶƚƌŝďƵƚŝŽŶăůΖĠƚƵĚĞĚĞƐĐLJĐůĞƐĚĞƌĞƉƌŽĚƵĐƚŝŽŶĚĞƐWĂƚĞůůŝĚĂĞĞŶ ůŐĠƌŝĞWƵďďůŝĐĂnjŝŽŶŝĚĞůůĂ^ƚĂnjŝŽŶĞŽŽůŽŐŝĐĂEĂƉŽůŝϯϵ García‐Gómez, J. C., López‐Fé, C. M., Espinosa, F., Guerra‐García, J. M., & Rivera‐ /ŶŐƌĂŚĂŵ ' ;ϮϬϭϭͿ Marine artificial micro‐reserves: A possibility for the ĐŽŶƐĞƌǀĂƚŝŽŶŽĨĞŶĚĂŶŐĞƌĞĚƐƉĞĐŝĞƐůŝǀŝŶŐŽŶĂƌƚŝĨŝĐŝĂůƐƵďƐƚƌĂƚĂDĂƌŝŶĞĐŽůŽŐLJ ϯϮ;ϭͿϲͲϭϰŚƚƚƉƐĚŽŝŽƌŐϭϬϭϭϭϭũϭϰϯϵͲϬϰϴϱϮϬϭϬϬϬϰϬϵdž García‐Gómez, J. C., Guerra‐García, J. M., Espinosa, F., Maestre, M. J., Rivera‐Ingraham, '&Ă& López‐Fé, C. M. (2015). Artificial Marine Micro‐Reserves Networks ;DDZEƐͿĂŶŝŶŶŽǀĂƚŝǀĞĂƉƉƌŽĂĐŚƚŽĐŽŶƐĞƌǀĞŵĂƌŝŶĞůŝƚƚŽƌĂůďŝŽĚŝǀĞƌƐŝƚLJĂŶĚ ƉƌŽƚĞĐƚ ĞŶĚĂŶŐĞƌĞĚ ƐƉĞĐŝĞƐ DĂƌŝŶĞ ĐŽůŽŐLJ ϯϲ;ϯͿ ϮϱϵͲϮϳϳ ŚƚƚƉƐĚŽŝŽƌŐϭϬϭϭϭϭũϭϰϯϵͲϬϰϴϱϮϬϭϬϬϬϰϬϵdž 'ŝďƐŽŶZƚŬŝŶƐŽŶZΘ'ŽƌĚŽŶ:;ϮϬϬϳͿ>ŽƐƐƐƚĂƚƵƐĂŶĚƚƌĞŶĚƐĨŽƌĐŽĂƐƚĂůŵĂƌŝŶĞ ŚĂďŝƚĂƚƐŽĨƵƌŽƉĞKĐĞĂŶŽŐƌĂƉŚLJĂŶĚDĂƌŝŶĞŝŽůŽŐLJĂŶĂŶŶƵĂůƌĞǀŝĞǁϰϱϯϰϱͲ ϰϬϱŚƚƚƉƐĚŽŝŽƌŐϭϬϭϮϬϭϵϳϴϭϰϮϬϬϱϬϵϰϯ 'ŝůůDĂƐĐŝĂDŚŵĂĚŝĂ'E'ůĞǁ>>ĞƐƚĞƌ^ĂƌŶĞƐDĞƚĂů;ϮϬϭϳͿ ĂƉĂĐŝƚLJƐŚŽƌƚĨĂůůƐŚŝŶĚĞƌƚŚĞƉĞƌĨŽƌŵĂŶĐĞŽĨŵĂƌŝŶĞƉƌŽͲƚĞĐƚĞĚĂƌĞĂƐŐůŽďĂůůLJ EĂƚƵƌĞϱϰϯϲϲϱ–ϲϲϵŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϯϴŶĂƚƵƌĞϮϭϳϬϴ
53 ƐƉŝŶŽƐĂ&ΘĂnjĂŝƌŝ,;ϮϬϮϯͿ/ŵƉĂĐƚƐĞǀŽůƵƚŝŽŶĂŶĚĐŚĂŶŐĞƐŽĨƉƌĞƐƐƵƌĞŽŶŵĂƌŝŶĞ ĞĐŽƐLJƐƚĞŵƐŝŶƌĞĐĞŶƚƚŝŵĞƐdŽǁĂƌĚŶĞǁĞŵĞƌŐŝŶŐĂŶĚƵŶĨŽƌĞƐĞĞŶŝŵƉĂĐƚƐǁŝƚŚŝŶ Ă ĐŚĂŶŐŝŶŐ ǁŽƌůĚ /Ŷ ŽĂƐƚĂů ,ĂďŝƚĂƚ ŽŶƐĞƌǀĂƚŝŽŶ ;ƉƉ ϭͲϭϲͿ ĐĂĚĞŵŝĐ WƌĞƐƐ ŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϭϲϵϳϴͲϬͲϯϮϯͲϴϱϲϭϯͲϯϬϬϬϬϰͲϵ ǀĂŶƐ:>ĂǁƌĞŶĐĞW:EĂƚĂŶnjŝ^DŽŽƌĞW:ĂǀŝĞƐ:ƌŽǁĞdWΘ ƌŽŽŬƐWZ;ϮϬϮϭͿZĞƉůŝĐĂƚŝŶŐŶĂƚƵƌĂůƚŽƉŽŐƌĂƉŚLJŽŶŵĂƌŝŶĞĂƌƚŝĨŝĐŝĂůƐƚƌƵĐƚƵƌĞƐ– ŶŽǀĞů ĂƉƉƌŽĂĐŚ ƚŽ ĞĐŽͲĞŶŐŝŶĞĞƌŝŶŐ ĐŽůŽŐŝĐĂů ŶŐŝŶĞĞƌŝŶŐ ϭϲϬ ϭϬϲϭϰϰ ŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϭϲũĞĐŽůĞŶŐϮϬϮϬϭϬϲϭϰϰ &ŝƌƚŚ>dŚŽŵƉƐŽŶZŽŚŶ<ďďŝĂƚŝDŝƌŽůĚŝ>ŽƵŵĂd:Θ,ĂǁŬŝŶƐ ^ : ;ϮϬϭϰͿ ĞƚǁĞĞŶ Ă ƌŽĐŬ ĂŶĚ Ă ŚĂƌĚ ƉůĂĐĞ ĞŶǀŝƌŽŶŵĞŶƚĂů ĂŶĚ ĞŶŐŝŶĞĞƌŝŶŐ ĐŽŶƐŝĚĞƌĂƚŝŽŶƐǁŚĞŶĚĞƐŝŐŶŝŶŐĐŽĂƐƚĂůĚĞĨĞŶĐĞƐƚƌƵĐƚƵƌĞƐŽĂƐƚĂůŶŐŝŶĞĞƌŝŶŐϴϳ ϭϮϮͲϭϯϱŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϭϲũĐŽĂƐƚĂůĞŶŐϮϬϭϯϭϬϬϭϱ &ŝƌƚŚ><ŶŝŐŚƚƐDƌŝĚŐĞƌǀĂŶƐDŝĞƐŬŽǁƐŬĂEDŽŽƌĞW:Θ ,ĂǁŬŝŶƐ^:;ϮϬϭϲͿKĐĞĂŶƐƉƌĂǁůĐŚĂůůĞŶŐĞƐĂŶĚŽƉƉŽƌƚƵŶŝƚŝĞƐĨŽƌďŝŽĚŝǀĞƌƐŝƚLJ ŵĂŶĂŐĞŵĞŶƚŝŶĂĐŚĂŶŐŝŶŐǁŽƌůĚŚƚƚƉƐĚŽŝŽƌŐϭϬϭϮϬϭϵϳϴϭϯϭϱϯϲϴϱϵϳ &ŝƌƚŚ>ŽŶĞ:ĂƌƚŚŽůŽŵĞǁŝƐŚŽƉD:ƵŐŶŽƚƵůůĞƌŝ&Θ<ŶŝŐŚƚƐ D;ϮϬϮϰ&ĞďƌƵĂƌLJͿŽĂƐƚĂůŐƌĞĞŶŝŶŐŽĨŐƌĞLJŝŶĨƌĂƐƚƌƵĐƚƵƌĞĂŶƵƉĚĂƚĞŽŶƚŚĞ ƐƚĂƚĞͲŽĨͲƚŚĞͲĂƌƚ /Ŷ WƌŽĐĞĞĚŝŶŐƐ ŽĨ ƚŚĞ /ŶƐƚŝƚƵƚŝŽŶ ŽĨ ŝǀŝů ŶŐŝŶĞĞƌƐͲDĂƌŝƚŝŵĞ ŶŐŝŶĞĞƌŝŶŐ;ƉƉϭͲϲϵͿŵĞƌĂůĚWƵďůŝƐŚŝŶŐ>ŝŵŝƚĞĚ &ƌĞŶŬŝĞů>;ϭϵϳϱͿŽŶƚƌŝďƵƚŝŽŶăůΖĠƚƵĚĞĚĞƐĐLJĐůĞƐĚĞƌĞƉƌŽĚƵĐƚŝŽŶĚĞƐWĂƚĞůůŝĚĂĞĞŶ ůŐĠƌŝĞWƵďďůŝĐĂnjŝŽŶŝĚĞůůĂ^ƚĂnjŝŽŶĞŽŽůŽŐŝĐĂEĂƉŽůŝϯϵ García‐Gómez, J. C., López‐Fé, C. M., Espinosa, F., Guerra‐García, J. M., & Rivera‐ /ŶŐƌĂŚĂŵ ' ;ϮϬϭϭͿ Marine artificial micro‐reserves: A possibility for the ĐŽŶƐĞƌǀĂƚŝŽŶŽĨĞŶĚĂŶŐĞƌĞĚƐƉĞĐŝĞƐůŝǀŝŶŐŽŶĂƌƚŝĨŝĐŝĂůƐƵďƐƚƌĂƚĂDĂƌŝŶĞĐŽůŽŐLJ ϯϮ;ϭͿϲͲϭϰŚƚƚƉƐĚŽŝŽƌŐϭϬϭϭϭϭũϭϰϯϵͲϬϰϴϱϮϬϭϬϬϬϰϬϵdž García‐Gómez, J. C., Guerra‐García, J. M., Espinosa, F., Maestre, M. J., Rivera‐Ingraham, '&Ă& López‐Fé, C. M. (2015). Artificial Marine Micro‐Reserves Networks ;DDZEƐͿĂŶŝŶŶŽǀĂƚŝǀĞĂƉƉƌŽĂĐŚƚŽĐŽŶƐĞƌǀĞŵĂƌŝŶĞůŝƚƚŽƌĂůďŝŽĚŝǀĞƌƐŝƚLJĂŶĚ ƉƌŽƚĞĐƚ ĞŶĚĂŶŐĞƌĞĚ ƐƉĞĐŝĞƐ DĂƌŝŶĞ ĐŽůŽŐLJ ϯϲ;ϯͿ ϮϱϵͲϮϳϳ ŚƚƚƉƐĚŽŝŽƌŐϭϬϭϭϭϭũϭϰϯϵͲϬϰϴϱϮϬϭϬϬϬϰϬϵdž 'ŝďƐŽŶZƚŬŝŶƐŽŶZΘ'ŽƌĚŽŶ:;ϮϬϬϳͿ>ŽƐƐƐƚĂƚƵƐĂŶĚƚƌĞŶĚƐĨŽƌĐŽĂƐƚĂůŵĂƌŝŶĞ ŚĂďŝƚĂƚƐŽĨƵƌŽƉĞKĐĞĂŶŽŐƌĂƉŚLJĂŶĚDĂƌŝŶĞŝŽůŽŐLJĂŶĂŶŶƵĂůƌĞǀŝĞǁϰϱϯϰϱͲ ϰϬϱŚƚƚƉƐĚŽŝŽƌŐϭϬϭϮϬϭϵϳϴϭϰϮϬϬϱϬϵϰϯ 'ŝůůDĂƐĐŝĂDŚŵĂĚŝĂ'E'ůĞǁ>>ĞƐƚĞƌ^ĂƌŶĞƐDĞƚĂů;ϮϬϭϳͿ ĂƉĂĐŝƚLJƐŚŽƌƚĨĂůůƐŚŝŶĚĞƌƚŚĞƉĞƌĨŽƌŵĂŶĐĞŽĨŵĂƌŝŶĞƉƌŽͲƚĞĐƚĞĚĂƌĞĂƐŐůŽďĂůůLJ EĂƚƵƌĞϱϰϯϲϲϱ–ϲϲϵŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϯϴŶĂƚƵƌĞϮϭϳϬϴ 'ŝƚƚŵĂŶZ<&ŽĚƌŝĞ&:WŽƉŽǁŝĐŚD<ĞůůĞƌƌƵŶŽ:&ƵƌƌŝŶΘ WŝĞŚůĞƌ D & ;ϮϬϭϱͿ ŶŐŝŶĞĞƌŝŶŐ ĂǁĂLJ ŽƵƌ ŶĂƚƵƌĂů ĚĞĨĞŶƐĞƐ ĂŶ ĂŶĂůLJƐŝƐ ŽĨ ƐŚŽƌĞůŝŶĞŚĂƌĚĞŶŝŶŐŝŶƚŚĞh^&ƌŽŶƚŝĞƌƐŝŶĐŽůŽŐLJĂŶĚƚŚĞŶǀŝƌŽŶŵĞŶƚϭϯ;ϲͿϯϬϭͲ ϯϬϳŚƚƚƉƐĚŽŝŽƌŐϭϬϭϴϵϬϭϱϬϬϲϱ ,ĞĞŶĂŶ'ŽƌŽƐƉĞ<tŝůůŝĂŵƐ/>ĞǀŝŶĞDĂƵƌŝŶWEĂĚŽŶDĞƚĂů;ϮϬϭϲͿ ĐŽƐLJƐƚĞŵ ŵŽŶŝƚŽƌŝŶŐ ĨŽƌ ĞĐŽƐLJƐƚĞŵͲďĂƐĞĚ ŵĂŶĂŐĞŵĞŶƚ hƐŝŶŐ Ă ƉŽůLJĐĞŶƚƌŝĐ ĂƉƉƌŽĂĐŚƚŽďĂůĂŶĐĞŝŶĨŽƌŵĂƚŝŽŶƚƌĂĚĞͲŽĨĨƐ:ŽƵƌŶĂůŽĨƉƉůŝĞĚĐŽůŽŐLJϱϯϲϵϵ– ϳϬϰŚƚƚƉƐĚŽŝŽƌŐϭϬϭϭϭϭϭϯϲϱͲϮϲϲϰϭϮϲϯϯ :ĂĐŬƐŽŶ:<ŝƌďLJDyĞƌŐĞƌt,ũŽƌŶĚĂů<ŽƚƐĨŽƌĚ>tŽƵƌƋƵĞ: ΘtĂƌŶĞƌZZ;ϮϬϬϭͿ,ŝƐƚŽƌŝĐĂůŽǀĞƌĨŝƐŚŝŶŐĂŶĚƚŚĞƌĞĐĞŶƚĐŽůůĂƉƐĞŽĨĐŽĂƐƚĂů ĞĐŽƐLJƐƚĞŵƐ ^ĐŝĞŶĐĞ Ϯϵϯ;ϱϱϯϬͿ ϲϮϵͲϲϯϳ ŚƚƚƉƐĚŽŝŽƌŐϭϬϭϭϮϲƐĐŝĞŶĐĞϭϬϱϵϭϵϵ <ŽůďĞƌƚdŚĞ^ŝdžƚŚdžƚŝŶĐƚŝŽŶŶhŶŶĂƚƵƌĂů,ŝƐƚŽƌLJΘůĂĐŬϮϬϭϰ <ŽŶŝƐŚŝ , ;ϮϬϬϬͿ &ŽƌŵĂƚŝŽŶ ŽĨ ŚƵď ĐŝƚŝĞƐ dƌĂŶƐƉŽƌƚĂƚŝŽŶ ĐŽƐƚ ĂĚǀĂŶƚĂŐĞ ĂŶĚ ƉŽƉƵůĂƚŝŽŶ ĂŐŐůŽŵĞƌĂƚŝŽŶ :ŽƵƌŶĂů ŽĨ hƌďĂŶ ĐŽŶŽŵŝĐƐ ϰϴ;ϭͿ ϭ–Ϯϴ ŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϬϲũƵĞĐϭϵϵϵϮϭϱϬ >ƵƋƵĞ'ƵĂůůĂƌƚ:'ŽŶnjĄůĞnj:dΘWŽůĂD;ϮϬϭϴͿZĞĐŽƉŝůĂĐŝſŶLJĂŶĄůŝƐŝƐĚĞůĂ ŝŶĨŽƌŵĂĐŝſŶ ĐŝĞŶƚşĨŝĐĂĚŝƐƉŽŶŝďůĞƐŽďƌĞ WĂƚĞůůĂ ĨĞƌƌƵŐŝŶĞĂ^ŽĐŝĞĚĂĚƐƉĂŹŽůĂĚĞ DĂůĂĐŽůŽŐşĂ DĂĞƐƚƌĞĞůŐĂĚŽD:ƐƉŝŶŽƐĂdŽƌƌĞ&&ĂWĂǀſŶWĂŶĞƋƵĞΘ'Ăƌкà 'ſŵĞnj:;ϮϬϭϴͿƐƚĂĚŽĚĞůĂƉŽďůĂĐŝſŶĚĞWĂƚĞůůĂ ĨĞƌƌƵŐŝŶĞĂĞŶĞůĄƌĞĂĚĞů ĞƐƚƌĞĐŚŽĚĞ'ŝďƌĂůƚĂƌůŵŽƌĂŝŵĂZĞǀŝƐƚĂĚĞƐƚƵĚŝŽƐĂŵƉŽŐŝďƌĂůƚĂƌĞŹŽƐϰϵϭϭϱͲ ϭϯϬ DŝƚƐĐŚt:;ϮϬϭϮͿtŚĂƚŝƐĞĐŽůŽŐŝĐĂůĞŶŐŝŶĞĞƌŝŶŐĐŽůŽŐŝĐĂůŶŐŝŶĞĞƌŝŶŐϰϱϱͲϭϮ ŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϭϲũĞĐŽůĞŶŐϮϬϭϮϬϰϬϭϯ DŽƌĞŶŽΘƌƌŽLJŽDϮϬϬϴWĂƚĞůůĂĨĞƌƌƵŐŝŶĞĂ'ŵĞůŝŶϭϳϵϭŶ>ŝďƌŽZŽũŽĚĞůŽƐ /ŶǀĞƌƚĞďƌĂĚŽƐ ĚĞ ŶĚĂůƵкà ƉƉ ϯϬϴͲϯϭϵ ĚƐ ĂƌĞĂͲnjĐſŶ : D ĂůůĞƐƚĞƌŽƐͲ ƵƉĞƌſŶ Θ DŽƌĞŶŽ ŽŶƐĞũĞƌşĂ ĚĞ DĞĚŝŽ ŵďŝĞŶƚĞ :ƵŶƚĂ ĚĞ ŶĚĂůƵкà ^ĞǀŝůůĂ^ƉĂŝŶ EĂŚƵĞůŚƵĂů > sĞƌŐĂƌĂ y :ƵůůŝĂŶ ĂƌŵŽŶĂ Θ ĂŵƉŽƐ ' ;ϮϬϭϵͿ ^ĞƌǀŝĐŝŽƐ ĞĐŽƐŝƐƚĠŵŝĐŽƐŵĂƌŝŶŽͲĐŽƐƚĞƌŽƐĞŶůĂZĞŐŝſŶĚĞDĂŐĂůůĂŶĞƐLJůĂŶƚĄƌƚŝĐĂŚŝůĞŶĂ ĞŶƚƌŽ ĚĞ /ŶǀĞƐƚŝŐĂĐŝſŶ ŝŶĄŵŝĐĂ ĚĞ ĐŽƐŝƐƚĞŵĂƐ DĂƌŝŶŽƐ ĚĞ ůƚĂƐ >ĂƚŝƚƵĚĞƐ /> EĂLJůŽƌ><ŝƉƉĞŶ,DĂĐƌƚŚƵƌD,ĂŶƐŽŵ:sŽǀŝĚĞƐ'ĂůĚşǀĂƌͲ:ŝŵĠŶĞnj ΘWĠƌĞnjͲĞďĂůůŽƐZ;ϮϬϮϬͿhƌďĂŶĞƐƚƵĂƌŝĞƐĂŶĚĐŽĂƐƚƐ/Ŷ/ŽƵŐůĂƐWD>
54 ŶĚĞƌƐŽŶ'ŽŽĚĞD,ŽƵĐŬDĂĚĚŽdž,EĂŐĞŶĚƌĂΘdWzŽŬ;ĚƐͿdŚĞ ZŽƵƚůĞĚŐĞ ŚĂŶĚŬ ŽĨ ƵƌďĂŶ ĞĐŽůŽŐLJ >ŽŶĚŽŶ h< ZŽƵƚůĞĚŐĞ ,ĂŶĚŬƐ ŚƚƚƉƐĚŽŝŽƌŐϭϬϰϯϮϰϵϳϴϬϰϮϵϱϬϲϳϱϴ EĞƵŵĂŶŶsĂĨĞŝĚŝƐdŝŵŵĞƌŵĂŶŶ:ΘEŝĐŚŽůůƐZ:;ϮϬϭϱͿ&ƵƚƵƌĞĐŽĂƐƚĂů ƉŽƉƵůĂƚŝŽŶ ŐƌŽǁƚŚ ĂŶĚ ĞdžƉŽƐƵƌĞ ƚŽ ƐĞĂͲůĞǀĞů ƌŝƐĞ ĂŶĚ ĐŽĂƐƚĂů ĨůŽŽĚŝŶŐͲĂ ŐůŽďĂů ĂƐƐĞƐƐŵĞŶƚ WůŽ^ ŽŶĞ ϭϬ;ϯͿ ĞϬϭϭϴϱϳϭ ŚƚƚƉƐĚŽŝŽƌŐϭϬϭϯϳϭũŽƵƌŶĂůƉŽŶĞϬϭϭϴϱϳϭ WĂƌĂĐƵĞůůŽƐ D EĞǀĂĚŽ : DŽƌĞŶŽ 'ŝŵĠŶĞnj Θ ůĞƐŝŶĂ : : ;ϮϬϬϯͿ ŽŶƐĞƌǀĂƚŝŽŶĂůƐƚĂƚƵƐĂŶĚĚĞŵŽŐƌĂƉŚŝĐĐŚĂƌĂĐƚĞƌŝƐƚŝĐƐŽĨWĂƚĞůůĂĨĞƌƌƵŐŝŶĞĂ'ŵĞůŝŶ ϭϳϵϭ ;DŽůůƵƐĐĂ ŐĂƐƚƌŽƉŽĚĂͿ ŽŶ ƚŚĞ ůďŽƌĂŶ /ƐůĂŶĚ ;tĞƐƚĞƌŶ DĞĚŝƚĞƌƌĂŶĞĂŶͿ ŶŝŵĂůŝŽĚŝǀĞƌƐŝƚLJĂŶĚŽŶƐĞƌǀĂƚŝŽŶϮϲ;ϮͿϮϵͲϯϳ WƌŽďĞƌƚW<;ϮϬϭϳͿDĂƌŝŶĞĐŽŶƐĞƌǀĂƚŝŽŶĂŵďƌŝĚŐĞhŶŝǀĞƌƐŝƚLJWƌĞƐƐ ŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϭϳϵϳϴϭϭϯϵϬϰϯϱϴϴ ZĂĨĨĂĞůůŝ Θ ,ĂǁŬŝŶƐ ^ : ;ϭϵϵϲͿ /ŶƚĞƌƚŝĚĂů ĞĐŽůŽŐLJ ^ƉƌŝŶŐĞƌ ^ĐŝĞŶĐĞ Θ ƵƐŝŶĞƐƐ DĞĚŝĂŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϬϳϵϳϴͲϵϰͲϬϬϵͲϭϰϴϵͲϲ ZŝǀĞƌĂͲ/ŶŐƌĂŚĂŵ ' ƐƉŝŶŽƐĂ & Θ 'ĂƌĐşĂͲ'ſŵĞnj : ;ϮϬϭϭͿ ŶǀŝƌŽŶŵĞŶƚĂůůLJ ŵĞĚŝĂƚĞĚ ƐĞdž ĐŚĂŶŐĞ ŝŶ ƚŚĞ ĞŶĚĂŶŐĞƌĞĚ ůŝŵƉĞƚ WĂƚĞůůĂ ĨĞƌƌƵŐŝŶĞĂ ;'ĂƐƚƌŽƉŽĚĂ WĂƚĞůůŝĚĂĞͿ :ŽƵƌŶĂů ŽĨ DŽůůƵƐĐĂŶ ^ƚƵĚŝĞƐ ϳϳ;ϯͿ ϮϮϲͲϮϯϭ ŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϵϯŵŽůůƵƐĞLJƌϬϬϳ Sardá, R., Requena, S., Dominguez‐Carrió, C., & Gili, J. M. (2017). Ecosystem‐Based DĂŶĂŐĞŵĞŶƚĨŽƌDĂƌŝŶĞWƌŽƚĞĐƚĞĚƌĞĂƐ^LJƐƚĞŵĂƚŝĐƉƉƌŽĂĐŚDĂŶĂŐĞŵĞŶƚŽĨ DĂƌŝŶĞ WƌŽƚĞĐƚĞĚ ƌĞĂƐ EĞƚǁŽƌŬ WĞƌƐƉĞĐƚŝǀĞ ϭϰϱͲ ϭϲϮŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϬϮϵϳϴϭϭϭϵϬϳϱϴϬϲĐŚϴ ^ĐŚƵůnjĞW&ƌŽƐĐŚZZŝƐƐĞƌW'ϭϵϵϲŶŐŝŶĞĞƌŝŶŐǁŝƚŚŝŶĐŽůŽŐŝĐĂůŽŶƐƚƌĂŝŶƚƐ EĂƚŝŽŶĂůĐĂĚĞŵLJWƌĞƐƐtĂƐŚŝŶŐƚŽŶƉƉ ^ĞůůĂ/ΘWĞƌŬŽůͲ&ŝŶŬĞů^;ϮϬϭϱͿůƵĞŝƐƚŚĞŶĞǁŐƌĞĞŶ–ĞĐŽůŽŐŝĐĂůĞŶŚĂŶĐĞŵĞŶƚŽĨ ĐŽŶĐƌĞƚĞďĂƐĞĚĐŽĂƐƚĂůĂŶĚŵĂƌŝŶĞŝŶĨƌĂƐƚƌƵĐƚƵƌĞĐŽůŽŐŝĐĂůŶŐŝŶĞĞƌŝŶŐϴϰϮϲϬ– ϮϳϮŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϭϲũĞĐŽůĞŶŐϮϬϭϱϬϵϬϭϲ ^ĞŵƉĞƌĞͲsĂůǀĞƌĚĞ:'ƵĞƌƌĂͲ'ĂƌĐşĂ:D'ĂƌĐşĂͲ'ſŵĞnj:ΘƐƉŝŶŽƐĂ&;ϮϬϮϯͿ ŽĂƐƚĂů ƵƌďĂŶŝnjĂƚŝŽŶ ĂŶ ŝƐƐƵĞ ĨŽƌ ŵĂƌŝŶĞ ĐŽŶƐĞƌǀĂƚŝŽŶ /Ŷ ŽĂƐƚĂů ,ĂďŝƚĂƚ ŽŶƐĞƌǀĂƚŝŽŶ ;ƉƉ ϰϭͲϳϵͿ ĐĂĚĞŵŝĐ WƌĞƐƐ ŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϭϲϵϳϴͲϬͲϯϮϯͲ ϴϱϲϭϯͲϯϬϬϬϬϳͲϰ ^ŵĂůůΘEŝĐŚŽůůƐZ:;ϮϬϬϯͿŐůŽďĂůĂŶĂůLJƐŝƐŽĨŚƵŵĂŶƐĞƚƚůĞŵĞŶƚŝŶĐŽĂƐƚĂůnjŽŶĞƐ :ŽƵƌŶĂůŽĨĐŽĂƐƚĂůƌĞƐĞĂƌĐŚϱϴϰͲϱϵϵ
55 ŶĚĞƌƐŽŶ'ŽŽĚĞD,ŽƵĐŬDĂĚĚŽdž,EĂŐĞŶĚƌĂΘdWzŽŬ;ĚƐͿdŚĞ ZŽƵƚůĞĚŐĞ ŚĂŶĚŬ ŽĨ ƵƌďĂŶ ĞĐŽůŽŐLJ >ŽŶĚŽŶ h< ZŽƵƚůĞĚŐĞ ,ĂŶĚŬƐ ŚƚƚƉƐĚŽŝŽƌŐϭϬϰϯϮϰϵϳϴϬϰϮϵϱϬϲϳϱϴ EĞƵŵĂŶŶsĂĨĞŝĚŝƐdŝŵŵĞƌŵĂŶŶ:ΘEŝĐŚŽůůƐZ:;ϮϬϭϱͿ&ƵƚƵƌĞĐŽĂƐƚĂů ƉŽƉƵůĂƚŝŽŶ ŐƌŽǁƚŚ ĂŶĚ ĞdžƉŽƐƵƌĞ ƚŽ ƐĞĂͲůĞǀĞů ƌŝƐĞ ĂŶĚ ĐŽĂƐƚĂů ĨůŽŽĚŝŶŐͲĂ ŐůŽďĂů ĂƐƐĞƐƐŵĞŶƚ WůŽ^ ŽŶĞ ϭϬ;ϯͿ ĞϬϭϭϴϱϳϭ ŚƚƚƉƐĚŽŝŽƌŐϭϬϭϯϳϭũŽƵƌŶĂůƉŽŶĞϬϭϭϴϱϳϭ WĂƌĂĐƵĞůůŽƐ D EĞǀĂĚŽ : DŽƌĞŶŽ 'ŝŵĠŶĞnj Θ ůĞƐŝŶĂ : : ;ϮϬϬϯͿ ŽŶƐĞƌǀĂƚŝŽŶĂůƐƚĂƚƵƐĂŶĚĚĞŵŽŐƌĂƉŚŝĐĐŚĂƌĂĐƚĞƌŝƐƚŝĐƐŽĨWĂƚĞůůĂĨĞƌƌƵŐŝŶĞĂ'ŵĞůŝŶ ϭϳϵϭ ;DŽůůƵƐĐĂ ŐĂƐƚƌŽƉŽĚĂͿ ŽŶ ƚŚĞ ůďŽƌĂŶ /ƐůĂŶĚ ;tĞƐƚĞƌŶ DĞĚŝƚĞƌƌĂŶĞĂŶͿ ŶŝŵĂůŝŽĚŝǀĞƌƐŝƚLJĂŶĚŽŶƐĞƌǀĂƚŝŽŶϮϲ;ϮͿϮϵͲϯϳ WƌŽďĞƌƚW<;ϮϬϭϳͿDĂƌŝŶĞĐŽŶƐĞƌǀĂƚŝŽŶĂŵďƌŝĚŐĞhŶŝǀĞƌƐŝƚLJWƌĞƐƐ ŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϭϳϵϳϴϭϭϯϵϬϰϯϱϴϴ ZĂĨĨĂĞůůŝ Θ ,ĂǁŬŝŶƐ ^ : ;ϭϵϵϲͿ /ŶƚĞƌƚŝĚĂů ĞĐŽůŽŐLJ ^ƉƌŝŶŐĞƌ ^ĐŝĞŶĐĞ Θ ƵƐŝŶĞƐƐ DĞĚŝĂŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϬϳϵϳϴͲϵϰͲϬϬϵͲϭϰϴϵͲϲ ZŝǀĞƌĂͲ/ŶŐƌĂŚĂŵ ' ƐƉŝŶŽƐĂ & Θ 'ĂƌĐşĂͲ'ſŵĞnj : ;ϮϬϭϭͿ ŶǀŝƌŽŶŵĞŶƚĂůůLJ ŵĞĚŝĂƚĞĚ ƐĞdž ĐŚĂŶŐĞ ŝŶ ƚŚĞ ĞŶĚĂŶŐĞƌĞĚ ůŝŵƉĞƚ WĂƚĞůůĂ ĨĞƌƌƵŐŝŶĞĂ ;'ĂƐƚƌŽƉŽĚĂ WĂƚĞůůŝĚĂĞͿ :ŽƵƌŶĂů ŽĨ DŽůůƵƐĐĂŶ ^ƚƵĚŝĞƐ ϳϳ;ϯͿ ϮϮϲͲϮϯϭ ŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϵϯŵŽůůƵƐĞLJƌϬϬϳ Sardá, R., Requena, S., Dominguez‐Carrió, C., & Gili, J. M. (2017). Ecosystem‐Based DĂŶĂŐĞŵĞŶƚĨŽƌDĂƌŝŶĞWƌŽƚĞĐƚĞĚƌĞĂƐ^LJƐƚĞŵĂƚŝĐƉƉƌŽĂĐŚDĂŶĂŐĞŵĞŶƚŽĨ DĂƌŝŶĞ WƌŽƚĞĐƚĞĚ ƌĞĂƐ EĞƚǁŽƌŬ WĞƌƐƉĞĐƚŝǀĞ ϭϰϱͲ ϭϲϮŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϬϮϵϳϴϭϭϭϵϬϳϱϴϬϲĐŚϴ ^ĐŚƵůnjĞW&ƌŽƐĐŚZZŝƐƐĞƌW'ϭϵϵϲŶŐŝŶĞĞƌŝŶŐǁŝƚŚŝŶĐŽůŽŐŝĐĂůŽŶƐƚƌĂŝŶƚƐ EĂƚŝŽŶĂůĐĂĚĞŵLJWƌĞƐƐtĂƐŚŝŶŐƚŽŶƉƉ ^ĞůůĂ/ΘWĞƌŬŽůͲ&ŝŶŬĞů^;ϮϬϭϱͿůƵĞŝƐƚŚĞŶĞǁŐƌĞĞŶ–ĞĐŽůŽŐŝĐĂůĞŶŚĂŶĐĞŵĞŶƚŽĨ ĐŽŶĐƌĞƚĞďĂƐĞĚĐŽĂƐƚĂůĂŶĚŵĂƌŝŶĞŝŶĨƌĂƐƚƌƵĐƚƵƌĞĐŽůŽŐŝĐĂůŶŐŝŶĞĞƌŝŶŐϴϰϮϲϬ– ϮϳϮŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϭϲũĞĐŽůĞŶŐϮϬϭϱϬϵϬϭϲ ^ĞŵƉĞƌĞͲsĂůǀĞƌĚĞ:'ƵĞƌƌĂͲ'ĂƌĐşĂ:D'ĂƌĐşĂͲ'ſŵĞnj:ΘƐƉŝŶŽƐĂ&;ϮϬϮϯͿ ŽĂƐƚĂů ƵƌďĂŶŝnjĂƚŝŽŶ ĂŶ ŝƐƐƵĞ ĨŽƌ ŵĂƌŝŶĞ ĐŽŶƐĞƌǀĂƚŝŽŶ /Ŷ ŽĂƐƚĂů ,ĂďŝƚĂƚ ŽŶƐĞƌǀĂƚŝŽŶ ;ƉƉ ϰϭͲϳϵͿ ĐĂĚĞŵŝĐ WƌĞƐƐ ŚƚƚƉƐĚŽŝŽƌŐϭϬϭϬϭϲϵϳϴͲϬͲϯϮϯͲ ϴϱϲϭϯͲϯϬϬϬϬϳͲϰ ^ŵĂůůΘEŝĐŚŽůůƐZ:;ϮϬϬϯͿŐůŽďĂůĂŶĂůLJƐŝƐŽĨŚƵŵĂŶƐĞƚƚůĞŵĞŶƚŝŶĐŽĂƐƚĂůnjŽŶĞƐ :ŽƵƌŶĂůŽĨĐŽĂƐƚĂůƌĞƐĞĂƌĐŚϱϴϰͲϱϵϵ hŶŝƚĞĚ EĂƚŝŽŶƐ ;ϮϬϭϵͿ tŽƌůĚ ƉŽƉƵůĂƚŝŽŶ ƉƌŽƐƉĞĐƚƐ EĞǁ zŽƌŬ h^ hŶŝƚĞĚ EĂƚŝŽŶƐ WƵďůŝĐĂƚŝŽŶƐŚƚƚƉƐƉŽƉƵůĂƚŝŽŶƵŶŽƌŐǁƵƉ hŶŝƚĞĚ EĂƚŝŽŶƐ ;ϮϬϮϬͿ ZĞǀŝĞǁ ŽĨ ŵĂƌŝƚŝŵĞ ƚƌĂŶƐƉŽƌƚ ϮϬϮϬ EĞǁ zŽƌŬ h^ hŶŝƚĞĚ EĂƚŝŽŶƐ WƵďůŝĐĂƚŝŽŶƐ ŚƚƚƉƐƵŶĐƚĂĚŽƌŐǁĞďĨůLJĞƌƌĞǀŝĞǁͲŵĂƌŝƚŝŵĞͲƚƌĂŶƐƉŽƌƚͲ ϮϬϮϬ
IV. PUBLICACIÓN 1. CREACIÓN DE MICROHÁBITATS (POZAS INTERMAREALES) EN ESCOLLERAS CON COMUNIDADES BIOLÓGICAS EN ETAPA CLÍMAX DE SU SUCESIÓN ECOLÓGICA COMO FORMA DE MITIGAR LOS EFECTOS NEGATIVOS DEL SUSTRATO ARTIFICIAL SOBRE LA BIODIVERSIDAD MARINA.
57 IV. PUBLICACIÓN 1. CREACIÓN DE MICROHÁBITATS (POZAS INTERMAREALES) EN ESCOLLERAS CON COMUNIDADES BIOLÓGICAS EN ETAPA CLÍMAX DE SU SUCESIÓN ECOLÓGICA COMO FORMA DE MITIGAR LOS EFECTOS NEGATIVOS DEL SUSTRATO ARTIFICIAL SOBRE LA BIODIVERSIDAD MARINA.
64 a clearer transition from control to tidepools occurs within artificial substrate, indicating a stronger “halo effect”from the created tidepools (Fig. 6). The percentage of vagile species individuals found on each artificial substrate treatment one year after blazing pools is plotted in Fig. 7. The creation of these microhabitats has allowed for settling of species such as Pisania striata,Phorcus turbinatus,Fissurella sp. and Lepidochitona sp., which were not found in the emergent rock of breakwaters. 4. Discussion Among the different results that this study has, it stands out that local biodiversity notably increased in just one year after the creation of intertidal tidepools on the already built coastal defence structures. In addition, some vagile species, that had been previously excluded from the adjacent emergent rock were found inside tidepools, demonstrating that this management actuation contributes to the reduction of these species populations fragmentation. The colonisation of tidepools and the halo around them reached the same species richness and Shannon diversity levels as the adjacent emergent rock (control) only three months after their creation. In this primary ecological succession, the colonization of tidepools was dominated by biofilm and Ralfsia verrucosa. After one year, tidepools were significantly different from the other two treatments and exceeded control species richness by 39.21% and control diversity by 30.70%. Focusing on the type of species, some vagile fauna which only had been found on the adjacent natural rocky shore or in low abundances on the riprap structures, were also observed in the created tidepools. Species of gastropods like Pisania striata,Osilinus turbinatus or Fisurella sp. and the polyplacophora Lepidochitona sp. were regularly found in the tidepool. It is remarkable that characteristic species of the infra-littoral level such as Paracentrotus sp.,mostly young individuals, and Aiptasia sp. were also observed exclusively inside pools. Additionally, the species Siphonaria pectinata increased its presence in the created tidepools, with these becoming an appropriated habitat for laying of their egg masses. Conversely, Patella ferruginea and Patella caerulea have not shown attraction to this microhabitat. However, green opportunistic algae such as Ulva rigida were found inside artificial pools (sometimes with coverage of up to 100%) as reported by Evans (Evans et al., 2016) for Ulva intestinalis in the UK, and Browne and Chapman (Browne and Chapman, 2011) for Ulva lactuca in Australia. Focusing on the tidepool halo (5 cm) multivariate analyses showed that the biological assemblages were different between halo and emerged rock, indicating that the new habitat created within the artificial structures extends its influence beyond the limits of the tidepools. As pointed out by Evans (Evans et al., 2016), artificial rock pools cannot yet be considered fully functionally equivalent to natural rock pools, but successional trajectories suggest that climax communities could converge over time, as is also found in the present study. In fact, Firth (Firth et al., 2013) analysed mature communities and reported similar values of species richness in pools on artificial and natural substrate. Previous studies have shown a decrease in diversity in pools with increasing intertidal height (Kooistra et al., 1989). In fact, Firth (Firth et al., 2013) found lower species richness on the higher intertidal level both in natural and artificial rock pools. However, our results did not find a significant difference in species richness or diversity between ‘high’and ‘low’levels on artificial substrate. Nevertheless, assemblage composition was different between the levels. This difference with Firth’s results (Firth et al., 2013) could be caused by the great difference in the tidal coefficient between the two studied areas, the southwest UK coast and the Strait of Gibraltar (present study). The community in artificial tidepools reflects a similar succession on both tidal levels and these results are consistent with an immature community of primary colonisers. Then, it would be plausible to expect a progressive differentiation between upper and lower Table 2 Multivariate RM-PERMANOVA and PERMIDISP dispersion results on natural and arti fi cial substrate datasets. Ti: time, T1: spring 2014, T2: summer 2014, T3: autumn 2014 and T4: winter 2015, Le: level, Tr: treatment, Tid: tidepool, 5 cm: halo perimeter, Con: control. Bold font: p < 0.05 and interaction between di fferent factors. Source Df MS Pseudo-F RM-PERMANOVA PERMDISP MS Pseudo-F RM-PERMANOVA PERMDISP P (perm) Pairwise comparisons P (perm) Pairwise comparisons P (perm) Pairwise comparisons P (perm) Pairwise comparisons NATURAL ARTIFICIAL Time 3 10,579 4.8165 < 0.001 T1 ≠T2 ≠T3 ≠T4 0.81 9785 4.6714 < 0.001 T1 ≠T2 ≠T3 ≠T4 < 0.05 T1 = T2 < T3 > T4 Level 1 131,080 59.681 < 0.001 Down ≠Up < 0.001 Down < Up 52,823 25.218 < 0.001 Down ≠Up 0.78 Treatment 2 20,518 9.3418 < 0.001 Tid ≠(5 cm = Con) 0.45 55,734 26.607 < 0.001 Tid ≠5 cm ≠Con < 0.001 (Tid = 5 cm) < Con Ti × Le 3 5223.7 2.3783 < 0.001 T1, T2, T3, T4: Down ≠Up Le × Tr Down: (Tid > 5 cm) = Con Up: Tid = 5 cm = Con 2869.9 1.3701 0.12 Ti × Tr T1, T2: Con > (5cm = Tid) T3: Con = 5 cm = Tid T4: Con > 5 cm > Tid Down: (Tid = 5 cm) > Con Up: (Tid < Con) = 5 cm Ti × Tr 6 1485.7 0.67641 0.96 3815.4 1.8215 < 0.05 T1, T2, T3, T4 : Tid ≠5 cm ≠Con < 0.001 Le × Tr 2 8042.1 3.6615 < 0.001 Down, Up: Tid ≠(5 cm = Con) < 0.05 10,404 4.967 < 0.001 Down, Up: Tid ≠5 cm ≠Con < 0.001 Residuals 223 2196.4 2094.7 E. Ostalé-Valriberas et al. Ecological Engineering 120 (2018) 522–531 527
65 a clearer transition from control to tidepools occurs within artificial substrate, indicating a stronger “halo effect”from the created tidepools (Fig. 6). The percentage of vagile species individuals found on each artificial substrate treatment one year after blazing pools is plotted in Fig. 7. The creation of these microhabitats has allowed for settling of species such as Pisania striata,Phorcus turbinatus,Fissurella sp. and Lepidochitona sp., which were not found in the emergent rock of breakwaters. 4. Discussion Among the different results that this study has, it stands out that local biodiversity notably increased in just one year after the creation of intertidal tidepools on the already built coastal defence structures. In addition, some vagile species, that had been previously excluded from the adjacent emergent rock were found inside tidepools, demonstrating that this management actuation contributes to the reduction of these species populations fragmentation. The colonisation of tidepools and the halo around them reached the same species richness and Shannon diversity levels as the adjacent emergent rock (control) only three months after their creation. In this primary ecological succession, the colonization of tidepools was dominated by biofilm and Ralfsia verrucosa. After one year, tidepools were significantly different from the other two treatments and exceeded control species richness by 39.21% and control diversity by 30.70%. Focusing on the type of species, some vagile fauna which only had been found on the adjacent natural rocky shore or in low abundances on the riprap structures, were also observed in the created tidepools. Species of gastropods like Pisania striata,Osilinus turbinatus or Fisurella sp. and the polyplacophora Lepidochitona sp. were regularly found in the tidepool. It is remarkable that characteristic species of the infra-littoral level such as Paracentrotus sp.,mostly young individuals, and Aiptasia sp. were also observed exclusively inside pools. Additionally, the species Siphonaria pectinata increased its presence in the created tidepools, with these becoming an appropriated habitat for laying of their egg masses. Conversely, Patella ferruginea and Patella caerulea have not shown attraction to this microhabitat. However, green opportunistic algae such as Ulva rigida were found inside artificial pools (sometimes with coverage of up to 100%) as reported by Evans (Evans et al., 2016) for Ulva intestinalis in the UK, and Browne and Chapman (Browne and Chapman, 2011) for Ulva lactuca in Australia. Focusing on the tidepool halo (5 cm) multivariate analyses showed that the biological assemblages were different between halo and emerged rock, indicating that the new habitat created within the artificial structures extends its influence beyond the limits of the tidepools. As pointed out by Evans (Evans et al., 2016), artificial rock pools cannot yet be considered fully functionally equivalent to natural rock pools, but successional trajectories suggest that climax communities could converge over time, as is also found in the present study. In fact, Firth (Firth et al., 2013) analysed mature communities and reported similar values of species richness in pools on artificial and natural substrate. Previous studies have shown a decrease in diversity in pools with increasing intertidal height (Kooistra et al., 1989). In fact, Firth (Firth et al., 2013) found lower species richness on the higher intertidal level both in natural and artificial rock pools. However, our results did not find a significant difference in species richness or diversity between ‘high’and ‘low’levels on artificial substrate. Nevertheless, assemblage composition was different between the levels. This difference with Firth’s results (Firth et al., 2013) could be caused by the great difference in the tidal coefficient between the two studied areas, the southwest UK coast and the Strait of Gibraltar (present study). The community in artificial tidepools reflects a similar succession on both tidal levels and these results are consistent with an immature community of primary colonisers. Then, it would be plausible to expect a progressive differentiation between upper and lower Table 2 Multivariate RM-PERMANOVA and PERMIDISP dispersion results on natural and artificial substrate datasets. Ti: time, T1: spring 2014, T2: summer 2014, T3: autumn 2014 and T4: winter 2015, Le: level, Tr: treatment, Tid: tidepool, 5 cm: halo perimeter, Con: control. Bold font: p < 0.05 and interaction between different factors. Source Df MS Pseudo-F RM-PERMANOVA PERMDISP MS Pseudo-F RM-PERMANOVA PERMDISP P (perm) Pairwise comparisons P (perm) Pairwise comparisons P (perm) Pairwise comparisons P (perm) Pairwise comparisons NATURAL ARTIFICIAL Time 3 10,579 4.8165 < 0.001 T1 ≠T2 ≠T3 ≠T4 0.81 9785 4.6714 < 0.001 T1 ≠T2 ≠T3 ≠T4 < 0.05 T1 = T2 < T3 > T4 Level 1 131,080 59.681 < 0.001 Down ≠Up < 0.001 Down < Up 52,823 25.218 < 0.001 Down ≠Up 0.78 Treatment 2 20,518 9.3418 < 0.001 Tid ≠(5 cm = Con) 0.45 55,734 26.607 < 0.001 Tid ≠5 cm ≠Con < 0.001 (Tid = 5 cm) < Con Ti × Le 3 5223.7 2.3783 < 0.001 T1, T2, T3, T4: Down ≠Up Le × Tr Down: (Tid > 5 cm) = Con Up: Tid = 5 cm = Con 2869.9 1.3701 0.12 Ti × Tr T1, T2: Con > (5cm = Tid) T3: Con = 5 cm = Tid T4: Con > 5 cm > Tid Down: (Tid = 5 cm) > Con Up: (Tid < Con) = 5 cm Ti × Tr 6 1485.7 0.67641 0.96 3815.4 1.8215 < 0.05 T1, T2, T3, T4 : Tid ≠5 cm ≠Con < 0.001 Le × Tr 2 8042.1 3.6615 < 0.001 Down, Up: Tid ≠(5 cm = Con) < 0.05 10,404 4.967 < 0.001 Down, Up: Tid ≠5 cm ≠Con < 0.001 Residuals 223 2196.4 2094.7 E. Ostalé-Valriberas et al. Ecological Engineering 120 (2018) 522–531 527 tidepools in the future, while the community matures, showing a similar trend as that of natural areas. In accordance with previous literature, the artificial substrate hosted lower species richness and diversity as well as different assemblages compared with those found on natural rocky shores (Glasby, 1999; Glasby and Connell, 1999; Chapman and Bulleri, 2003; Bulleri and Chapman, 2004; Moschella et al., 2005; Firth et al., 2013; Aguilera et al., 2014). Similarly, the riprap coastal defence structures on the Strait of Gibraltar support lower diversity than adjacent natural hard substrate, particularly for vagile fauna. The assemblages recorded in natural substrate at low tidal levels showed high values of species richness, diversity and a more homogeneous composition among treatments, probably due to the more benign environment (Martins et al., 2007). Conversely, the high tide level on artificial substrate Table 3 SIMPER analysis showing contribution of different taxa to similarity within treatments at different substrates and levels (breakdown: 92%). Results include average abundance of each taxa (Avg) and its relative contribution to the overall group similarity (ϐ%). Artificial Natural Down Up Down Up Tidepool 5 cm Control Tidepool 5 cm Control Tidepool 5 cm Control Tidepool 5 cm Control Avg ϐ% Avg ϐ% Avg ϐ% Avg ϐ% Avg ϐ% Avg ϐ% Avg ϐ% Avg ϐ% Avg ϐ% Avg ϐ% Avg ϐ% Avg ϐ% Verrucaria maura 00000000000000000000001.96.5 Biofilm 15.9 30.5 4.1 9.7 2.1 8.3 25.7 48.7 9.3 20.1 3.3 8.2 0.8 1.9 0 0 0 0 2.4 8.2 0 0 0 0 Ralfsia verrucosa 10 19 24.6 57.8 7.3 28.7 9.6 18.2 15.5 33.8 8.8 21.9 6.8 17 5.2 11.4 8 18.4 8.3 27.9 2.8 7.7 1.6 5.7 Hidenbrandia rubra 1.6 3.09 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 2 2.9 9.9 10.3 28.7 3.6 12.2 Lithophyllum incrustans 14.7 28.1 1.4 3.3 0 0 6.2 11.7 0 0 0 0 4.5 11.4 0 0 0 0 1.6 5.3 0 0 0 0 Corallina sp. 2 3.9 4.6 10.9 6.7 26.2 0 0 0 0 0 0 19.8 49.3 22.3 49.2 14.9 34.2 3.1 10.5 0 0 0 0 Red filamentous algae 3.15.90000000000000000000000 Caulacanthus ustulatus 0 0 1.1 2.7 1 3.8 0 0 0 0 0 0 0 0 2.1 4.7 1.6 3.6 0 0 1.8 4.9 3.1 10.5 Gelidium sp. 0 0 0 0 1.8 7.1 0 0 0 0 0 0 0 0 1.3 2.8 3 6.8 0 0 0 0 0 0 Ceramium sp. 3.7 9.3 5.3 11.7 4.4 10 0 0 0 0 0 0 Ulva sp. 0000001.32.5000000001.32.9000000 Ulva rigida 000000000000001.12.524.600000.82.7 Chaetomorpha aerea 0000000000000000001.86.10000 Chthamalus sp. 0 0 0 0 1.6 6.3 2.2 4.2 13.6 29.6 18.5 46 0 0 4.2 9.3 4.1 9.3 3.9 13.2 13.3 37 12.9 44.5 Siphonaria pectinata 0 0 2.3 5.5 1.8 7.2 3.8 7.2 0 0 2.9 7.3 0 0 0 0 0 0 3.2 11 0 0 0 0 Patella caerulea 0 0 1.2 2.7 1.5 5.8 0 0 4.7 10.1 1.5 3.7 0 0 0 0 0 0 0 0 0 0 0 0 Patella ferruginea 00000000002.4600000000000.72.3 Melarhaphe neritoides 000000000000000000004.713.21.75.9 Anemonia sulcata 0000000000000.71.80000000000 Fig. 5. Species richness and Shannon diversity (mean ± SD) for natural and artificial substrate according to the factors time (T1: spring 2014, T2: summer 2014, T3: autumn 2014 and T4: winter 2015), level and treatment. E. Ostalé-Valriberas et al. Ecological Engineering 120 (2018) 522–531 528
66 showed lower biodiversity and more heterogeneous assemblages, due to harsh conditions driven by desiccation (see Raffaelli and Hawkins, 1996). Finally, high levels on natural substrates and low levels on artificial ones showed intermediate values of diversity and heterogeneous assemblages, in accordance with the intermediate perturbation hypothesis (Connell, 1978). Focusing on the description of biological assemblages in this type of microhabitats within the natural environment, it is proven that tidal height is an important structuring force for rocky intertidal communities (Underwood et al., 1984). Furthermore, Martins (Martins et al., 2007) showed consistent differences in the assemblages in natural rock pools at different heights. In this sense, the results of the present study also showed strong differences between low and high midlittoral levels, the lower level having the highest values of diversity and species richness. 4.1. Conclusions and management implications The creation of small tidepools on breakwaters during or after structure construction is an affordable method that should be taken into account due to the substantial ecological benefits it provides. In fact, the present study shows a significant increase of species richness and Shannon diversity in one year even in a coastal defence structure that has reached a steady state climax community. Besides, it has been demonstrated that the creation of this microhabitat has allowed several species of vagile fauna to colonize the intertidal habitat. According to Underwood (Underwood and Skilleter, 1996) and Martins (Martins et al., 2007), better results can be expected with the creation of greater and deeper tidepools. For the creation of pools, a hydraulic jackhammer (present study) or diamond-tipped bits of variable diameters can be used (Underwood and Skilleter, 1996; Evans et al., 2016). Previous experiences have revealed that the artificial structures preserve their integrity, indicating that this is a long-term option which is resistant to storms and wave action (see Firth et al., 2016). From a conservationist point of view, the creation of these intertidal water-retaining microhabitats in artificial structures has two major benefits. First, tidepools produce refuge for vagile species and their egg masses. These species had only been observed in natural rocky shores; hence artificial tidepools reduce habitat fragmentation and enhance population connectivity. Second, tidepools provide ecological stability via biodiversity enhancement on artificial structures, complicating colonization by invasive species (see McCann, 2000; Glasby et al., 2007). Table 4 Three-way RM-ANOVA results for species richness and Shannon diversity on control treatment data. Mauchly’s test: p > 0.05. Ti: time, T1: spring 2014, T2: summer 2014, T3: autumn 2014 and T4: winter 2015. Le: level. Su: substrate. N: natural. A: artificial. Bold font: p < 0.05 and interaction between different factors. Species richness Shannon diversity index Source Df F P Pairwise comparisons F P Pairwise comparisons CONTROL TREATMENT WITHIN-SUBJECT VARIATION Time 3 11.45 < 0.001 (T1 = T2 = T3) < T4 5.28 < 0.05 T1 < (T2 = T3 = T4) Ti × Le 3 1.05 0.37 0.58 0.62 Ti × Su 3 5.37 < 0.005 Ti × Su: T1. T2. T3: N = A T4: N > A 0.85 0.46 Ti × Le × Su 3 0.83 0.47 1.41 0.23 Residuals 168 BETWEEN-SUBJECT VARIATION Level 1 2.04 0.15 3.56 0.064 N>A Substrate 1 5.30 < 0.05 N>A 5.13 < 0.05 Le × Su 1 3.10 0.08 6.76 < 0.05 Le × Su: Residuals 56 (Up-A = Up-N = Down-A) < Down-N Table 5 Multivariate RM-PERMANOVA results on control treatment data. *PERMDISP dispersion results for level*substrate interaction. No differences were found among seasons (p = 0.877) and levels (p = 0.114). Ti: time. Le: level. Su: substrate. N: natural. A: artificial. Bold font: p > 0.05 and interaction between different factors. Source Df MS Pseudo-F P (perm) Pairwise comparisons CONTROL TREATMENT Time 3 5379 2.2343 < 0.05 (T1 = T2 = T3) ≠T4 Level 1 75,976 31.553 < 0.001 Substrate 1 25,688 10.668 < 0.001 Le × Su: N: Up ≠Down Up = A ≠N A: Up ≠Down Down = A ≠N *N-Down < A-Up < (N- Up = A-Down) Ti × Le 3 2535 1.0528 0.37 Ti × Su 3 2737 1.1369 0.28 Le × Su 1 9670 4.016 < 0.001 Fig. 6. nMDS showing PCO centroids for level and treatment factors combination according to each studied time. Results were plotted separately for natural and artificial surfaces. E. Ostalé-Valriberas et al. Ecological Engineering 120 (2018) 522–531 529 Therefore, the design of biotypes with higher spatial heterogeneity (pools and crevices), and the subsequent microhabitat diversification would mimic nearby natural rocky shores and hinder the settlement of invasive species. In this sense, it is important that the design of artificial structures favour the settlement of native species in the shortest time possible. Acknowledgements The authors would like to express their gratitude to our colleagues from the Laboratorio de Biología Marina of the University of Sevilla who provided insight and expertise that greatly assisted the research. We thank Gemma Martínez, Íñigo Donazar, Javier Pellón, Francisco Sedano and Altai C. Pavón for their help provided in the sampling process and the two anonymous referees who have greatly improved the original version of the manuscript with constructive critiques. For their support we are grateful to María Ambrona de la Lastra, Rocío Valriberas and Enrique Ostalé, without whom the study would not have been done. We are also particularly grateful for the assistance given by the Estación de Biología Marina del Estrecho de la Universidad de Sevilla, especially by Javier Ibañez and José Manuel Ávila, and the Consejería de Medio Ambiente y Sostenibilidad, Ciudad Autónoma de Ceuta (OBIMASA). References Aguilera, M.A., Broitman, B.R., Thiel, M., 2014. Spatial variability in community composition on a granite breakwater versus natural rocky shores: lack of microhabitats suppresses intertidal biodiversity. Mar. Pollut. Bull. 87, 257–268. Airoldi, L., Abbiati, M., Beck, M.W., Hawkins, S.J., Jonsson, P.R., Martin, D., Moschella, P.S., Sundelöf, A., Thompson, R.C., Åberg, P., 2005. An ecological perspective on the deployment and design of low-crested and other hard coastal defence structures. Coast. Eng. 52, 1073–1087. Airoldi, L., Beck, M.W., 2007. Loss, status and trends for coastal marine habitats of Europe. Oceanogr. Mar. Biol. Annu. Rev. 45, 345–405. Anderson, M.J., Walsh, D.C.I., 2013. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing? Ecol. Monogr. 83, 557–574. Araujo, R., Sousa-Pinto, I., Barbara, I., Quintino, V., 2006. Macroalgal communities of intertidal rock pools in the northwest coast of Portugal. Acta Oecol. 30, 192–202. Asif, M., Muneer, T., 2007. Energy supply, its demand and security issues for developed and emerging economies. Renew Sustain. Energy Rev. 11, 1388–1413. Bennett, B.A., 1987. The rock-pool fish community of Koppie Alleen and an assessment of the importance of Cape rock-pools as nurseries for juvenile fish. S. Afr. J. Zool. 25–32. Bergen, S.D., Bolton, S.M., Fridley, J.L., 2001. Design principles for ecological engineering. Ecol. Eng. 18, 201–210. Browne, M.A., Chapman, M.G., 2011. Ecologically-informed engineering reduces loss of intertidal biodiversity on artificial shorelines. Environ. Sci. Technol. 45, 8204–8207. Browne, M.A., Chapman, M.G., 2014. Mitigating against the loss of species by adding artificial intertidal pools to existing seawalls. Mar. Ecol. Prog. Ser. 497, 119–129. Bulleri, F., 2005. Experimental evaluation of early patterns of colonization of space on rocky shores and seawalls. Mar. Environ. Res.60, 355–374. Bulleri, F., Chapman, M.G., 2004. Intertidal assemblages on artificial and natural habitats in marinas on the north-west coast of Italy. Mar. Biol. 145, 381–391. Bulleri, F., Chapman, M.G., 2010. The introduction of coastal infrastructures as a driver of change in marine environments. J. Appl. Ecol. 47, 26–35. Burgos-Rubio, V., De la Rosa, J., Altamirano, M., Espinosa, F., 2015. The role of patellid limpets as omnivorous grazers: a new insight into intertidal ecology. Mar. Biol. 162 (10), 2093–2106. Castelló, J., Carballo, J.L., 2001. Isopod fauna, excluding Epicaridea, from the Strait of Gibraltar and nearby areas (Southern Iberian Peninsula). Sci. Mar. 65, 221–241. Chapman, M.G., Blockley, D., 2009. Engineering novel habitats on urban infrastructure to increase intertidal biodiversity. Oecologia 161, 625–635. Chapman, M.G., Bulleri, F., 2003. Intertidal seawalls new features of landscape in intertidal environments. Landsc. Urban. Plan. 62, 159–172. Chapman, M.G., Underwood, A.J., 2011. Evaluation of ecological engineering of “armoured”shorelines to improve their value as habitat. J. Exp. Mar. Biol. Ecol. 400, 302–313. Clarke, K.R., 1993. Non-parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 18, 117–143. Clarke, K.R., Gorley, R.N., 2006. PRIMER v6: User manual/tutorial. PRIMER-e, Plymouth, UK, pp. 192. Connell, J.H., 1978. Diversity in tropical rain forests and coral reefs. Science 199, 1302–1310. Coombes, M.A., 2011. Biogeomorphology of Coastal Structures: Understanding Interactions Between Hard Substrate and Colonising Organisms as a Tool for Ecological Enhancement. University of Exeter, Exeter, United Kingdom PhD dissertation. Dafforn, K.A., Glasby, T.M., Airoldi, L., Rivero, N.K., Mayer-Pino, M., Johnston, E.L., 2015. Marine urbanization: an ecological framework for designing multifunctional artificial structures. Front. Ecol. Environ. 13, 82–90. Delany, J., Myers, A.A., Mc Grath, D., 1998. Recruitment, immigration and population structure of two coexisting limpet species in mid-shore tidepools, on the west coast of Ireland. J. Exp. Mar. Biol. Ecol. 221, 221–230. DELOS project, Environmental Design of Low Crested Coastal Defense Structure. Deliverable 46: Identification of design features to maintain biodiversity of epibiota, EVK3-CT-2000-00041. Dong, Y., Huang, X., Wang, W., Li, Y., Wang, J., 2016. The marine ¨great wall¨ of China: local and broad-scale ecological impacts of coastal infrastructure on intertidal Fig. 7. Percentage of individuals of vagile species and Siphonaria sp. eggs masses observed over artificial substrate in each treatment one year after pool blazing. E. Ostalé-Valriberas et al. Ecological Engineering 120 (2018) 522–531 530
67 showed lower biodiversity and more heterogeneous assemblages, due to harsh conditions driven by desiccation (see Raffaelli and Hawkins, 1996). Finally, high levels on natural substrates and low levels on artificial ones showed intermediate values of diversity and heterogeneous assemblages, in accordance with the intermediate perturbation hypothesis (Connell, 1978). Focusing on the description of biological assemblages in this type of microhabitats within the natural environment, it is proven that tidal height is an important structuring force for rocky intertidal communities (Underwood et al., 1984). Furthermore, Martins (Martins et al., 2007) showed consistent differences in the assemblages in natural rock pools at different heights. In this sense, the results of the present study also showed strong differences between low and high midlittoral levels, the lower level having the highest values of diversity and species richness. 4.1. Conclusions and management implications The creation of small tidepools on breakwaters during or after structure construction is an affordable method that should be taken into account due to the substantial ecological benefits it provides. In fact, the present study shows a significant increase of species richness and Shannon diversity in one year even in a coastal defence structure that has reached a steady state climax community. Besides, it has been demonstrated that the creation of this microhabitat has allowed several species of vagile fauna to colonize the intertidal habitat. According to Underwood (Underwood and Skilleter, 1996) and Martins (Martins et al., 2007), better results can be expected with the creation of greater and deeper tidepools. For the creation of pools, a hydraulic jackhammer (present study) or diamond-tipped bits of variable diameters can be used (Underwood and Skilleter, 1996; Evans et al., 2016). Previous experiences have revealed that the artificial structures preserve their integrity, indicating that this is a long-term option which is resistant to storms and wave action (see Firth et al., 2016). From a conservationist point of view, the creation of these intertidal water-retaining microhabitats in artificial structures has two major benefits. First, tidepools produce refuge for vagile species and their egg masses. These species had only been observed in natural rocky shores; hence artificial tidepools reduce habitat fragmentation and enhance population connectivity. Second, tidepools provide ecological stability via biodiversity enhancement on artificial structures, complicating colonization by invasive species (see McCann, 2000; Glasby et al., 2007). Table 4 Three-way RM-ANOVA results for species richness and Shannon diversity on control treatment data. Mauchly’s test: p > 0.05. Ti: time, T1: spring 2014, T2: summer 2014, T3: autumn 2014 and T4: winter 2015. Le: level. Su: substrate. N: natural. A: artificial. Bold font: p < 0.05 and interaction between different factors. Species richness Shannon diversity index Source Df F P Pairwise comparisons F P Pairwise comparisons CONTROL TREATMENT WITHIN-SUBJECT VARIATION Time 3 11.45 < 0.001 (T1 = T2 = T3) < T4 5.28 < 0.05 T1 < (T2 = T3 = T4) Ti × Le 3 1.05 0.37 0.58 0.62 Ti × Su 3 5.37 < 0.005 Ti × Su: T1. T2. T3: N = A T4: N > A 0.85 0.46 Ti × Le × Su 3 0.83 0.47 1.41 0.23 Residuals 168 BETWEEN-SUBJECT VARIATION Level 1 2.04 0.15 3.56 0.064 N>A Substrate 1 5.30 < 0.05 N>A 5.13 < 0.05 Le × Su 1 3.10 0.08 6.76 < 0.05 Le × Su: Residuals 56 (Up-A = Up-N = Down-A) < Down-N Table 5 Multivariate RM-PERMANOVA results on control treatment data. *PERMDISP dispersion results for level*substrate interaction. No differences were found among seasons (p = 0.877) and levels (p = 0.114). Ti: time. Le: level. Su: substrate. N: natural. A: artificial. Bold font: p > 0.05 and interaction between different factors. Source Df MS Pseudo-F P (perm) Pairwise comparisons CONTROL TREATMENT Time 3 5379 2.2343 < 0.05 (T1 = T2 = T3) ≠T4 Level 1 75,976 31.553 < 0.001 Substrate 1 25,688 10.668 < 0.001 Le × Su: N: Up ≠Down Up = A ≠N A: Up ≠Down Down = A ≠N *N-Down < A-Up < (N- Up = A-Down) Ti × Le 3 2535 1.0528 0.37 Ti × Su 3 2737 1.1369 0.28 Le × Su 1 9670 4.016 < 0.001 Fig. 6. nMDS showing PCO centroids for level and treatment factors combination according to each studied time. Results were plotted separately for natural and artificial surfaces. E. Ostalé-Valriberas et al. Ecological Engineering 120 (2018) 522–531 529 Therefore, the design of biotypes with higher spatial heterogeneity (pools and crevices), and the subsequent microhabitat diversification would mimic nearby natural rocky shores and hinder the settlement of invasive species. In this sense, it is important that the design of artificial structures favour the settlement of native species in the shortest time possible. Acknowledgements The authors would like to express their gratitude to our colleagues from the Laboratorio de Biología Marina of the University of Sevilla who provided insight and expertise that greatly assisted the research. We thank Gemma Martínez, Íñigo Donazar, Javier Pellón, Francisco Sedano and Altai C. Pavón for their help provided in the sampling process and the two anonymous referees who have greatly improved the original version of the manuscript with constructive critiques. For their support we are grateful to María Ambrona de la Lastra, Rocío Valriberas and Enrique Ostalé, without whom the study would not have been done. We are also particularly grateful for the assistance given by the Estación de Biología Marina del Estrecho de la Universidad de Sevilla, especially by Javier Ibañez and José Manuel Ávila, and the Consejería de Medio Ambiente y Sostenibilidad, Ciudad Autónoma de Ceuta (OBIMASA). References Aguilera, M.A., Broitman, B.R., Thiel, M., 2014. Spatial variability in community composition on a granite breakwater versus natural rocky shores: lack of microhabitats suppresses intertidal biodiversity. Mar. Pollut. Bull. 87, 257–268. Airoldi, L., Abbiati, M., Beck, M.W., Hawkins, S.J., Jonsson, P.R., Martin, D., Moschella, P.S., Sundelöf, A., Thompson, R.C., Åberg, P., 2005. An ecological perspective on the deployment and design of low-crested and other hard coastal defence structures. Coast. Eng. 52, 1073–1087. Airoldi, L., Beck, M.W., 2007. Loss, status and trends for coastal marine habitats of Europe. Oceanogr. Mar. Biol. Annu. Rev. 45, 345–405. Anderson, M.J., Walsh, D.C.I., 2013. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing? Ecol. Monogr. 83, 557–574. Araujo, R., Sousa-Pinto, I., Barbara, I., Quintino, V., 2006. Macroalgal communities of intertidal rock pools in the northwest coast of Portugal. Acta Oecol. 30, 192–202. Asif, M., Muneer, T., 2007. 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69
Ecological Engineering 200 (2024) 107187 Available online 28 January 2024 0925-8574/© 2024 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC license (http://creativecommons.org/licenses/bync/4.0/). Ecological succession within microhabitats (tidepools) created in riprap structures hosting climax communities: An economical strategy for mitigating the negative effects of coastal defence structure on marine biodiversity E. Ostal´ e-Valriberas a , b , * , A. Martín-Zorrilla a , J. Sempere-Valverde a , J.C. García-G´ omez a , F. Espinosa a a Laboratorio de Biología Marina de la Universidad de Sevilla (LBMUS)/´ Area de Investigaci´ on I+D+i del Acuario de Sevilla/Estaci´ on de Biología Marina del Estrecho (Ceuta), Universidad de Sevilla, Seville, Spain b Instituto de Estudios Ceutíes, Paseo del Revellín 30, 51001 Ceuta, Spain. ARTICLE INFO Keywords: Coastal engineering Rockpools Functional diversity Population fragmentation Invasive species Artificial structure ABSTRACT The substitution of natural habitats with artificial structures, such as coastal defence structures, has significantly detrimental effects on the marine biological community. In this context, the application of ecological engineering to marine ecosystems presents an opportunity to mitigate these environmental impacts and enhance ecosystem services. There are proposals aimed at mimicking structures found in the natural environment to increase topographic complexity in artificial substrates, thereby promoting biodiversity and hindering the establishment of invasive species. The present study focuses on assessing change in the biological community of intertidal pools constructed on existing coastal defence structures and their influence on a halo (5 cm) of humidity created around the pools. Using an inexpensive method, the tidepools were created at the beginning of 2014 using a pneumatic hammer (DeWalt brand D25902K), imitating the tidepools of the adjacent natural substrate. The coastal defence structures (riprap) which were selected for the study host climax communities since they were built >8 years ago. After 7.5 years of the creation of this microhabitat, the value of species richness in the tidepool was 64.2% higher than in the control, Shannon diversity 41.54% and functional diversity 6.27%. The study of the effect on a halo (5 cm) of humidity produced around the pool shows that Shannon diversity is higher than in the control treatment, demonstrating that the microhabitat created mitigates the harsh environmental (high temperature and desiccation) conditions of the intertidal zone beyond the interior of the tidepool. The results showed that the species richness in the tidepools was bigger in the high intertidal than the low, therefore it is more beneficial to create this microhabitat in high intertidal zone. The created microhabitats serve as shelter and breeding sites for animal species that were not previously observed in the studied artificial structure, as detected for species such as Pisania striata, Ocenebra edwarasii, Stramonita haemastoma, Meralarhaphe neritoides, Siphonaria pectinata, Paracentrotus lividus and Spirorbis sp., thus contribute to reducing the fragmentation of their populations. In terms of “ecological succession”, the current study demonstrated that typical species of a mature benthic biological community had colonised the created microhabitat 7.5 years later. These species included the Anthozoa Anemonia sulcata, Actinia equina and Exaiptasia diaphana or the endangered Mollusc Dendropoma lebeche. 1. Introduction Coastal cities are rapidly expanding in response to a growing demand for space, the protection of coastal assets and populations, aquatic tourism, and maritime traffic (Espinosa and Bazairi, 2023). The replacement of natural habitats with artificial structures, such as coastal * Corresponding author at: Laboratorio de Biología Marina de la Universidad de Sevilla (LBMUS)/´ Area de Investigaci´ on I+D+i del Acuario de Sevilla/Estaci´ on de Biología Marina del Estrecho (Ceuta), Universidad de Sevilla, Seville, Spain. E-mail address: [email protected] (E. Ostal´ e-Valriberas). Contents lists available at ScienceDirect Ecological Engineering journal homepage: www.elsevier.com/locate/ecoleng https://doi.org/10.1016/j.ecoleng.2024.107187 Received 8 August 2023; Received in revised form 8 January 2024; Accepted 14 January 2024
71 Ecological Engineering 200 (2024) 107187 Available online 28 January 2024 0925-8574/© 2024 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC license (http://creativecommons.org/licenses/bync/4.0/). Ecological succession within microhabitats (tidepools) created in riprap structures hosting climax communities: An economical strategy for mitigating the negative effects of coastal defence structure on marine biodiversity E. Ostal´ e-Valriberas a , b , * , A. Martín-Zorrilla a , J. Sempere-Valverde a , J.C. García-G´ omez a , F. Espinosa a a Laboratorio de Biología Marina de la Universidad de Sevilla (LBMUS)/´ Area de Investigaci´ on I+D+i del Acuario de Sevilla/Estaci´ on de Biología Marina del Estrecho (Ceuta), Universidad de Sevilla, Seville, Spain b Instituto de Estudios Ceutíes, Paseo del Revellín 30, 51001 Ceuta, Spain. ARTICLE INFO Keywords: Coastal engineering Rockpools Functional diversity Population fragmentation Invasive species Artificial structure ABSTRACT The substitution of natural habitats with artificial structures, such as coastal defence structures, has significantly detrimental effects on the marine biological community. In this context, the application of ecological engineering to marine ecosystems presents an opportunity to mitigate these environmental impacts and enhance ecosystem services. There are proposals aimed at mimicking structures found in the natural environment to increase topographic complexity in artificial substrates, thereby promoting biodiversity and hindering the establishment of invasive species. The present study focuses on assessing change in the biological community of intertidal pools constructed on existing coastal defence structures and their influence on a halo (5 cm) of humidity created around the pools. Using an inexpensive method, the tidepools were created at the beginning of 2014 using a pneumatic hammer (DeWalt brand D25902K), imitating the tidepools of the adjacent natural substrate. The coastal defence structures (riprap) which were selected for the study host climax communities since they were built >8 years ago. After 7.5 years of the creation of this microhabitat, the value of species richness in the tidepool was 64.2% higher than in the control, Shannon diversity 41.54% and functional diversity 6.27%. The study of the effect on a halo (5 cm) of humidity produced around the pool shows that Shannon diversity is higher than in the control treatment, demonstrating that the microhabitat created mitigates the harsh environmental (high temperature and desiccation) conditions of the intertidal zone beyond the interior of the tidepool. The results showed that the species richness in the tidepools was bigger in the high intertidal than the low, therefore it is more beneficial to create this microhabitat in high intertidal zone. The created microhabitats serve as shelter and breeding sites for animal species that were not previously observed in the studied artificial structure, as detected for species such as Pisania striata, Ocenebra edwarasii, Stramonita haemastoma, Meralarhaphe neritoides, Siphonaria pectinata, Paracentrotus lividus and Spirorbis sp., thus contribute to reducing the fragmentation of their populations. In terms of “ecological succession”, the current study demonstrated that typical species of a mature benthic biological community had colonised the created microhabitat 7.5 years later. These species included the Anthozoa Anemonia sulcata, Actinia equina and Exaiptasia diaphana or the endangered Mollusc Dendropoma lebeche. 1. Introduction Coastal cities are rapidly expanding in response to a growing demand for space, the protection of coastal assets and populations, aquatic tourism, and maritime traffic (Espinosa and Bazairi, 2023). The replacement of natural habitats with artificial structures, such as coastal * Corresponding author at: Laboratorio de Biología Marina de la Universidad de Sevilla (LBMUS)/´ Area de Investigaci´ on I+D+i del Acuario de Sevilla/Estaci´ on de Biología Marina del Estrecho (Ceuta), Universidad de Sevilla, Seville, Spain. E-mail address: [email protected] (E. Ostal´ e-Valriberas). Contents lists available at ScienceDirect Ecological Engineering journal homepage: www.elsevier.com/locate/ecoleng https://doi.org/10.1016/j.ecoleng.2024.107187 Received 8 August 2023; Received in revised form 8 January 2024; Accepted 14 January 2024
72 Ecological Engineering 200 (2024) 107187 2 defence structures, has exerted a substantial adverse impact on the environment (Firth et al., 2020; Sempere-Valverde et al., 2023). This leads to the destruction and fragmentation of native species’ habitats, isolating their populations and adversely affecting marine biodiversity. This, in turn, facilitates the proliferation of invasive species, carrying significant consequences at both national and international scales (Airoldi et al., 2005; Waltham and Dafforn, 2018). In this context, the application of ecological engineering in marine biology represents an opportunity to ameliorate these environmental impacts and enhance ecosystem services (Mitsch, 2012; Bishop et al., 2017). The concept of “Ecological Engineering,” recently applied in the field of marine biology, integrates ecological, economic, and social considerations into the planning of artificial ecosystems. Essentially, it entails integrating ecological objectives and principles into the design of human-made structures in marine environments (Bergen et al., 2001; Schulze et al., 1996; Firth et al., 2014). The biota present in artificial systems varies from that found in adjacent natural systems (Glasby, 1999; Firth et al., 2013a; Farrugia Drakard et al., 2021, Thompson et al., 2023.). In natural substrates, the heterogeneity of the substrate is an essential factor for maintaining biodiversity, whereas artificial substrates tend to be smoother and more homogeneous, resulting in lower biodiversity (Evans et al., 2019). There are proposals aimed at imitating structures found in the natural environment to increase topographic complexity in artificial substrates and, consequently, enhancing biodiversity which has been termed as ‘Greening of Grey Infrastructures (GGI)’ (Firth et al., 2020). It could be done in several ways such as creation of textured surfaces (Strain et al., 2020; Evans et al., 2021), holes and crevices (Chapman and Underwood, 2011; Hall et al., 2019), and rock pools (Firth et al., 2014; Morris et al., 2019; Ostal´ e-Valriberas et al., 2018). Fig. 1. The areas under study in Ceuta, located in the Strait of Gibraltar, include the following locations: A) Dock of Levante, B) Chorrillo Beach, and C) Fuente Caballo Beach. From Ostal´ e-Valriberas et al. (2018). Fig. 2. Example of species coverage appraisal by random point count methodology. A: Tidepool filled with water to delimit pool edge, B: Tidepool. C: Halo with a 5 cm perimeter, D: Control (10 cm from the halo area). From Ostal´ e-Valriberas et al. (2018). E. Ostal´ e-Valriberas et al.
73 Ecological Engineering 200 (2024) 107187 2 defence structures, has exerted a substantial adverse impact on the environment (Firth et al., 2020; Sempere-Valverde et al., 2023). This leads to the destruction and fragmentation of native species’ habitats, isolating their populations and adversely affecting marine biodiversity. This, in turn, facilitates the proliferation of invasive species, carrying significant consequences at both national and international scales (Airoldi et al., 2005; Waltham and Dafforn, 2018). In this context, the application of ecological engineering in marine biology represents an opportunity to ameliorate these environmental impacts and enhance ecosystem services (Mitsch, 2012; Bishop et al., 2017). The concept of “Ecological Engineering,” recently applied in the field of marine biology, integrates ecological, economic, and social considerations into the planning of artificial ecosystems. Essentially, it entails integrating ecological objectives and principles into the design of human-made structures in marine environments (Bergen et al., 2001; Schulze et al., 1996; Firth et al., 2014). The biota present in artificial systems varies from that found in adjacent natural systems (Glasby, 1999; Firth et al., 2013a; Farrugia Drakard et al., 2021, Thompson et al., 2023.). In natural substrates, the heterogeneity of the substrate is an essential factor for maintaining biodiversity, whereas artificial substrates tend to be smoother and more homogeneous, resulting in lower biodiversity (Evans et al., 2019). There are proposals aimed at imitating structures found in the natural environment to increase topographic complexity in artificial substrates and, consequently, enhancing biodiversity which has been termed as ‘Greening of Grey Infrastructures (GGI)’ (Firth et al., 2020). It could be done in several ways such as creation of textured surfaces (Strain et al., 2020; Evans et al., 2021), holes and crevices (Chapman and Underwood, 2011; Hall et al., 2019), and rock pools (Firth et al., 2014; Morris et al., 2019; Ostal´ e-Valriberas et al., 2018). Fig. 1. The areas under study in Ceuta, located in the Strait of Gibraltar, include the following locations: A) Dock of Levante, B) Chorrillo Beach, and C) Fuente Caballo Beach. From Ostal´ e-Valriberas et al. (2018). Fig. 2. Example of species coverage appraisal by random point count methodology. A: Tidepool filled with water to delimit pool edge, B: Tidepool. C: Halo with a 5 cm perimeter, D: Control (10 cm from the halo area). From Ostal´ e-Valriberas et al. (2018). E. Ostal´ e-Valriberas et al. Ecological Engineering 200 (2024) 107187 3 Tidepools are micro-habitats that host great biodiversity, as they protect against the harsh environmental conditions of the intertidal zone, such as desiccation and high temperatures when the tide goes down (Metaxas and Scheibling, 1993; Araújo et al., 2006; Firth et al., 2013b). Previous studies have demonstrated that the establishment of these microhabitats within coastal defence structures enhances the biodiversity of these man-made constructions, including the facilitation of new species’ establishment of the natural adjacent zone (Sempere- Valverde et al., 2023). As a consequence, the inclusion of tidepools enhances ecological stability by increasing biodiversity on artificial structures, complicating the colonization by potential invasive species not previously established in the environment (McCann, 2000; Glasby et al., 2007; Dafforn et al., 2015). The present study focuses on the work of Ostal´ e-Valriberas et al. (2018), whose objectives were to investigate the ecological benefits of constructing intertidal pools in coastal defence structures and their effect on a halo of humidity produced around the pool. In conclusion, after one year of monitoring the created microhabitat, the biological community was more complex in terms of biodiversity, serving as a refuge for species not present in the original artificial substrate in its first year of creation (Ostal´ e-Valriberas et al., 2018). However, most of the studies have not undergone long-term changes and critical assessment, hindering the adoption of GGI as a mainstream solution (Firth et al., 2020). Consequently, this study places particular emphasis on the long-term monitoring of the biological community within the established microhabitat. Changes have been studied in two different intertidal heights to elucidate whether the new microhabitats contributed differently to the overall diversity depending on their tidal range. In this context, previous findings by Bulleri and Chapman (2010) indicated a greater contribution in the high level in seawalls from Australia, although such data is limited in other regions or for various types of artificial structures. Furthermore, the majority of studies have predominantly used taxonomic diversity as a proxy for assessing the impact of artificial substrata on marine biodiversity, while functional diversity (including different biological traits) has received notably less attention (Sedano et al., 2020). To this end, the objectives of this study are to answer the following questions: i) does the creation of tidal pools increase local biodiversity in artificial coastal protection structures in which the biological community that had already reached its climax state was established?, ii) is the increase in diversity caused by artificial pools greater in the upper level than in the lower level of the intertidal zone?, iii) how has been the succession of the biological community in the new microhabitat created? and iv) what species have been directly benefited from the created microhabitat? 2. Materials and methods 2.1. Study location The study was conducted in Ceuta, a city on the southern coast of the Strait of Gibraltar (North Africa, Spain). This area is considered to be of high ecological value, since it is on the border of three biogeographical provinces: Mediterranean, Lusitanian and Mauritanian, as well as the Mediterranean Sea and the Atlantic Ocean causing its marine flora and fauna to overlap, therefore, it is a transition area with a high biodiversity (Coll et al., 2010). Its location makes it an area of special risk of disturbance since it is one of the most maritime traffic zones worldwide where many important ports are located (Algeciras, Gibraltar and Tangier Med). It makes this area a habitat with a high risk of disturbances, impacts or possible environmental disasters (Ostal´ e-Valriberas et al., 2022). The present study extends the ongoing monitoring of the artificial rock pools, previously created and studied during the first year by Ostal´ e-Valriberas et al. (2018). As it was originally described in such study, it was conducted on three artificial substrates made with dolomite limestone rock: the ripraps of the Chorrillo and Fuente Caballos beaches, and the Levante breakwater that belongs to the port of Ceuta (Fig. 2). For the study, coastal defence structures were selected that had been built for more than eight years, so it could be stated that the established (control) biological community had already reached the climax phase of ecological succession in intertidal rocky habitats (Coombes, 2011; Dong, 2016). (See Fig. 1.) 2.2. Experimental design and sampling The experimental design included the same three factors as in Ostal´ e- Valriberas et al. (2018): time, height at the intertidal fringe, and treatment. However, the “Time” factor was considerably expanded from one to seven years of monitoring, and now consisted of eight levels covering different seasons and years: T1 (summer 2014), T2 (winter 2015), T3 Table 1 Biological traits with their categories for the taxa studied. Adapted from Martini et al. (2021). Biological traits Traits categories Growth Form Algae Articulated-arborescent Filamentous Foliose No articulated-arborescent Flattened Globose Growth Form Animal Tubular shell Turriculate shell Conical shell Shield shell Tentacle Sharp thorns Bivalve Longevity <2 years (animals); annual (complete their life cycle in one season) (macroalgae). 2–5 years (animals); perennial (macroalgae). 5–15 years (animals); perennial long lived (macroalgae). >15 years (animals) Introductory potential Yes No Reproductive strategy Asexual - vegetative (fragmentation) Asexual - vegetative (spores/propagules) Sexual – gonochoric Sexual – hermaphrodite Environmental position Epilithic Epiphytic Epizoic Vagil Feeding strategy Autotroph Suspension Feeder / Filter Predator Herbivore/Grazer Detritivore Sociality Solitary Gregarious Colonial Turf Relative adult mobility None Low Medium High Development mode Planktotrophic Lecithotrophic Direct Maximum size 0–1 cm 1–5 cm 5–10 cm 10–25 cm >25 cm E. Ostal´ e-Valriberas et al.
80 Ecological Engineering 200 (2024) 107187 10 for example, Evans et al., 2015; Ostal´ e-Valriberas et al., 2018; Farrugia- Drakard et al., 2023), typically involving short-term temporal monitoring (maximum 2 years) showed substantial improvements in biological parameters within tidepools, suggesting positive ecological trends within these artificial habitats. The relevance of the current study lies in showing the persistence of these patterns over a long-term period (7.5 years) for artificial tidepools built within old coastal defence structures. During the initial three years (T5), the biological community was largely established and exhibited significantly higher 7.5 years after its establishment. Therefore, these types of solutions have been proven to be useful in the context of greening of grey infrastructure (GGI). Previous studies have shown a decrease in diversity in pools with increasing intertidal height, because the high intertidal zone is subject to a higher environmental stress (Firth et al., 2013b). Same results have been observed in the control treatment of the present study. However, in contrast, the number of species within tidepools has been similar between the different heights. Therefore, artificial tidepools increased higher the biological diversity within upper when compared to the lower intertidal (Table 3). Similarly, Bulleri and Chapman (2010) observed that the number of ‘new’ species provided by artificial tidepools (compared to those existing in the surrounding area) was greater in the high intertidal compared to the low intertidal. The ecological succession that takes place within the tidepools adheres to the model of “succession by inhibition” (Rodríguez-Martínez, 2016). During the initial stage, pioneer species, in this case, opportunistic or r-strategist species such as biofilm, Ulva sp., Ralfsia verrucosa, colonize the area, favoring the possibility of settlement of herbivorous rstrategist species such as S. pectinata, P. lividus or P. caerulea inhibiting their growth as a disruptive agent (Espinosa, 2006) (Table 4-T1 and Fig. 7). In this succession, the second stage is driven by herbivore pressure on species dominating the first stage (Laure et al., 2009). In the intermediate stage, red algae with complex thalli, low growth and low net productivity, such as E. elongata, J. rubens or Gelidium sp. experience an increase in biomass (Littler and Littler, 1980). In the model, the species controlling the initial phase remain present in the community, although with reduced coverage (Rodríguez-Martínez, 2016) (Fig. 7-A). In the present study, species such as D. lebeche, A. equina or A. sulcata with a more complex life cycle settle in the mature phase of the succession (Fig. 7-B). In particular, the created microhabitat contributed to the settlement of some vagile species such as the echinoderm P. lividus, the molluscs Fissurella sp., P. striata, S. haemastoma, O. edwardsii and Phorcus turbinatus. The persistence over time of these species demonstrates that the creation of tidepools in artificial structures could reduce habitat fragmentation for these species and improve the connectivity of their populations, considering the disruption impact caused by these structures on connectivity (Bishop et al., 2017). Furthermore, the increase in biodiversity and functional diversity over time in these types of artificial structures following the creation of these experimental microhabitats enhanced the number of functional features or niches and would therefore provide ecological resilience and, according to existing literature, make it more difficult for invasive species to settle and thus disperse, reducing invasive processes (see McCann, 2000; Glasby et al., 2007; Kennedy et al., 2002). For example, in contrast to the control treatment, herbivorous species such as P. lividus and P. striata or carnivorous species such as S. haemastoma have settled exclusively in the tidepools. 4.1. Conclusions and management implications As demonstrated in the present study, the topographic heterogeneity provided by artificially created tidepools within coastal defence structures mimic the microhabitats found in the adjacent natural substrates, providing refuges for various species and enhancing species richness, Shannon diversity and functional traits or biological niches over time. This feature promotes ecological stability, thus hindering the establishment and spread of invasive species (Essink and Dekker, 2002; Paavola et al., 2005; Glasby et al., 2007). Moreover, adding shelters for native predators within such artificial structures is crucial to hinder the colonization by invasive species, considering that artificial substrates are well-known transmission vectors (Morris et al., 2019). In addition, these created microhabitats serve as refuges and breeding sites for animal species that are not usually observed in artificial structures, such as P. striata, O. edwardsii, S. haemastoma, Melarhaphe neritoides and P. turbinatus (Ostal´ e-Valriberas et al., 2018, 2022). It could contribute to reducing the fragmentation of the populations of these species. Within a coastal defence scheme, tidepools can be created at little expense, obtaining ecological benefits even in those with a climax biological community. This practice aids in mitigating the negative effects caused by low levels of biodiversity due to homogeneity caused by artificial substrates (see Naylor et al., 2023). According to previous studies, these results can be improved by increasing the size of the pool (Martins et al., 2007). Supplementary data to this article can be found online at https://doi. org/10.1016/j.ecoleng.2024.107187. Declaration of generative AI and AI-assisted technologies in the writing process During the preparation of this work the author(s) used ChatGPT in order to review the English grammar. After using this tool/service, the author(s) reviewed and edited the content as needed and take(s) full responsibility for the content of the publication. CRediT authorship contribution statement E. Ostal´ e-Valriberas: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Software, Validation, Visualization, Writing – original draft. A. Martín-Zorrilla: Data curation, Formal analysis, Investigation, Software, Validation, Visualization, Writing – original draft. J. Sempere-Valverde: Data curation, Formal analysis, Methodology, Validation, Writing – review & editing, Visualization. J.C. García-G´ omez: Funding acquisition, Supervision, Validation, Writing – review & editing. F. Espinosa: Conceptualization, Data curation, Methodology, Validation, Writing – review & editing, Formal analysis, Supervision. Declaration of competing interest The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Data availability No data was used for the research described in the article. References Airoldi, L., Abbiati, M., Beck, M.W., Hawkins, S.J., Jonsson, P.R., Martin, D., Åberg, P., 2005. An ecological perspective on the deployment and design of low-crested and other hard coastal defence structures. Coast. Eng. 52 (10−11), 1073–1087. Araújo, R., Sousa-Pinto, I., B´ arbara, I., Quintino, V., 2006. Macroalgal communities of intertidal rock pools in the northwest coast of Portugal. Acta Oecol. 30 (2), 192–202. Bergen, S.D., Bolton, S.M., Fridley, J.L., 2001. Design principles for ecological engineering. Ecol. Eng. 18, 201–210. 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VI. PUBLICACIÓN 3. MICRORRESERVAS MARINAS ARTIFICIALES COMO NUEVA HERRAMIENTA DE GESTIÓN ECOSISTÉMICA PARA LA CONSERVACIÓN MARINA: EL CASO DE P. FERRUGINEA (GASTROPODA, PATELLIDAE), UNO DE LOS INVERTEBRADOS MARINOS MÁS AMENAZADOS DEL MEDITERRÁNEO.
85 VI. PUBLICACIÓN 3. MICRORRESERVAS MARINAS ARTIFICIALES COMO NUEVA HERRAMIENTA DE GESTIÓN ECOSISTÉMICA PARA LA CONSERVACIÓN MARINA: EL CASO DE P. FERRUGINEA (GASTROPODA, PATELLIDAE), UNO DE LOS INVERTEBRADOS MARINOS MÁS AMENAZADOS DEL MEDITERRÁNEO.
Marine Policy 136 (2022) 104917 Available online 30 December 2021 0308-597X/© 2021 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Artificial marine micro-reserves as a new ecosystem-based management tool for marine conservation: The case of Patella ferruginea (Gastropoda, Patellidae), one of the most endangered marine invertebrates of the Mediterranean E. Ostal´ e-Valriberas a , * , J. Sempere-Valverde a , A. Pav´ on-Paneque a , S. Coppa b , F. Espinosa a , J. C. García-G´ omez a a Laboratorio de Biología Marina de la Universidad de Sevilla (LBMUS)/´ Area de Investigaci´ on I+D+i del Acuario de Sevilla/Estaci´ on de Biología Marina del Estrecho (Ceuta), Seville, Spain b Consiglio Nazionale delle Ricerche, Istituto per lo studio degli impatti Antropici e Sostenibilit` a in ambiente marino (CNR-IAS), Oristano, Italy ARTICLE INFO Keywords: Artificial Marine Micro-Reserves Conservation Extinction risk Ecosystem-based Management Patella ferruginea ABSTRACT During the Anthropocene, species are becoming extinct at unprecedented rates, a trend that will be difficult to reverse, even if we ignore the possibility of a considerable extinction debt. Among the different factors that affect the natural environment, fragmentation of ecosystems by urbanization processes can cause a reduction in species population sizes, thus enhancing their risk of extinction. Nevertheless, some species can maintain stable populations in these urbanized ecosystems. This is the case of the intertidal mollusc Patella ferruginea (Gmelin, 1791), a broadcast spawner, and a sequential protandrous hermaphrodite limpet, whose populations have been historically decimated due to human harvesting. In this study, we analyse the benefits of a new marine conservation tool called ¨Artificial Marine Micro-Reserves¨(AMMR) in P. ferruginea, one of the most endangered marine invertebrates of the Mediterranean Sea. The results showed that accessibility is the main factor concerning the conservation status of this species, with no-entry areas where populations achieve balanced sex-ratios and high reproductive outputs. The present study was conducted in Ceuta (North Africa, Gibraltar Area), and among its varying results, it shows that in the same body of water inside the port, the proportion of females of P. ferruginea in the area without accessibility (high protection) was 4.68 and 43.54 times higher than in the medium and low accessibility (non-protected areas), respectively. Therefore, the effective protection of these artificial areas has a positive effect on population size structures, as the female’s percentage in the population is crucial for fostering the creation of genetic bridges for the recolonization of natural habitats. Furthermore, a potential ‘umbrella effect’ can be derived from the implementation of the proposed AMMR in other protected species, bioindicators, or commercially exploited species detected in artificial structures. In this sense, the creation of artificial marine microreserve networks (AMMRNs) in coastal defense structures is in line with the interdisciplinary approach of Ecosystem-Based Management (EMB), given that this methodology balances ecological, social and governmental principles for achieving humane sustainable development. 1. Introduction Urban sprawl is expanding into the marine realm with the construction of artificial structures. In areas of Europe, the United States or North America, Australia, and Asia, more than 50% of the shoreline has been altered by hard engineering (man-made coastal defenses) such as breakwaters, ripraps, seawalls, pontoons, groins, etc. to protect against erosion and wave action and for recreational purposes [16,43]. The human impact associated with these structures has been reported to affect biological processes on all spatial and temporal scales [3]. These impacts have negative effects on marine ecosystems in general on local (1–10 km) and regional scales (over hundreds of kilometers) [10,22,44]. Among them, fragmentation of natural habitats by urbanization processes can cause a reduction in species population size and connectivity, * Corresponding author. E-mail address: [email protected] (E. Ostal´ e-Valriberas). Contents lists available at ScienceDirect Marine Policy journal homepage: www.elsevier.com/locate/marpol https://doi.org/10.1016/j.marpol.2021.104917 Received 17 September 2021; Received in revised form 22 November 2021; Accepted 14 December 2021
87 Marine Policy 136 (2022) 104917 Available online 30 December 2021 0308-597X/© 2021 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Artificial marine micro-reserves as a new ecosystem-based management tool for marine conservation: The case of Patella ferruginea (Gastropoda, Patellidae), one of the most endangered marine invertebrates of the Mediterranean E. Ostal´ e-Valriberas a , * , J. Sempere-Valverde a , A. Pav´ on-Paneque a , S. Coppa b , F. Espinosa a , J. C. García-G´ omez a a Laboratorio de Biología Marina de la Universidad de Sevilla (LBMUS)/´ Area de Investigaci´ on I+D+i del Acuario de Sevilla/Estaci´ on de Biología Marina del Estrecho (Ceuta), Seville, Spain b Consiglio Nazionale delle Ricerche, Istituto per lo studio degli impatti Antropici e Sostenibilit` a in ambiente marino (CNR-IAS), Oristano, Italy ARTICLE INFO Keywords: Artificial Marine Micro-Reserves Conservation Extinction risk Ecosystem-based Management Patella ferruginea ABSTRACT During the Anthropocene, species are becoming extinct at unprecedented rates, a trend that will be difficult to reverse, even if we ignore the possibility of a considerable extinction debt. Among the different factors that affect the natural environment, fragmentation of ecosystems by urbanization processes can cause a reduction in species population sizes, thus enhancing their risk of extinction. Nevertheless, some species can maintain stable populations in these urbanized ecosystems. This is the case of the intertidal mollusc Patella ferruginea (Gmelin, 1791), a broadcast spawner, and a sequential protandrous hermaphrodite limpet, whose populations have been historically decimated due to human harvesting. In this study, we analyse the benefits of a new marine conservation tool called ¨Artificial Marine Micro-Reserves¨(AMMR) in P. ferruginea, one of the most endangered marine invertebrates of the Mediterranean Sea. The results showed that accessibility is the main factor concerning the conservation status of this species, with no-entry areas where populations achieve balanced sex-ratios and high reproductive outputs. The present study was conducted in Ceuta (North Africa, Gibraltar Area), and among its varying results, it shows that in the same body of water inside the port, the proportion of females of P. ferruginea in the area without accessibility (high protection) was 4.68 and 43.54 times higher than in the medium and low accessibility (non-protected areas), respectively. Therefore, the effective protection of these artificial areas has a positive effect on population size structures, as the female’s percentage in the population is crucial for fostering the creation of genetic bridges for the recolonization of natural habitats. Furthermore, a potential ‘umbrella effect’ can be derived from the implementation of the proposed AMMR in other protected species, bioindicators, or commercially exploited species detected in artificial structures. In this sense, the creation of artificial marine microreserve networks (AMMRNs) in coastal defense structures is in line with the interdisciplinary approach of Ecosystem-Based Management (EMB), given that this methodology balances ecological, social and governmental principles for achieving humane sustainable development. 1. Introduction Urban sprawl is expanding into the marine realm with the construction of artificial structures. In areas of Europe, the United States or North America, Australia, and Asia, more than 50% of the shoreline has been altered by hard engineering (man-made coastal defenses) such as breakwaters, ripraps, seawalls, pontoons, groins, etc. to protect against erosion and wave action and for recreational purposes [16,43]. The human impact associated with these structures has been reported to affect biological processes on all spatial and temporal scales [3]. These impacts have negative effects on marine ecosystems in general on local (1–10 km) and regional scales (over hundreds of kilometers) [10,22,44]. Among them, fragmentation of natural habitats by urbanization processes can cause a reduction in species population size and connectivity, * Corresponding author. E-mail address: [email protected] (E. Ostal´ e-Valriberas). Contents lists available at ScienceDirect Marine Policy journal homepage: www.elsevier.com/locate/marpol https://doi.org/10.1016/j.marpol.2021.104917 Received 17 September 2021; Received in revised form 22 November 2021; Accepted 14 December 2021
88 Marine Policy 136 (2022) 104917 2 and thus increase their risk of extinction in the face of certain permanent disturbances [12,1]. In order to handle these impacts, the field of coastal ecological engineering aims to integrate ecology, economy, and society’s need to design artificial marine structures that maintain the greatest biodiversity in relation to the natural environment [7]. Essentially, it represents the incorporation of ecological considerations into the design of artificial marine structures [32]. Such an approach is urgently needed, given that anthropic demands on coastlines are expected to increase in the future [3]. Recent studies have shown that organisms that provide important ecosystem services and even protected species can benefit from artificial structures [33,88]. Some of these protected species have substantial populations inhabiting artificial habitats. This is the case of the endangered limpet Patella ferruginea (Gmelin, 1791), whose densest populations exist in the breakwaters of the Strait of Gibraltar and Alboran Sea harbors [27,46,49,48]. In addition to this species, many sessile or vagile organisms of conservational importance can also be found in artificial structures (see Table 1). In the case of P. ferruginea, the presence of a strictly protected species on artificial structures has led to a problem for many administrations within the western Mediterranean, as these structures require frequent restoration, modification, or reconstruction [29,49]. The concept of micro-reserve has been developed in eastern Spain for rare endemic plants with small distribution zones, for which the usual conservation areas such as parks or reserves are unsuitable [58,60]. Microreserves are a very useful tool for the conservation of reduced populations of nonmobile organisms such as plants, and should be equally applicable to coastal sessile biota, which are very similar to land plants in terms of dispersion and substrate occupation [40,59]. The terrestrial micro-reserves of the Community of Valencia are located in natural areas, (some of them moderately human-disturbed) but not in artificial places (Figura de protecci´ on de especies silvestres denominada microrreserva vegetal, 1994; [17]). In this regard, García-G´ omez et al. [40,41] proposed a new form of environmental protection, the ‘Artificial Marine Micro-Reserve’ (AMMR), defined as an artificial coastal construction that, by mutual agreement between owners and authorities, is protected due to the environmental value of species or ecosystems it hosts. According to García-G´ omez et al. [40], the criteria to be met by a marine artificial habitat for its protection under an AMMR are the following: 1. It has hosted at least one endangered species, whose individuals are settled naturally. In addition to this, both the recruitment and growth (adult) of these individuals should be present to generate a reproductively viable population. The AMMR could be applied to an entire coastal structure or parts thereof (for example, a section of breakwater), but always presents different age classes and reproductive individuals. The creation of AMMRs should encourage a network to promote genetic bridges. 2. The proposal for the creation of an AMMR must be limited to already build installations, where endangered species have already naturally settled. The positive results of AMMRs must not be used as a reasoning for building a new artificial structure. 3. An AMMR cannot be assigned without the agreement of its owner, public or private. The agreement can be temporary and must be compatible with the normal use of the installation. The AMMR must be permanently armoured with fences and video monitoring, which is not very expensive, since harbors are already guarded by their respective administration. 4. AMMRs must be assigned to a coastline with a good environmental quality of marine waters. In the case it is located inside a port, it ought to be implemented to areas that fall within the quality requirements of the Water Framework Directive 2000/60/EC (hereafter WFD; [21]) and must include an emergency contingency plan for oil spills (i.e. sea booms, oil skimmer, etc.) or different environmental impacts. 5. The statement of AMMRs should not pose a problem in itself. In Table 1 Summary of organisms of conservation importance associated with artificial structures. Group, species Legislation (Nº annexe) Source Algae Cystoseira amentacea Bern Convention (I); Barcelona Convention (II) Susini et al.,[90] Cystoseira barbata Barcelona Convention (II) Perkol-Finkel et al.,[74];[31]; Ferrario et al.,[30] Lithophyllum byssoides Barcelona Convention (II) García-G´ omez et al.,[41]; Present study Gymnogongrus crenulatus Barcelona Convention (II) Present study Porifera Spongia agaricina Bern Convention (III) García-G´ omez et al.,[41] Spongia offinalis Bern Convention (III) de Voogd[95] Tethya aurantium/ Tethya sp. plur. Barcelona Convention (II) García-G´ omez et al.,[41] Cnidaria Astroides calycularis Bern Convention (II), Barcelona Convention (II) García-G´ omez et al.,[41]; present study Lophelia pertusa Habitats; Barcelona Convention (II) Gass & Roberts[42] Mollusca Charonia lampas Bern Convention (II); Barcelona Convention (II) García-G´ omez et al.,[41]; present study Cymbula safiana Bern Convention (II); Barcelona Convention (II) Rivera–Ingraham et al.,[80]; García-G´ omez et al.,[41]; present study Dendropoma cristatum Bern Convention (II); Barcelona Convention (II) García-G´ omez et al.,[41]; present study Lithophaga lithophaga CITES, Bern Convention (II); Barcelona Convention (II) Devescovi & IVEˇ SA[19]; García-G´ omez et al.,[41] Luria lurida Bern Convention (II); Barcelona Convention (II) García-G´ omez et al.,[41] Patella ferruginea Habitats; Bern Convention (II); Barcelona Convention (II) Guerra-Garcıa et al.,[48]; Espinosa et al.,[25,28,27]; García-G´ omez et al.,[41]; Martins et al.,[67]; present study Pinna nobilis Habitats; Barcelona Convention (II) García-G´ omez et al.,[41] Pinna rudis Bern Convention (II); Barcelona Convention (II) García-G´ omez et al.,[41]; present study Crustacea Homarus gammarus Bern Convention (III) Langhamer & Wilhelmsson[61]; García-G´ omez et al.,[41] Maja squinado Bern Convention (III) García-G´ omez et al.,[41]; present study Palinurus elephas IUCN (VU), Bern Convention (III) García-G´ omez et al.,[41] Megabalanus azoricus OSPAR Southward[89] Echinodermata Centrostephanus longispinus Bern Convention (II), Barcelona Convention (II) García-G´ omez et al.,[41]; present study Echinus esculentus IUCN (NT) Moore[68] Ophidiaster ophidianus Bern Convention (II) García-G´ omez et al.,[41]; present study Paracentrotus lividus Bern Convention (III) García-G´ omez et al.,[41]; present study Note: Species were selected if protected under international and/or national legislation. CITES =Convention on International Trade in Endangered Species of Wild Fauna and Flora; IUCN =International Union for Conservation of Nature Red List; NT =Near Threatened; VU =Vulnerable; Bern Convention on the conservation of European wildlife and natural habitats; Barcelona Convention for the Protection of the Mediterranean Sea Against Pollution; Habitats =EU E. Ostal´ e-Valriberas et al. Marine Policy 136 (2022) 104917 3 contrast, it would be an opportunity to protect and monitor endangered and sensitive species together with the competent environmental authority. It can also contribute to control and improve the quality of coastal water effectively and play a significant role in achieving the objectives of the WFD [35,36]. In addition, it should be managed for integration into society and landscape. It must include a management plan that promotes interest in the marine environment and its biota in the local population, as well as encourages environmental education. The creation of artificial marine microreserve networks (AMMRNs), as a new conservation tool, is in line with the interdisciplinary approach of Ecosystem-Based Management (EMB). This methodology balances ecological, social and governmental principles on appropriate temporal and spatial scales in a distinct geographical area to achieve the use of sustainable resources (Long, 2015), hence the AMMR would be a conservation tool for the port sector for a possible action guide. In addition, AMMRs fit conceptually within new management approaches such as ‘novel ecosystems’ (Hobbs et al., [53]) or Locally Managed Marine Area ([54,56]) which have already been developed. Therefore, the AMMR is a new form of protection that has been proposed but not yet implemented. The present study focuses on providing empirical data on its viability. Consequently, the objectives of the present study are (i) to determine whether the artificial coastal defense structures of Ceuta (Strait of Gibraltar) meet the requisites mentioned above for implementing an AMMR and to identify which species could benefit from such protection, and (ii) what effect is expected on the population of the endangered mollusc Patella ferruginea as a model species benefitting from this novel approach. 2. Materials and methods 2.1. Study area The Strait of Gibraltar is one of the marine areas with the greatest biological diversity of the European coastline, hosting typical species from the temperate and subtropical regions of the European and African Atlantic and the Mediterranean, as well as numerous endemic species [14,37]. On the other hand, it is also an area of confluence of many Habitats Directive on the conservation of natural habitats and of wild fauna and flora; OSPAR =Oslo and Paris Conventions. Fig. 1. Study area: A: intertidal sampling zones on Ceuta’s riprap structures (North Bay, South Bay, Inside Harbor) and nearby natural substrata (Natural Zone); B: within the zone ¨Inside Harbor¨, four subzones were considered to the intertidal and subtidal study; C: subtidal sampling subzones; D: different water bodies inside the harbor of Ceuta. Figure modified from the work of S´ anchez-Badorrey & García Anguita [84]. E. Ostal´ e-Valriberas et al.
89 Marine Policy 136 (2022) 104917 2 and thus increase their risk of extinction in the face of certain permanent disturbances [12,1]. In order to handle these impacts, the field of coastal ecological engineering aims to integrate ecology, economy, and society’s need to design artificial marine structures that maintain the greatest biodiversity in relation to the natural environment [7]. Essentially, it represents the incorporation of ecological considerations into the design of artificial marine structures [32]. Such an approach is urgently needed, given that anthropic demands on coastlines are expected to increase in the future [3]. Recent studies have shown that organisms that provide important ecosystem services and even protected species can benefit from artificial structures [33,88]. Some of these protected species have substantial populations inhabiting artificial habitats. This is the case of the endangered limpet Patella ferruginea (Gmelin, 1791), whose densest populations exist in the breakwaters of the Strait of Gibraltar and Alboran Sea harbors [27,46,49,48]. In addition to this species, many sessile or vagile organisms of conservational importance can also be found in artificial structures (see Table 1). In the case of P. ferruginea, the presence of a strictly protected species on artificial structures has led to a problem for many administrations within the western Mediterranean, as these structures require frequent restoration, modification, or reconstruction [29,49]. The concept of micro-reserve has been developed in eastern Spain for rare endemic plants with small distribution zones, for which the usual conservation areas such as parks or reserves are unsuitable [58,60]. Microreserves are a very useful tool for the conservation of reduced populations of nonmobile organisms such as plants, and should be equally applicable to coastal sessile biota, which are very similar to land plants in terms of dispersion and substrate occupation [40,59]. The terrestrial micro-reserves of the Community of Valencia are located in natural areas, (some of them moderately human-disturbed) but not in artificial places (Figura de protecci´ on de especies silvestres denominada microrreserva vegetal, 1994; [17]). In this regard, García-G´ omez et al. [40,41] proposed a new form of environmental protection, the ‘Artificial Marine Micro-Reserve’ (AMMR), defined as an artificial coastal construction that, by mutual agreement between owners and authorities, is protected due to the environmental value of species or ecosystems it hosts. According to García-G´ omez et al. [40], the criteria to be met by a marine artificial habitat for its protection under an AMMR are the following: 1. It has hosted at least one endangered species, whose individuals are settled naturally. In addition to this, both the recruitment and growth (adult) of these individuals should be present to generate a reproductively viable population. The AMMR could be applied to an entire coastal structure or parts thereof (for example, a section of breakwater), but always presents different age classes and reproductive individuals. The creation of AMMRs should encourage a network to promote genetic bridges. 2. The proposal for the creation of an AMMR must be limited to already build installations, where endangered species have already naturally settled. The positive results of AMMRs must not be used as a reasoning for building a new artificial structure. 3. An AMMR cannot be assigned without the agreement of its owner, public or private. The agreement can be temporary and must be compatible with the normal use of the installation. The AMMR must be permanently armoured with fences and video monitoring, which is not very expensive, since harbors are already guarded by their respective administration. 4. AMMRs must be assigned to a coastline with a good environmental quality of marine waters. In the case it is located inside a port, it ought to be implemented to areas that fall within the quality requirements of the Water Framework Directive 2000/60/EC (hereafter WFD; [21]) and must include an emergency contingency plan for oil spills (i.e. sea booms, oil skimmer, etc.) or different environmental impacts. 5. The statement of AMMRs should not pose a problem in itself. In Table 1 Summary of organisms of conservation importance associated with artificial structures. Group, species Legislation (Nº annexe) Source Algae Cystoseira amentacea Bern Convention (I); Barcelona Convention (II) Susini et al.,[90] Cystoseira barbata Barcelona Convention (II) Perkol-Finkel et al.,[74];[31]; Ferrario et al.,[30] Lithophyllum byssoides Barcelona Convention (II) García-G´ omez et al.,[41]; Present study Gymnogongrus crenulatus Barcelona Convention (II) Present study Porifera Spongia agaricina Bern Convention (III) García-G´ omez et al.,[41] Spongia offinalis Bern Convention (III) de Voogd[95] Tethya aurantium/ Tethya sp. plur. Barcelona Convention (II) García-G´ omez et al.,[41] Cnidaria Astroides calycularis Bern Convention (II), Barcelona Convention (II) García-G´ omez et al.,[41]; present study Lophelia pertusa Habitats; Barcelona Convention (II) Gass & Roberts[42] Mollusca Charonia lampas Bern Convention (II); Barcelona Convention (II) García-G´ omez et al.,[41]; present study Cymbula safiana Bern Convention (II); Barcelona Convention (II) Rivera–Ingraham et al.,[80]; García-G´ omez et al.,[41]; present study Dendropoma cristatum Bern Convention (II); Barcelona Convention (II) García-G´ omez et al.,[41]; present study Lithophaga lithophaga CITES, Bern Convention (II); Barcelona Convention (II) Devescovi & IVEˇ SA[19]; García-G´ omez et al.,[41] Luria lurida Bern Convention (II); Barcelona Convention (II) García-G´ omez et al.,[41] Patella ferruginea Habitats; Bern Convention (II); Barcelona Convention (II) Guerra-Garcıa et al.,[48]; Espinosa et al.,[25,28,27]; García-G´ omez et al.,[41]; Martins et al.,[67]; present study Pinna nobilis Habitats; Barcelona Convention (II) García-G´ omez et al.,[41] Pinna rudis Bern Convention (II); Barcelona Convention (II) García-G´ omez et al.,[41]; present study Crustacea Homarus gammarus Bern Convention (III) Langhamer & Wilhelmsson[61]; García-G´ omez et al.,[41] Maja squinado Bern Convention (III) García-G´ omez et al.,[41]; present study Palinurus elephas IUCN (VU), Bern Convention (III) García-G´ omez et al.,[41] Megabalanus azoricus OSPAR Southward[89] Echinodermata Centrostephanus longispinus Bern Convention (II), Barcelona Convention (II) García-G´ omez et al.,[41]; present study Echinus esculentus IUCN (NT) Moore[68] Ophidiaster ophidianus Bern Convention (II) García-G´ omez et al.,[41]; present study Paracentrotus lividus Bern Convention (III) García-G´ omez et al.,[41]; present study Note: Species were selected if protected under international and/or national legislation. CITES =Convention on International Trade in Endangered Species of Wild Fauna and Flora; IUCN =International Union for Conservation of Nature Red List; NT =Near Threatened; VU =Vulnerable; Bern Convention on the conservation of European wildlife and natural habitats; Barcelona Convention for the Protection of the Mediterranean Sea Against Pollution; Habitats =EU E. Ostal´ e-Valriberas et al. Marine Policy 136 (2022) 104917 3 contrast, it would be an opportunity to protect and monitor endangered and sensitive species together with the competent environmental authority. It can also contribute to control and improve the quality of coastal water effectively and play a significant role in achieving the objectives of the WFD [35,36]. In addition, it should be managed for integration into society and landscape. It must include a management plan that promotes interest in the marine environment and its biota in the local population, as well as encourages environmental education. The creation of artificial marine microreserve networks (AMMRNs), as a new conservation tool, is in line with the interdisciplinary approach of Ecosystem-Based Management (EMB). This methodology balances ecological, social and governmental principles on appropriate temporal and spatial scales in a distinct geographical area to achieve the use of sustainable resources (Long, 2015), hence the AMMR would be a conservation tool for the port sector for a possible action guide. In addition, AMMRs fit conceptually within new management approaches such as ‘novel ecosystems’ (Hobbs et al., [53]) or Locally Managed Marine Area ([54,56]) which have already been developed. Therefore, the AMMR is a new form of protection that has been proposed but not yet implemented. The present study focuses on providing empirical data on its viability. Consequently, the objectives of the present study are (i) to determine whether the artificial coastal defense structures of Ceuta (Strait of Gibraltar) meet the requisites mentioned above for implementing an AMMR and to identify which species could benefit from such protection, and (ii) what effect is expected on the population of the endangered mollusc Patella ferruginea as a model species benefitting from this novel approach. 2. Materials and methods 2.1. Study area The Strait of Gibraltar is one of the marine areas with the greatest biological diversity of the European coastline, hosting typical species from the temperate and subtropical regions of the European and African Atlantic and the Mediterranean, as well as numerous endemic species [14,37]. On the other hand, it is also an area of confluence of many Habitats Directive on the conservation of natural habitats and of wild fauna and flora; OSPAR =Oslo and Paris Conventions. Fig. 1. Study area: A: intertidal sampling zones on Ceuta’s riprap structures (North Bay, South Bay, Inside Harbor) and nearby natural substrata (Natural Zone); B: within the zone ¨Inside Harbor¨, four subzones were considered to the intertidal and subtidal study; C: subtidal sampling subzones; D: different water bodies inside the harbor of Ceuta. Figure modified from the work of S´ anchez-Badorrey & García Anguita [84]. E. Ostal´ e-Valriberas et al.
96 Marine Policy 136 (2022) 104917 10 naturally settled. The positive results of AMMRs must not be used as a reason for the construction of a new artificial structure. 3. An AMMR cannot be assigned without the agreement of its owner, public or private. Depending on the status of the species, the agreement can be temporary and must be compatible with the normal use of the installation. The AMMR must be permanently armored with fences and video monitoring, which is not very expensive since the harbors are already guarded by their respective responsible. 4. In the case that it is located inside a port, it ought to be implemented to areas that fall within the quality requirements of the WFD and must include an emergency contingency plan for oil spills (i.e. sea booms, oil skimmer, etc.) or different environmental impacts. The statement of AMMRs should not pose a problem in itself. In contrast, it would be an opportunity to protect and monitor endangered and sensitive species together with the competent environmental authority. In addition, a well management plan can promote to society interest in the marine environment, biota, and port sector ([33]; Janis et al., [55]; O′Neil et al., [70]). The AMMR conservation tool can be introduced into regional or national legislation for the environmental authority, for example, the Government of Gibraltar declared Marine Conservation Zone some areas of the artificial coastal defense structures [66], In addition, AMMRNs can fit within the conceptual framework of several sustainable development or conservation approaches, so that it could be a conservation tool for the port sector in a possible action guide. Moreover, AMMRNs can fit within the conceptual framework of Ecosystem Based Management (EBM; see [64]), ‘novel ecosystems’ (see Hobbs et al., [53]) or more particularly within the concept called Locally Managed Marine Areas (LMMAs). In this sense, Jupiter et al., [56] indicated that “LMMAs have garnered support because of their adaptability to different contexts and focus on locally identified objectives”. These authors concluded that the management actions undertaken on LMMAs included permanent closures, periodically-harvested closures, restrictions on gear, access or species that are the kind of measures that could be easily implemented within AMMRs in artificial substrata. Furthermore, according to the Aichi target 11 (conserving biodiversity in situ), the IUCN has considered the LMMAs as an example of secondary conservation [54] and, consequently, this approach for a more adaptive and locally managed conservation effort has gained attention. In this sense, AMMRs could play a new role in marine conservation. In fact, the marine conservation tool AMMR recognizes coupled socio-ecological systems with stakeholders involved in an integrated and adaptive management process where decisions reflect societal choice, similarly to EBM (Long, 2015). Humanity has been modifying the planet in an unmeasurable way for thousands of years. Recently, this influence has been such that a new era has been proposed: the Anthropocene and the Sixth Extinction, as the ongoing extinction event of species in present times [6,51,57]. Species are becoming extinct at unprecedented rates, even if we ignore the possibility of a considerable extinction debt [50,75]. The urgency of the situation leaves no room for ’paralysis by over-analysis’ (sensu [11]). It is no longer legitimate to assert that the AMMR concept has not been tested and therefore should not be applied. Acknowledgments The authors would like to express their gratitude to our colleagues from the Laboratorio de Biología Marina of the University of Sevilla who provided insight and expertize, which greatly benefitted this research. We thank ´ I˜ nigo Donazar, Javier Pell´ on, ´ Alvaro Sabino and Francisco S´ anchez for their help in the sampling process. We are grateful to María Fig. 7. Size frequency distribution of P. ferruginea over different levels of accessibility (A, B and C). Number of oocytes according to the percentage of females settled in the different levels of protection (D). Table 5 Percentage (%) of recruits, males and females of P. ferruginea individuals according to the different levels of protection. The relation between the size class and the sex ratio was obtained from Espinosa, 2006 and Rivera-Ingraham et al., 2011. Recruit Male Female High 17.78 76.09 6.13 Medium 29.56 69.13 1.31 Low 29.30 70.56 0.14 E. Ostal´ e-Valriberas et al. Marine Policy 136 (2022) 104917 11 Ambrona de la Lastra, Rocío Valriberas and Enrique Ostal´ e for their support in Ceuta. The study could not have been done without them. We are also particularly grateful for the assistance given by the diving center Water Game Gran Azul, especially by Javier Iba˜ nez and Jos´ e Manuel ´ Avila. Thanks also go to Prof. Quentin Hanich and two anonymous referees for their useful comments on the original manuscript. We thank the Instituto de Estudios Ceutíes from Spain for additional financial support with the ¨Convocatoria de ayudas a la investigaci´ on¨2012 and 2015. Appendix A. Supporting information Supplementary data associated with this article can be found in the online version at doi:10.1016/j.marpol.2021.104917. References [1] M.A. Aguilera, J. Tapia, C. Gallardo, P. Nú˜ nez, K. Varas-Belemmi, Loss of coastal ecosystem spatial connectivity and services by urbanization: Natural-to-urban integration for bay management, J. Environ. Manag. 276 (2020), 111297. [2] L. Airoldi, M.W. Beck, L.B. Firth, A.B. Bugnot, P.D. Steinberg, K.A. Dafforn, Emerging solutions to return nature to the urban ocean, Annu. Rev. Mar. Sci. 13 (2021) 445–477. [3] L. Airoldi, M. Abbiati, M.W. Beck, S.J. Hawkins, P.R. Jonsson, D. Martin, P. S. Moschella, A. Sundel¨ of, R.C. Thompson, P. Åberg, An ecological perspective on the deployment and design of low-crested and other hard coastal defence structures, Costa Eng. 52 (2005) 1073–1087. [4] M.J. Anderson, D.C. Walsh, PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing? Ecological monographs 83 (4) (2013) 557–574. [5] M.J. Anderson, R.N. Gorley, R.K. Clarke, PERMANOVA+para PRIMER: Guía para el Programa y M´ etodos Estadísticos. PRIMER-E: Plymouth, UK Massey University,, 2008. [6] A.D. Barnosky, N. Matzke, S. Tomiya, G.O. Wogan, B. Swartz, T.B. Quental, B. Mersey, Has the Earth’s sixth mass extinction already arrived? Nature 471 (7336) (2011) 51–57. [7] S.D. Bergen, S.M. Bolton, J.L. Fridley, Design principles for ecological engineering, Ecol. Eng. 18 (2) (2001) 201–210. [8] C.F. Boudouresque, G. Cadiou, L. Le Dir´ eac’h, Marine protected areas: a tool for coastal areas management, in: Eugene Levner, Igor Linkov, Jean-Marie Proth (Eds.), Strategic Management of Marine Ecosystems, Springer, Dordrecht, 2005, pp. 29–52. [9] G.M. Branch, F. Odendaal, The effects of marine protected areas on the population dynamics of a South African limpet, Cymbula oculus, relative to the influence of wave action, Biol. Conserv. 114 (2) (2003) 255–269. [10] F. Bulleri, M.G. Chapman, The introduction of coastal infrastructure as a driver of change in marine environments, J. Appl. Ecol. 47 (1) (2010) 26–35. [11] C.R. Carroll, G.K. Meffe, Management to meet conservation goals: general principles and applications, in: G.K. Meffe, C.R. Carroll (Eds.), Principles of Conservation Biology, Sinauer Associates, Sunderland, MA, 1994, pp. 307–366. [12] J.M. Chase, S.A. Blowes, T.M. Knight, K. Gerstner, F. May, Ecosystem decay exacerbates biodiversity loss with habitat loss, Nature 584 (7820) (2020) 238–243. [13] K.R. Clarke, R.N. Gorley, PRIMER: Getting Started with v6, 931, PRIMER-E Ltd,, Plymouth, UK, 2005, p. 932. [14] M. Coll, C. Piroddi, J. Steenbeek, K. Kaschner, F. Ben Rais Lasram, J. Aguzzi, E. Ballesteros, C.N. Bianchi, J. Corbera, T. Dailianis, R. Danovaro, M. Estrada, C. Froglia, B.S. Galil, J.M. Gasol, R. Gertwagen, J. Gil, F. Guilhaumon, K. Kesner- Reyes, M.S. Kitsos, A. Koukouras, N. Lampadariou, E. Laxamana, C.M. L´ opez-F´ e de la Cuadra, H.K. Lotze, D. Martin, D. Mouillot, D. Oro, S. Raicevich, J. Rius-Barile, J. I. Saiz-Salinas, C. San Vicente, S. Somot, J. Templado, X. Turon, D. Vafidis, R. Villanueva, E. Voultsiadou, The biodiversity of the Mediterranean Sea: estimates, patterns, and threats, PLOS One 5 (8) (2010), e11842. [15] S. Coppa, G.A. De Lucia, G. Massaro, A. Camedda, S. Marra, P. Magni, F. Espinosa, Is the establishment of MPAs enough to preserve endangered intertidal species? The case of Patella ferruginea in Mal di Ventre Island (W Sardinia, Italy), Aquat. Conserv.: Mar. Freshw. Ecosyst. 26 (4) (2016) 623–638. [16] K.A. Dafforn, T.M. Glasby, L. Airoldi, N.K. Rivero, M. Mayer-Pinto, E.L. Johnston, Marine urbanization: an ecological framework for designing multifunctional artificial structures, Front. Ecol. Environ. 13 (2) (2015) 82–90. [17] Decreto 218/, de 17 de octubre, por el que se crea la figura de protecci´ on de especies silvestres denominada Microrreserva vegetal, Conselleria de Medio Ambiente, Comunidad Valenciana,, 1994. [18] M.N. Dethier, E.S. Graham, S. Cohen, L.M. Tear, Visual versus random-point percent cover estimations:’objective’is not always better, Mar. Ecol. Prog. Ser. 96 (1993) 93–100. [19] M. Devescovi, L. IVEˇ SA, Colonization patterns of the date mussel Lithophaga lithophaga (L., 1758) on limestone breakwater boulders of a marina, Period. Biol. 110 (4) (2008) 339–345. [20] H. Dietz, T. Steinlein, Determination of plant species cover by means of image analysis, J. Veg. Sci. 7 (1) (1996) 131–136. [21] Directiva 2000/60/CE del Parlamento Europeo y del Consejo, de 23 de octubre de 2000, por la que se establece un marco comunitario de actuaci´ on en el ´ ambito de la política de aguas, Diario Oficial de las Comunidades Europeas L 327 de 22.12.2000, 1–73. [22] J.E. Dugan, L. Airoldi, M.G. Chapman, S.J. Walker, T. Schlacher, E. Wolanski, D. McLusky, 8.02-Estuarine and coastal structures: environmental effects, a focus on shore and nearshore structures, Treatise Estuar. Coast. Sci. 8 (2011) 17–41. [23] F. Espinosa, G.A. Rivera-Ingraham, Subcellular evidences of redox imbalance in well-established populations of an endangered limpet. Reasons for alarm? Mar. Pollut. Bull. 109 (1) (2016) 72–80. [24] F. Espinosa, G.A. Rivera-Ingraham, Biological conservation of giant limpets: the implications of large size, Advances in marine biology 76 (2017) 105–155. [25] F. Espinosa, J.M. Guerra-Garcia, F.A. D, J.C. Garcia-Gomez, Aspects of reproduction and their implications for the conservation of the endangered limpet, Patella ferruginea, Invertebr. Reprod. Dev. 49 (1–2) (2006) 85–92. [26] F. Espinosa, G.A. Rivera-Ingraham, D. Fa, J.C. García-G´ omez, Effect of human pressure on population size structures of the endangered ferruginean limpet: toward future management measures, J. Coast. Res. 25 (4) (2009) 857–863. [27] F. Espinosa, G.A. Rivera-Ingraham, E. Ostal´ e-Valriberas, J.C. García-G´ omez, Predicting the fate of the most endangered marine invertebrate of the Mediterranean: The power of long-term monitoring in conservation biology, Aquat. Conserv.: Mar. Freshw. Ecosyst. 28 (6) (2018) 1283–1293. [28] F. Espinosa, A.R. Gonz´ alez, M.J. Maestre, D. Fa, J.M. Guerra-García, J.C. García- G´ omez, Responses of the endangered limpet Patella ferruginea to reintroduction under different environmental conditions: survival, growth rates and life-history, Ital. J. Zool. 75 (4) (2008) 371–384. [29] D.A. Fa, G. Finlayson, J. Sempere-Valverde, J.C. García-G´ omez, ‘Impossible’reintroduction of the endangered limpet Patella ferruginea Gmelin, 1791? Progress in resolving translocation mortality, Endanger. Species Res. 37 (2018) 219–232. [30] F. Ferrario, L. Iveˇ sa, A. Jaklin, S. Perkol-Finkel, L. Airoldi, The overlooked role of biotic factors in controlling the ecological performance of artificial marine habitats, J. Appl. Ecol. 53 (1) (2016) 16–24. [31] L.B. Firth, M. Schofield, F.J. White, M.W. Skov, S.J. Hawkins, Biodiversity in intertidal rock pools: informing engineering criteria for artificial habitat enhancement in the built environment, Mar. Environ. Res. 102 (2014) 122–130. [32] L.B. Firth, R.C. Thompson, K. Bohn, M. Abbiati, L. Airoldi, T.J. Bouma, S. J. Hawkins, Between a rock and a hard place: environmental and engineering considerations when designing coastal defence structures, Coast. Eng. 87 (2014) 122–135. [33] Firth, L.B., Knights, A.M., Bridger, D., Evans, A., Mieskowska, N., Moore, P.J.,. & Hawkins, S.J. (2016). Ocean sprawl: challenges and opportunities for biodiversity management in a changing world. [34] M.S. Foster, C. Harrold, D.D. Hardin, Point vs. photo quadrat estimates of the cover of sessile marine organisms, J. Exp. Mar. Biol. Ecol. 146 (2) (1991) 193–203. [35] J.C. García-G´ omez, Biota litoral y vigilancia ambiental en las ´ Areas Marinas Protegidas, Consejería de Medio Ambiente,, Junta de Andalucía, 2007. [36] J.C. García-G´ omez, A guide on environmental monitoring of rocky seabeds in Mediterranean Marine Protected Areas and surrounding zones, Marine Biology Laboratory, Department of Zoology, Faculty of Biology, University of Seville,, 2015. [37] J.C. García-G´ omez, S.M. Rubio, Bucear en el último confín de Europa, la isla de Tarifa, Instituto de Estudios Campogibraltare˜ nos,, 2010. [38] J.C. García-G´ omez, A.R. Gonz´ alez, M.J. Maestre, F. Espinosa, Detect coastal disturbances and climate change effects in coralligenous community through sentinel stations, PLOS One 15 (5) (2020), e0231641. [39] J.C. García-G´ omez, J. Sempere-Valverde, A.R. Gonz´ alez, M. Martínez-Chac´ on, L. Olaya-Ponzone, E. S´ anchez-Moyano, E. Ostal´ e-Valriberas, C. Megina, From exotic to invasive in record time: the extreme impact of Rugulopteryx okamurae (Dictyotales, Ochrophyta) in the strait of Gibraltar, Sci. Total Environ. 704 (2020), 135408. [40] J.C. García-G´ omez, C.M. L´ opez-F´ e, F. Espinosa, J.M. Guerra-García, G.A. Rivera- Ingraham, Marine artificial micro-reserves: a possibility for the conservation of endangered species living on artificial substrata, Mar. Ecol. 32 (1) (2011) 6–14. [41] J.C. García-G´ omez, J.M. Guerra-García, F. Espinosa, M.J. Maestre, G. Rivera- Ingraham, D. Fa, C.M. L´ opez-F´ e, Artificial M arine M icro-R eserves N etworks (AMMRN s): an innovative approach to conserve marine littoral biodiversity and protect endangered species, Mar. Ecol. 36 (3) (2015) 259–277. [42] S.E. Gass, J.M. Roberts, The occurrence of the cold-water coral Lophelia pertusa (Scleractinia) on oil and gas platforms in the North Sea: colony growth, recruitment and environmental controls on distribution, Mar. Pollut. Bull. 52 (5) (2006) 549–559. [43] Rachel K. Gittman, F. Joel Fodrie, Alyssa M. Popowich, Danielle A. Keller, John F. Bruno, Carolyn A. Currin, Charles H. Peterson, Michael F. Piehler, Engineering away our natural defenses: an analysis of shoreline hardening in the US, Front. Ecol. Environ. 13 (6) (2015) 301–307, https://doi.org/10.1890/150065. [44] A. Govarets, B. Lauwerts, Assessment of the Impact of Coastal Defence Structures, Biodiversity series: OSPAR Commission,, 2009. [45] M.J. Groom, G.K. Meffe, C.R. Carroll, S.J. Andelman. Principles of Conservation Biology, Sinauer Associates,, Sunderland, 2006 ((No. Sirsi) i9780878935185)). [46] J. Guallart, A.A. Luque, I. Acevedo, M. Calvo, Distribution and updated census of the ferrugineous limpet (Patella ferruginea Gmelin, 1791) in the littoral of Melilla (SW Mediterranean), Iberus 31 (2013) 21–51. [47] J.M. Guerra-Garcia, J.C. García-G´ omez, Oxygen levels versus chemical pollutants: do they have similar influence on macrofaunal assemblages? A case study in a harbour with two opposing entrances, Environ. Pollut. 135 (2) (2005) 281–291. E. Ostal´ e-Valriberas et al.
97 Marine Policy 136 (2022) 104917 11 Ambrona de la Lastra, Rocío Valriberas and Enrique Ostal´ e for their support in Ceuta. The study could not have been done without them. We are also particularly grateful for the assistance given by the diving center Water Game Gran Azul, especially by Javier Iba˜ nez and Jos´ e Manuel ´ Avila. Thanks also go to Prof. Quentin Hanich and two anonymous referees for their useful comments on the original manuscript. We thank the Instituto de Estudios Ceutíes from Spain for additional financial support with the ¨Convocatoria de ayudas a la investigaci´ on¨2012 and 2015. Appendix A. Supporting information Supplementary data associated with this article can be found in the online version at doi:10.1016/j.marpol.2021.104917. References [1] M.A. Aguilera, J. Tapia, C. Gallardo, P. Nú˜ nez, K. Varas-Belemmi, Loss of coastal ecosystem spatial connectivity and services by urbanization: Natural-to-urban integration for bay management, J. Environ. Manag. 276 (2020), 111297. [2] L. Airoldi, M.W. Beck, L.B. Firth, A.B. Bugnot, P.D. Steinberg, K.A. Dafforn, Emerging solutions to return nature to the urban ocean, Annu. Rev. Mar. Sci. 13 (2021) 445–477. [3] L. Airoldi, M. Abbiati, M.W. Beck, S.J. Hawkins, P.R. Jonsson, D. Martin, P. S. Moschella, A. Sundel¨ of, R.C. Thompson, P. Åberg, An ecological perspective on the deployment and design of low-crested and other hard coastal defence structures, Costa Eng. 52 (2005) 1073–1087. [4] M.J. Anderson, D.C. Walsh, PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing? Ecological monographs 83 (4) (2013) 557–574. [5] M.J. Anderson, R.N. Gorley, R.K. Clarke, PERMANOVA+para PRIMER: Guía para el Programa y M´ etodos Estadísticos. PRIMER-E: Plymouth, UK Massey University,, 2008. [6] A.D. Barnosky, N. Matzke, S. Tomiya, G.O. Wogan, B. Swartz, T.B. Quental, B. Mersey, Has the Earth’s sixth mass extinction already arrived? Nature 471 (7336) (2011) 51–57. [7] S.D. Bergen, S.M. Bolton, J.L. Fridley, Design principles for ecological engineering, Ecol. Eng. 18 (2) (2001) 201–210. [8] C.F. Boudouresque, G. Cadiou, L. Le Dir´ eac’h, Marine protected areas: a tool for coastal areas management, in: Eugene Levner, Igor Linkov, Jean-Marie Proth (Eds.), Strategic Management of Marine Ecosystems, Springer, Dordrecht, 2005, pp. 29–52. [9] G.M. Branch, F. Odendaal, The effects of marine protected areas on the population dynamics of a South African limpet, Cymbula oculus, relative to the influence of wave action, Biol. Conserv. 114 (2) (2003) 255–269. [10] F. Bulleri, M.G. Chapman, The introduction of coastal infrastructure as a driver of change in marine environments, J. Appl. Ecol. 47 (1) (2010) 26–35. [11] C.R. Carroll, G.K. Meffe, Management to meet conservation goals: general principles and applications, in: G.K. Meffe, C.R. Carroll (Eds.), Principles of Conservation Biology, Sinauer Associates, Sunderland, MA, 1994, pp. 307–366. [12] J.M. Chase, S.A. Blowes, T.M. Knight, K. Gerstner, F. May, Ecosystem decay exacerbates biodiversity loss with habitat loss, Nature 584 (7820) (2020) 238–243. [13] K.R. Clarke, R.N. Gorley, PRIMER: Getting Started with v6, 931, PRIMER-E Ltd,, Plymouth, UK, 2005, p. 932. [14] M. Coll, C. Piroddi, J. Steenbeek, K. Kaschner, F. Ben Rais Lasram, J. Aguzzi, E. Ballesteros, C.N. Bianchi, J. Corbera, T. Dailianis, R. Danovaro, M. Estrada, C. Froglia, B.S. Galil, J.M. Gasol, R. Gertwagen, J. Gil, F. Guilhaumon, K. Kesner- Reyes, M.S. Kitsos, A. Koukouras, N. Lampadariou, E. Laxamana, C.M. L´ opez-F´ e de la Cuadra, H.K. Lotze, D. Martin, D. Mouillot, D. Oro, S. Raicevich, J. Rius-Barile, J. I. Saiz-Salinas, C. San Vicente, S. Somot, J. Templado, X. Turon, D. Vafidis, R. Villanueva, E. Voultsiadou, The biodiversity of the Mediterranean Sea: estimates, patterns, and threats, PLOS One 5 (8) (2010), e11842. [15] S. Coppa, G.A. De Lucia, G. Massaro, A. Camedda, S. Marra, P. Magni, F. Espinosa, Is the establishment of MPAs enough to preserve endangered intertidal species? The case of Patella ferruginea in Mal di Ventre Island (W Sardinia, Italy), Aquat. Conserv.: Mar. Freshw. Ecosyst. 26 (4) (2016) 623–638. [16] K.A. Dafforn, T.M. Glasby, L. Airoldi, N.K. Rivero, M. Mayer-Pinto, E.L. Johnston, Marine urbanization: an ecological framework for designing multifunctional artificial structures, Front. Ecol. Environ. 13 (2) (2015) 82–90. [17] Decreto 218/, de 17 de octubre, por el que se crea la figura de protecci´ on de especies silvestres denominada Microrreserva vegetal, Conselleria de Medio Ambiente, Comunidad Valenciana,, 1994. [18] M.N. Dethier, E.S. Graham, S. Cohen, L.M. Tear, Visual versus random-point percent cover estimations:’objective’is not always better, Mar. Ecol. Prog. Ser. 96 (1993) 93–100. [19] M. Devescovi, L. IVEˇ SA, Colonization patterns of the date mussel Lithophaga lithophaga (L., 1758) on limestone breakwater boulders of a marina, Period. Biol. 110 (4) (2008) 339–345. [20] H. Dietz, T. Steinlein, Determination of plant species cover by means of image analysis, J. Veg. Sci. 7 (1) (1996) 131–136. [21] Directiva 2000/60/CE del Parlamento Europeo y del Consejo, de 23 de octubre de 2000, por la que se establece un marco comunitario de actuaci´ on en el ´ ambito de la política de aguas, Diario Oficial de las Comunidades Europeas L 327 de 22.12.2000, 1–73. [22] J.E. Dugan, L. Airoldi, M.G. Chapman, S.J. Walker, T. Schlacher, E. Wolanski, D. McLusky, 8.02-Estuarine and coastal structures: environmental effects, a focus on shore and nearshore structures, Treatise Estuar. Coast. Sci. 8 (2011) 17–41. [23] F. Espinosa, G.A. Rivera-Ingraham, Subcellular evidences of redox imbalance in well-established populations of an endangered limpet. Reasons for alarm? Mar. Pollut. Bull. 109 (1) (2016) 72–80. [24] F. Espinosa, G.A. Rivera-Ingraham, Biological conservation of giant limpets: the implications of large size, Advances in marine biology 76 (2017) 105–155. [25] F. Espinosa, J.M. Guerra-Garcia, F.A. D, J.C. Garcia-Gomez, Aspects of reproduction and their implications for the conservation of the endangered limpet, Patella ferruginea, Invertebr. Reprod. Dev. 49 (1–2) (2006) 85–92. [26] F. Espinosa, G.A. Rivera-Ingraham, D. Fa, J.C. García-G´ omez, Effect of human pressure on population size structures of the endangered ferruginean limpet: toward future management measures, J. Coast. Res. 25 (4) (2009) 857–863. [27] F. Espinosa, G.A. Rivera-Ingraham, E. Ostal´ e-Valriberas, J.C. García-G´ omez, Predicting the fate of the most endangered marine invertebrate of the Mediterranean: The power of long-term monitoring in conservation biology, Aquat. Conserv.: Mar. Freshw. Ecosyst. 28 (6) (2018) 1283–1293. [28] F. Espinosa, A.R. Gonz´ alez, M.J. Maestre, D. Fa, J.M. Guerra-García, J.C. García- G´ omez, Responses of the endangered limpet Patella ferruginea to reintroduction under different environmental conditions: survival, growth rates and life-history, Ital. J. Zool. 75 (4) (2008) 371–384. [29] D.A. Fa, G. Finlayson, J. Sempere-Valverde, J.C. García-G´ omez, ‘Impossible’reintroduction of the endangered limpet Patella ferruginea Gmelin, 1791? Progress in resolving translocation mortality, Endanger. Species Res. 37 (2018) 219–232. [30] F. Ferrario, L. Iveˇ sa, A. Jaklin, S. Perkol-Finkel, L. Airoldi, The overlooked role of biotic factors in controlling the ecological performance of artificial marine habitats, J. Appl. Ecol. 53 (1) (2016) 16–24. [31] L.B. Firth, M. Schofield, F.J. White, M.W. Skov, S.J. Hawkins, Biodiversity in intertidal rock pools: informing engineering criteria for artificial habitat enhancement in the built environment, Mar. Environ. Res. 102 (2014) 122–130. [32] L.B. Firth, R.C. Thompson, K. Bohn, M. Abbiati, L. Airoldi, T.J. Bouma, S. J. Hawkins, Between a rock and a hard place: environmental and engineering considerations when designing coastal defence structures, Coast. Eng. 87 (2014) 122–135. [33] Firth, L.B., Knights, A.M., Bridger, D., Evans, A., Mieskowska, N., Moore, P.J.,. & Hawkins, S.J. (2016). Ocean sprawl: challenges and opportunities for biodiversity management in a changing world. [34] M.S. Foster, C. Harrold, D.D. Hardin, Point vs. photo quadrat estimates of the cover of sessile marine organisms, J. Exp. Mar. Biol. Ecol. 146 (2) (1991) 193–203. [35] J.C. García-G´ omez, Biota litoral y vigilancia ambiental en las ´ Areas Marinas Protegidas, Consejería de Medio Ambiente,, Junta de Andalucía, 2007. [36] J.C. García-G´ omez, A guide on environmental monitoring of rocky seabeds in Mediterranean Marine Protected Areas and surrounding zones, Marine Biology Laboratory, Department of Zoology, Faculty of Biology, University of Seville,, 2015. [37] J.C. García-G´ omez, S.M. Rubio, Bucear en el último confín de Europa, la isla de Tarifa, Instituto de Estudios Campogibraltare˜ nos,, 2010. [38] J.C. García-G´ omez, A.R. Gonz´ alez, M.J. Maestre, F. Espinosa, Detect coastal disturbances and climate change effects in coralligenous community through sentinel stations, PLOS One 15 (5) (2020), e0231641. [39] J.C. García-G´ omez, J. Sempere-Valverde, A.R. Gonz´ alez, M. Martínez-Chac´ on, L. Olaya-Ponzone, E. S´ anchez-Moyano, E. Ostal´ e-Valriberas, C. Megina, From exotic to invasive in record time: the extreme impact of Rugulopteryx okamurae (Dictyotales, Ochrophyta) in the strait of Gibraltar, Sci. Total Environ. 704 (2020), 135408. [40] J.C. García-G´ omez, C.M. L´ opez-F´ e, F. Espinosa, J.M. Guerra-García, G.A. Rivera- Ingraham, Marine artificial micro-reserves: a possibility for the conservation of endangered species living on artificial substrata, Mar. Ecol. 32 (1) (2011) 6–14. [41] J.C. García-G´ omez, J.M. Guerra-García, F. Espinosa, M.J. Maestre, G. Rivera- Ingraham, D. Fa, C.M. L´ opez-F´ e, Artificial M arine M icro-R eserves N etworks (AMMRN s): an innovative approach to conserve marine littoral biodiversity and protect endangered species, Mar. Ecol. 36 (3) (2015) 259–277. [42] S.E. Gass, J.M. Roberts, The occurrence of the cold-water coral Lophelia pertusa (Scleractinia) on oil and gas platforms in the North Sea: colony growth, recruitment and environmental controls on distribution, Mar. Pollut. Bull. 52 (5) (2006) 549–559. [43] Rachel K. Gittman, F. Joel Fodrie, Alyssa M. Popowich, Danielle A. Keller, John F. Bruno, Carolyn A. Currin, Charles H. Peterson, Michael F. Piehler, Engineering away our natural defenses: an analysis of shoreline hardening in the US, Front. Ecol. Environ. 13 (6) (2015) 301–307, https://doi.org/10.1890/150065. [44] A. Govarets, B. Lauwerts, Assessment of the Impact of Coastal Defence Structures, Biodiversity series: OSPAR Commission,, 2009. [45] M.J. Groom, G.K. Meffe, C.R. Carroll, S.J. Andelman. Principles of Conservation Biology, Sinauer Associates,, Sunderland, 2006 ((No. Sirsi) i9780878935185)). [46] J. Guallart, A.A. Luque, I. Acevedo, M. Calvo, Distribution and updated census of the ferrugineous limpet (Patella ferruginea Gmelin, 1791) in the littoral of Melilla (SW Mediterranean), Iberus 31 (2013) 21–51. [47] J.M. Guerra-Garcia, J.C. García-G´ omez, Oxygen levels versus chemical pollutants: do they have similar influence on macrofaunal assemblages? A case study in a harbour with two opposing entrances, Environ. Pollut. 135 (2) (2005) 281–291. E. Ostal´ e-Valriberas et al.
98 Marine Policy 136 (2022) 104917 12 [48] J.M. Guerra-Garcıa, J. Corzo, F. Espinosa, J.C. García-G´ omez, Assessing habitat use of the endangered marine mollusc Patella ferruginea (Gastropoda, Patellidae) in northern Africa: preliminary results and implications for conservation, Biol. Conserv. 116 (3) (2004) 319–326. [49] J.M. Guerra-García, J. Corzo, F. Espinosa, D. Fa, J.C. García-G´ omez, Extinction risk and harbours as marine reserves? J. Mollusca Stud. 70 (1) (2004) 96–98. [50] I. Hanski, O. Ovaskainen, Extinction debt at extinction threshold, Conserv. Biol. 16 (3) (2002) 666–673. [51] Q. He, B.R. Silliman, Climate change, human impacts, and coastal ecosystems in the Anthropocene, Curr. Biol. 29 (19) (2019) R1021–R1035. [52] M.A. Hixon, D.W. Johnson, S.M. Sogard, BOFFFFs: on the importance of conserving old-growth age structure in fishery populations, ICES J. Mar. Sci. 71 (8) (2014) 2171–2185. [53] R.J. Hobbs, E. Higgs, J.A. Harris, Novel ecosystems: implications for conservation and restoration, Trends in ecology & evolution 24 (11) (2009) 599–605. [54] IUCN-WCPA Task Force on OECMs, Recognising and Reporting Other Effective Area-based Conservation Measures, IUCN,, Gland, Switzerland, 2019 doi.org/ 10.2305/IUCN.CH.2019.PATRS.3.en. [55] S. Janis, L. Birney, R. Newton, Billion oyster project: linking public school teaching and learning to ecological restoration of New York Harbor using innovative applications of environmental and digital technologies, International journal of digital content technology and its applications 10 (1) (2016). [56] S.D. Jupiter, P.J. Cohen, R. Weeks, A. Tawake, H. Govan, Locally-managed marine areas: multiple objectives and diverse strategies, Pac. Conserv. Biol. 20 (2) (2014) 165–179. [57] E. Kolbert, The Sixth Extinction: An Unnatural History, A&C Black,, 2014. [58] E. Laguna, The micro-reserves as a tool for conservation of threatened plants in Europe, Nat. Environ. Ser. 121 (1.119) (2001). [59] E. Laguna, S. Fos, J. Jim´ enez, S. Volis, Role of micro-reserves in conservation of endemic, rare and endangered plants of the Valencian region (Eastern Spain), Isr. J. Plant Sci. 63 (4) (2016) 320–332. [60] E. Laguna, V.I. Deltoro, J. P´ erez-Botella, P. P´ erez-Rovira, L. Serra, A. Olivares, C. Fabregat, The role of small reserves in plant conservation in a region of high diversity in eastern Spain, Biol. Conserv. 119 (3) (2004) 421–426. [61] O. Langhamer, D. Wilhelmsson, Colonisation of fish and crabs of wave energy foundations and the effects of manufactured holes–a field experiment, Mar. Environ. Res. 68 (4) (2009) 151–157. [62] A. Lattos, K. Bitchava, I.A. Giantsis, J.A. Theodorou, C. Batargias, B. Michaelidis, The implication of vibrio bacteria in the winter mortalities of the critically endangered Pinna nobilis, Microorganisms 9 (5) (2021) 922. [63] G.H. Leonard, R.P. Clark, Point quadrat versus video transect estimates of the cover of benthic red algae, Mar. Ecol.-Prog. Ser. 101 (1993) 203–203–208. [64] R.D. Long, A. Charles, R.L. Stephenson, Key principles of marine ecosystem-based management, Mar. Policy 57 (2015) 53–60. [65] ´ A.A. Luque, J. Guallart, J.T. Gonz´ alez, M. Pola, Recopilaci´ on y an´ alisis de la informaci´ on científica disponible sobre Patella ferruginea, Sociedad Espa˜ nola de Malacología,, 2018. [66] Marine Protection Regulations, LN. 2014/180, 2014. [67] G.M. Martins, R.C. Thompson, A.I. Neto, S.J. Hawkins, S.R. Jenkins, Enhancing stocks of the exploited limpet Patella candei d′Orbigny via modifications in coastal engineering, Biol. Conserv. 143 (1) (2010) 203–211. [68] H.B. Moore, A comparison of the biology of Echinus esculentus in different habitats, J. Mar. Biol. Assoc. 19 (2) (1934) 869–885. [69] R.F. Noss, Indicators for monitoring biodiversity: a hierarchical approach, Conserv. Biol. 4 (4) (1990) 355–364. [70] J.M. O’Neil, R.J. Newton, E.K. Bone, L.B. Birney, A.E. Green, B. Merrick, A. Fraioli, Using urban harbors for experiential, environmental literacy: Case studies of New York and Chesapeake Bay, Regional Studies in Marine Science 33 (2020), 100886. [71] A. Ospina-Alvarez, S. de Juan, J. Al´ os, G. Basterretxea, A. Alonso-Fern´ andez, G. Follana-Bern´ a, I.A. Catal´ an, MPA network design based on graph theory and emergent properties of larval dispersal, Mar. Ecol. Prog. Ser. 650 (2020) 309–326. [72] J. Pallant, SPSS Survival Manual: A Step by Step Guide to Data Analysis Using IBM SPSS, Routledge, 2020. [73] M. Paracuellos, J.C. Nevado, D. Moreno, A. Gim´ enez, J.J. Alesina, Conservational status and demographic characteristics of Patella ferruginea Gmelin, 1791 (Mollusca, gastropoda) on the Alboran Island (Western Mediterranean), Anim. Biodivers. Conserv. 26 (2) (2003) 29–37. [74] S. Perkol-Finkel, F. Ferrario, V. Nicotera, L. Airoldi, Conservation challenges in urban seascapes: promoting the growth of threatened species on coastal infrastructures, J. Appl. Ecol. 49 (6) (2012) 1457–1466. [75] S.L. Pimm, G.J. Russell, J.L. Gittleman, T.M. Brooks, The future of biodiversity, Science 269 (5222) (1995) 347–350. [76] F. Piniella, J. Walliser, Maritime safety in the strait of gibraltar: taxonomy and evolution of emergencies rate in 2000-2004 period, J. Marit. Res. 10 (1) (2013) 25–30. [77] M.A. Ramos, Implementing the habitats directive for mollusc species in Spain, J. Conchol. Spec. Publ. 2 (1998) 125–132. [78] G.A. Rivera-Ingraham, F. Espinosa, J.C. García-G´ omez, Environmentally mediated sex change in the endangered limpet Patella ferruginea (Gastropoda: Patellidae), J. Mollusca Stud. 77 (3) (2011) 226–231. [79] G.A. Rivera-Ingraham, G. Malanga, S. Puntarulo, A.F. P´ erez, A. Ruiz-Tabares, M. Maestre, J.C. García-G´ omez, Antioxidant defenses and trace metal bioaccumulation capacity of Cymbula nigra (Gastropoda: Patellidae), Water, Air, Soil Pollut. 224 (3) (2013) 1–13. [80] G.A. Rivera–Ingraham, F. Espinosa, J.C. García–G´ omez, Present status of the endangered limpet Cymbula nigra (Gastropoda, Patellidae) in Ceuta: how do substrate heterogeneity and area accessibility affect population structure? Anim. Biodivers. Conserv. 34 (2) (2011) 319–330. [81] G.A. Rivera–Ingraham, F. Espinosa, J.C. García–G´ omez, Present status of the endangered limpet Cymbula nigra (Gastropoda, Patellidae) in Ceuta: how do substrate heterogeneity and area accessibility affect population structure? Anim. Biodivers. Conserv. 34 (2) (2011) 319–330. [82] J.M. ROBERGE, P.E.R. Angelstam, Usefulness of the umbrella species concept as a conservation tool, Conserv. Biol. 18 (1) (2004) 76–85. [83] A. Ruiz-Tabares, I. Gordillo, J.R. Corzo, J.C. García-G´ omez, Macrofitobentos mediolitoral y delimitaci´ on de ´ areas sensibles a la contaminaci´ on marina en el litoral ceutí (estrecho de Gibraltar), Bol. Inst. Esp. De. Oceanogr. 19 (1–4) (2011) 93–103. [84] S´ anchez-Badorrey E. & García Anguita F.J. (2015). Informe final: Bases científicas para la implantaci´ on de la Directiva Marco del Agua en el litoral ceutí. Institudo de Estudios Ceutíes (unpublished report). [85] E. S´ anchez-Badorrey, J.A. García-García, R. Ortego-Jurado, F.J. García Anguita, Variabilidad clim´ atica, renovaci´ on y calidad de las aguas del puerto de Ceuta y su entorno, Instituto de Estudios Ceutíes,, 2021, pp. 115–118. ISBN: 978-84-16595- 30-3. [86] D. Sanna, P. Cossu, G.L. Dedola, F. Scarpa, F. Maltagliati, A. Castelli, P. Franzoi, T. Lai, B. Cristo, M. Curini-Galletti, P. Francalacci, M. Casu, Surviving at the edge of a fragmented range: patterns of genetic diversity in isolated populations of the endangered giant Mediterranean limpet (Patella ferruginea), Mar. Biol. 164 (3) (2017) 41. [87] J. Sempere-Valverde, E. Ostal´ e-Valriberas, M. Maestre, R.G. Aranda, H. Bazairi, F. Espinosa, Impacts of the non-indigenous seaweed Rugulopteryx okamurae on a Mediterranean coralligenous community (Strait of Gibraltar): The role of long-term monitoring, Ecol. Indic. 121 (2021), 107135. [88] A. Shabtay, M.E. Portman, Y. Carmel, Contributions of marine infrastructures to marine planning and protected area networking, Aquat. Conserv.: Mar. Freshw. Ecosyst. 28 (4) (2018) 830–839. [89] A.J. Southward, New observations on barnacles (Crustacea: Cirripedia) of the Azores region, Arquipelago. Life Mar. Sci. 16 (1998) 11–27. [90] M.L. Susini, L. Mangialajo, T. Thibaut, A. Meinesz, Development of a transplantation technique of Cystoseira amentacea var. stricta and Cystoseira compressa, in: G. Relini, J. Ryland (Eds.), Biodiversity in Enclosed Seas and Artificial Marine Habitats, Springer, Dordrecht, 2007, pp. 241–244. [91] S. Taljaard, J.H. Slinger, S. Arabi, S.P. Weerts, H. Vreugdenhil, The natural environment in port development: a ‘green handbrake’or an equal partner? Ocean Coast. Manag. 199 (2021), 105390. [92] A.J. Underwood. Experiments in ecology: their logical design and interpretation using analysis of variance, Cambridge University Press, Cambridge, 1997. [93] M. V´ azquez-Luis, E. ´ Alvarez, A. Barrajon, J.R. Garcia-March, A. Grau, I. E. Hendriks, S. Deudero, SOS Pinna nobilis: a mass mortality event in western Mediterranean Sea, Frontiers in Marine Science 4 (2017) 220. [94] V. Vikolainen, H. Bressers, K. Lulofs, A shift toward building with nature in the dredging and port development industries: managerial implications for projects in or near natura 2000 areas, Environ. Manag. 54 (1) (2014) 3–13. [95] N.J. de Voogd, The mariculture potential of the Indonesian reef-dwelling sponge Callyspongia (Euplacella) biru: growth, survival and bioactive compounds, Aquaculture 262 (1) (2007) 54–64. E. Ostal´ e-Valriberas et al. Table 1: Species list of the intertidal benthic community. FLORA Fucus spiralis 4 Siphonaria pectinata Dyctiota dichotoma Mytilus galloprovincialis 6 Chlorophyceae Colpomenia sinuosa Gibbula sp. Ulva clathrata Padina pavonica Echinolittorina punctata Ulva rigida Melarhaphe neritoides Chaetomorpha gracilis Ochrophyta Dendropoma cristatum 1,2,4 Codium adhaerens Ralfsia verrucosa Pomatoceros sp. Ocenebra edwardsii Rhodophyceae FUNGI Lepidochitona sp. Asparagopsis armata 5 Acanthochitona fascicularis Ellisolandia elongata Ascomycota Leiosolenus aristatus Jania rubens Verrucaria maura Lithophyllum byssoides 1,2,4 Arthropoda Lithophyllum sp. BACTERIA Pollicipes pollicipes 6 Mesophyllum lichenoides Chthamalus sp. Mesophyllum sp. Cyanophyceae Perforatus perforates Caulacanthus ustulatus Rivularia sp. Hildenbrandia rubra FAUNA Cnidaria Gelidium sp. Actinia equina 4 Valonia utricularis Mollusca Anemonia sulcata Osmundea pinnatifida Patella ferruginea 1,2,3,4 Astroides calycularis 1,2,4,5 Gymnogongrus crenulatus 2 Cymbula safiana 1,2 Patella rustica Equinodermata Phaeophyceae Patella caerulea Paracentrotus lividus 1 1: Annex I (flora) y II (fauna) Berne Convention; 2: Annex II Barcelona Convention; 3: Annex IV Directive 92/43; 4: Bioindicators species; 5: Invasive or non-indigenous species; 6: Regulated harvesting species.
99 Marine Policy 136 (2022) 104917 12 [48] J.M. Guerra-Garcıa, J. Corzo, F. Espinosa, J.C. García-G´ omez, Assessing habitat use of the endangered marine mollusc Patella ferruginea (Gastropoda, Patellidae) in northern Africa: preliminary results and implications for conservation, Biol. Conserv. 116 (3) (2004) 319–326. [49] J.M. Guerra-García, J. Corzo, F. Espinosa, D. Fa, J.C. García-G´ omez, Extinction risk and harbours as marine reserves? J. Mollusca Stud. 70 (1) (2004) 96–98. [50] I. Hanski, O. Ovaskainen, Extinction debt at extinction threshold, Conserv. Biol. 16 (3) (2002) 666–673. [51] Q. He, B.R. Silliman, Climate change, human impacts, and coastal ecosystems in the Anthropocene, Curr. Biol. 29 (19) (2019) R1021–R1035. [52] M.A. Hixon, D.W. Johnson, S.M. Sogard, BOFFFFs: on the importance of conserving old-growth age structure in fishery populations, ICES J. Mar. Sci. 71 (8) (2014) 2171–2185. [53] R.J. Hobbs, E. Higgs, J.A. Harris, Novel ecosystems: implications for conservation and restoration, Trends in ecology & evolution 24 (11) (2009) 599–605. [54] IUCN-WCPA Task Force on OECMs, Recognising and Reporting Other Effective Area-based Conservation Measures, IUCN,, Gland, Switzerland, 2019 doi.org/ 10.2305/IUCN.CH.2019.PATRS.3.en. [55] S. Janis, L. Birney, R. Newton, Billion oyster project: linking public school teaching and learning to ecological restoration of New York Harbor using innovative applications of environmental and digital technologies, International journal of digital content technology and its applications 10 (1) (2016). [56] S.D. Jupiter, P.J. Cohen, R. Weeks, A. Tawake, H. Govan, Locally-managed marine areas: multiple objectives and diverse strategies, Pac. Conserv. Biol. 20 (2) (2014) 165–179. [57] E. Kolbert, The Sixth Extinction: An Unnatural History, A&C Black,, 2014. [58] E. Laguna, The micro-reserves as a tool for conservation of threatened plants in Europe, Nat. Environ. Ser. 121 (1.119) (2001). [59] E. Laguna, S. Fos, J. Jim´ enez, S. Volis, Role of micro-reserves in conservation of endemic, rare and endangered plants of the Valencian region (Eastern Spain), Isr. J. Plant Sci. 63 (4) (2016) 320–332. [60] E. Laguna, V.I. Deltoro, J. P´ erez-Botella, P. P´ erez-Rovira, L. Serra, A. Olivares, C. Fabregat, The role of small reserves in plant conservation in a region of high diversity in eastern Spain, Biol. Conserv. 119 (3) (2004) 421–426. [61] O. Langhamer, D. Wilhelmsson, Colonisation of fish and crabs of wave energy foundations and the effects of manufactured holes–a field experiment, Mar. Environ. Res. 68 (4) (2009) 151–157. [62] A. Lattos, K. Bitchava, I.A. Giantsis, J.A. Theodorou, C. Batargias, B. Michaelidis, The implication of vibrio bacteria in the winter mortalities of the critically endangered Pinna nobilis, Microorganisms 9 (5) (2021) 922. [63] G.H. Leonard, R.P. Clark, Point quadrat versus video transect estimates of the cover of benthic red algae, Mar. Ecol.-Prog. Ser. 101 (1993) 203–203–208. [64] R.D. Long, A. Charles, R.L. Stephenson, Key principles of marine ecosystem-based management, Mar. Policy 57 (2015) 53–60. [65] ´ A.A. Luque, J. Guallart, J.T. Gonz´ alez, M. Pola, Recopilaci´ on y an´ alisis de la informaci´ on científica disponible sobre Patella ferruginea, Sociedad Espa˜ nola de Malacología,, 2018. [66] Marine Protection Regulations, LN. 2014/180, 2014. [67] G.M. Martins, R.C. Thompson, A.I. Neto, S.J. Hawkins, S.R. Jenkins, Enhancing stocks of the exploited limpet Patella candei d′Orbigny via modifications in coastal engineering, Biol. Conserv. 143 (1) (2010) 203–211. [68] H.B. Moore, A comparison of the biology of Echinus esculentus in different habitats, J. Mar. Biol. Assoc. 19 (2) (1934) 869–885. [69] R.F. Noss, Indicators for monitoring biodiversity: a hierarchical approach, Conserv. Biol. 4 (4) (1990) 355–364. [70] J.M. O’Neil, R.J. Newton, E.K. Bone, L.B. Birney, A.E. Green, B. Merrick, A. Fraioli, Using urban harbors for experiential, environmental literacy: Case studies of New York and Chesapeake Bay, Regional Studies in Marine Science 33 (2020), 100886. [71] A. Ospina-Alvarez, S. de Juan, J. Al´ os, G. Basterretxea, A. Alonso-Fern´ andez, G. Follana-Bern´ a, I.A. Catal´ an, MPA network design based on graph theory and emergent properties of larval dispersal, Mar. Ecol. Prog. Ser. 650 (2020) 309–326. [72] J. Pallant, SPSS Survival Manual: A Step by Step Guide to Data Analysis Using IBM SPSS, Routledge, 2020. [73] M. Paracuellos, J.C. Nevado, D. Moreno, A. Gim´ enez, J.J. Alesina, Conservational status and demographic characteristics of Patella ferruginea Gmelin, 1791 (Mollusca, gastropoda) on the Alboran Island (Western Mediterranean), Anim. Biodivers. Conserv. 26 (2) (2003) 29–37. [74] S. Perkol-Finkel, F. Ferrario, V. Nicotera, L. Airoldi, Conservation challenges in urban seascapes: promoting the growth of threatened species on coastal infrastructures, J. Appl. Ecol. 49 (6) (2012) 1457–1466. [75] S.L. Pimm, G.J. Russell, J.L. Gittleman, T.M. Brooks, The future of biodiversity, Science 269 (5222) (1995) 347–350. [76] F. Piniella, J. Walliser, Maritime safety in the strait of gibraltar: taxonomy and evolution of emergencies rate in 2000-2004 period, J. Marit. Res. 10 (1) (2013) 25–30. [77] M.A. Ramos, Implementing the habitats directive for mollusc species in Spain, J. Conchol. Spec. Publ. 2 (1998) 125–132. [78] G.A. Rivera-Ingraham, F. Espinosa, J.C. García-G´ omez, Environmentally mediated sex change in the endangered limpet Patella ferruginea (Gastropoda: Patellidae), J. Mollusca Stud. 77 (3) (2011) 226–231. [79] G.A. Rivera-Ingraham, G. Malanga, S. Puntarulo, A.F. P´ erez, A. Ruiz-Tabares, M. Maestre, J.C. García-G´ omez, Antioxidant defenses and trace metal bioaccumulation capacity of Cymbula nigra (Gastropoda: Patellidae), Water, Air, Soil Pollut. 224 (3) (2013) 1–13. [80] G.A. Rivera–Ingraham, F. Espinosa, J.C. García–G´ omez, Present status of the endangered limpet Cymbula nigra (Gastropoda, Patellidae) in Ceuta: how do substrate heterogeneity and area accessibility affect population structure? Anim. Biodivers. Conserv. 34 (2) (2011) 319–330. [81] G.A. Rivera–Ingraham, F. Espinosa, J.C. García–G´ omez, Present status of the endangered limpet Cymbula nigra (Gastropoda, Patellidae) in Ceuta: how do substrate heterogeneity and area accessibility affect population structure? Anim. Biodivers. Conserv. 34 (2) (2011) 319–330. [82] J.M. ROBERGE, P.E.R. Angelstam, Usefulness of the umbrella species concept as a conservation tool, Conserv. Biol. 18 (1) (2004) 76–85. [83] A. Ruiz-Tabares, I. Gordillo, J.R. Corzo, J.C. García-G´ omez, Macrofitobentos mediolitoral y delimitaci´ on de ´ areas sensibles a la contaminaci´ on marina en el litoral ceutí (estrecho de Gibraltar), Bol. Inst. Esp. De. Oceanogr. 19 (1–4) (2011) 93–103. [84] S´ anchez-Badorrey E. & García Anguita F.J. (2015). Informe final: Bases científicas para la implantaci´ on de la Directiva Marco del Agua en el litoral ceutí. Institudo de Estudios Ceutíes (unpublished report). [85] E. S´ anchez-Badorrey, J.A. García-García, R. Ortego-Jurado, F.J. García Anguita, Variabilidad clim´ atica, renovaci´ on y calidad de las aguas del puerto de Ceuta y su entorno, Instituto de Estudios Ceutíes,, 2021, pp. 115–118. ISBN: 978-84-16595- 30-3. [86] D. Sanna, P. Cossu, G.L. Dedola, F. Scarpa, F. Maltagliati, A. Castelli, P. Franzoi, T. Lai, B. Cristo, M. Curini-Galletti, P. Francalacci, M. Casu, Surviving at the edge of a fragmented range: patterns of genetic diversity in isolated populations of the endangered giant Mediterranean limpet (Patella ferruginea), Mar. Biol. 164 (3) (2017) 41. [87] J. Sempere-Valverde, E. Ostal´ e-Valriberas, M. Maestre, R.G. Aranda, H. Bazairi, F. Espinosa, Impacts of the non-indigenous seaweed Rugulopteryx okamurae on a Mediterranean coralligenous community (Strait of Gibraltar): The role of long-term monitoring, Ecol. Indic. 121 (2021), 107135. [88] A. Shabtay, M.E. Portman, Y. Carmel, Contributions of marine infrastructures to marine planning and protected area networking, Aquat. Conserv.: Mar. Freshw. Ecosyst. 28 (4) (2018) 830–839. [89] A.J. Southward, New observations on barnacles (Crustacea: Cirripedia) of the Azores region, Arquipelago. Life Mar. Sci. 16 (1998) 11–27. [90] M.L. Susini, L. Mangialajo, T. Thibaut, A. Meinesz, Development of a transplantation technique of Cystoseira amentacea var. stricta and Cystoseira compressa, in: G. Relini, J. Ryland (Eds.), Biodiversity in Enclosed Seas and Artificial Marine Habitats, Springer, Dordrecht, 2007, pp. 241–244. [91] S. Taljaard, J.H. Slinger, S. Arabi, S.P. Weerts, H. Vreugdenhil, The natural environment in port development: a ‘green handbrake’or an equal partner? Ocean Coast. Manag. 199 (2021), 105390. [92] A.J. Underwood. Experiments in ecology: their logical design and interpretation using analysis of variance, Cambridge University Press, Cambridge, 1997. [93] M. V´ azquez-Luis, E. ´ Alvarez, A. Barrajon, J.R. Garcia-March, A. Grau, I. E. Hendriks, S. Deudero, SOS Pinna nobilis: a mass mortality event in western Mediterranean Sea, Frontiers in Marine Science 4 (2017) 220. [94] V. Vikolainen, H. Bressers, K. Lulofs, A shift toward building with nature in the dredging and port development industries: managerial implications for projects in or near natura 2000 areas, Environ. Manag. 54 (1) (2014) 3–13. [95] N.J. de Voogd, The mariculture potential of the Indonesian reef-dwelling sponge Callyspongia (Euplacella) biru: growth, survival and bioactive compounds, Aquaculture 262 (1) (2007) 54–64. E. Ostal´ e-Valriberas et al. Table 1: Species list of the intertidal benthic community. FLORA Fucus spiralis 4 Siphonaria pectinata Dyctiota dichotoma Mytilus galloprovincialis 6 Chlorophyceae Colpomenia sinuosa Gibbula sp. Ulva clathrata Padina pavonica Echinolittorina punctata Ulva rigida Melarhaphe neritoides Chaetomorpha gracilis Ochrophyta Dendropoma cristatum 1,2,4 Codium adhaerens Ralfsia verrucosa Pomatoceros sp. Ocenebra edwardsii Rhodophyceae FUNGI Lepidochitona sp. Asparagopsis armata 5 Acanthochitona fascicularis Ellisolandia elongata Ascomycota Leiosolenus aristatus Jania rubens Verrucaria maura Lithophyllum byssoides 1,2,4 Arthropoda Lithophyllum sp. BACTERIA Pollicipes pollicipes 6 Mesophyllum lichenoides Chthamalus sp. Mesophyllum sp. Cyanophyceae Perforatus perforates Caulacanthus ustulatus Rivularia sp. Hildenbrandia rubra FAUNA Cnidaria Gelidium sp. Actinia equina 4 Valonia utricularis Mollusca Anemonia sulcata Osmundea pinnatifida Patella ferruginea 1,2,3,4 Astroides calycularis 1,2,4,5 Gymnogongrus crenulatus 2 Cymbula safiana 1,2 Patella rustica Equinodermata Phaeophyceae Patella caerulea Paracentrotus lividus 1 1: Annex I (flora) y II (fauna) Berne Convention; 2: Annex II Barcelona Convention; 3: Annex IV Directive 92/43; 4: Bioindica tors species; 5: Invasive or non-indigenous species; 6: Regulated harvesting species.
100 Table 2: Species list of the subtidal benthic community. FLORA Phaeophyceae Sabella sp.* Myriapora truncata Mollusca Filamentous seaweed * Cladostephus spongiosus Sabella pavonina Schizobrachiella sanguinea Bolma rugosa Biofilm* Colpomenia sp. Arthropoda Porifera Charonia lampas 1,2 Chlorophyceae Cystoseira sp.2,4 Perforatus perforatus Acanthella acuta Cratena peregrina Bryopsis plumosa Dictyota sp. Maja squinado 6,7 Cliona sp. Cymbula safiana 1,2 Caulerpa cylindracea 5 Dictyota fasciola Pollicipes pollicipes Crambe / Spirastrella sp. Dendropoma lebeche 1,2 Codium bursa Fucus spiralis 4 Scyllarides arctus Dendroxea lenis Felimare sp. Flabellia petiolata Halopteris filicina 4 Cnidaria Dysidea avara Flabellina sp. Palmophyllum crassum Halopteris scoparia Actinia equina 4 Haliclona mucosa Haliotis sp. Ulva sp. Halichrysis depressa Aglaophenia sp. Hemimycale columella Hexaplex trunculus Valonia utricularis Padina pavonica Exaiptasia diaphana Ircinia sp. Mytilus galloprovincialis Rhodophyceae Peyssonnelia rosa-marina Aiptasia mutabilis Leucosolenia sp. Pinna rudis 1,2 Apoglossum sp. Peyssonnelia rubra Alcyonium acaule Oscarella lobularis Pinna nobilis Asparagopsis armata 5 Phyllariopsis brevipes 4 Alcyonium coralloides Peraplysilla spinifera Echinodermata Asparagopsis taxiformis 5 Sargassum sp. Alicia mirabilis Petrosia sp. Arbacia lixula. Ellisolandia elongata Sporochnus sp. Astroides calycularis 1,2,4 Sarcotragus sp. Centrostephanus longispinus 1,2,3 Gelidium corneum 4 Zonaria tournefortii Caryophyllia inornata Spongia agaricina Holothuria tubulosa Gelidium pusillum FAUNA Clavularia sp. Terpios gelatinosus Holothuria orguinensis Gelidium sp. Tunicata Corynactis viridis Tethya sp. Holothuria forskali Gymnogongrus crenulatus 2 Halocynthia papillosa 4 Eunicella singularis Tunicata Holothuria sanctori Jania rubens Polycitor adriaticus 4 Eunicella verrucosa Aplidium conicum Paracentrotus lividus Lithophyllum incrustans Polysincraton sp. Hoplangia durotrix Aplidium elegans Ophioderma longicauda Mesophyllum expansum 4 Pseudodistoma sp. Calliactis parasitica Botrylloides leachii Ophiocomina nigra Mesophyllum lichenoides Stolonica socialis Paramuricea clavata 4 Clavelina dellavallei Osmundea pinnatifida 4 Synoicum blochmanni Bryozoa Pycnoclavella nana Plocamium cartilagineum Annelida Adeonella calveti Clavelina lepadiformis Sphaerococcus coronopifolius Filograna implexa Caberea boryi Diplosoma spongiforme 1: Annex I (flora) and II (fauna) Berne Convention; 2: Annex II and III Barcelona Convention; 3: Annex IV Directive 92/43; 4: Bioindicators species; 5: Invasive or non-indigenous species; 6: Annex III (special measures for its management) Berna Convention 7: Annex III (regulated harvesting species) Barcelona Convention; *: with an asterisk, the categories in which the was not possible to reach an identification at the species level with the photographic methodology.
101 Table 2: Species list of the subtidal benthic community. FLORA Phaeophyceae Sabella sp.* Myriapora truncata Mollusca Filamentous seaweed * Cladostephus spongiosus Sabella pavonina Schizobrachiella sanguinea Bolma rugosa Biofilm* Colpomenia sp. Arthropoda Porifera Charonia lampas 1,2 Chlorophyceae Cystoseira sp.2,4 Perforatus perforatus Acanthella acuta Cratena peregrina Bryopsis plumosa Dictyota sp. Maja squinado 6,7 Cliona sp. Cymbula safiana 1,2 Caulerpa cylindracea 5 Dictyota fasciola Pollicipes pollicipes Crambe / Spirastrella sp. Dendropoma lebeche 1,2 Codium bursa Fucus spiralis 4 Scyllarides arctus Dendroxea lenis Felimare sp. Flabellia petiolata Halopteris filicina 4 Cnidaria Dysidea avara Flabellina sp. Palmophyllum crassum Halopteris scoparia Actinia equina 4 Haliclona mucosa Haliotis sp. Ulva sp. Halichrysis depressa Aglaophenia sp. Hemimycale columella Hexaplex trunculus Valonia utricularis Padina pavonica Exaiptasia diaphana Ircinia sp. Mytilus galloprovincialis Rhodophyceae Peyssonnelia rosa-marina Aiptasia mutabilis Leucosolenia sp. Pinna rudis 1,2 Apoglossum sp. Peyssonnelia rubra Alcyonium acaule Oscarella lobularis Pinna nobilis Asparagopsis armata 5 Phyllariopsis brevipes 4 Alcyonium coralloides Peraplysilla spinifera Echinodermata Asparagopsis taxiformis 5 Sargassum sp. Alicia mirabilis Petrosia sp. Arbacia lixula. Ellisolandia elongata Sporochnus sp. Astroides calycularis 1,2,4 Sarcotragus sp. Centrostephanus longispinus 1,2,3 Gelidium corneum 4 Zonaria tournefortii Caryophyllia inornata Spongia agaricina Holothuria tubulosa Gelidium pusillum FAUNA Clavularia sp. Terpios gelatinosus Holothuria orguinensis Gelidium sp. Tunicata Corynactis viridis Tethya sp. Holothuria forskali Gymnogongrus crenulatus 2 Halocynthia papillosa 4 Eunicella singularis Tunicata Holothuria sanctori Jania rubens Polycitor adriaticus 4 Eunicella verrucosa Aplidium conicum Paracentrotus lividus Lithophyllum incrustans Polysincraton sp. Hoplangia durotrix Aplidium elegans Ophioderma longicauda Mesophyllum expansum 4 Pseudodistoma sp. Calliactis parasitica Botrylloides leachii Ophiocomina nigra Mesophyllum lichenoides Stolonica socialis Paramuricea clavata 4 Clavelina dellavallei Osmundea pinnatifida 4 Synoicum blochmanni Bryozoa Pycnoclavella nana Plocamium cartilagineum Annelida Adeonella calveti Clavelina lepadiformis Sphaerococcus coronopifolius Filograna implexa Caberea boryi Diplosoma spongiforme 1: Annex I (flora) and II (fauna) Berne Convention; 2: Annex II and III Barcelona Convention; 3: Annex IV Directive 92/43; 4: Bioindicators species; 5: Invasive or non-indigenous species; 6: Annex III (special measures for its management) Berna Convention 7: Annex III (regulated harvesting species) Barcelona Convention; *: with an asterisk, the categories in which the was not possible to reach an identification at the species level with the photographic methodology. VII. PUBLICACIÓN 4. ESTUDIO DE LA DINÁMICA POBLACIONAL Y EFECTOS ABIÓTICOS QUE LO MODELAN LA ESTRUCTURA POBLACIONAL DEL MOLUSCO GASTERÓPODO P. FERRUGINEA ASENTADO EN EL LITORAL DE CEUTA.
When the population of an endangered marine mollusc (Patella ferruginea) increases almost three-fold in ten years. Reality or fiction? E. Ostale ´-Valriberas*,A ´ . Sabino-Lorenzo, A. Ali-Ahmed, A. Pavo ´n-Paneque, J. Sempere-Valverde, F. Espinosa and J. C. Garcı ´a-Go ´mez Laboratorio de Biologı ´a Marina de la Universidad de Sevilla (LBMUS)/ A ´rea de Investigacio ´n I+D+i del Acuario de Sevilla/ Estacio ´n de Biologı ´a Marina del Estrecho (Ceuta), Universidad de Sevilla, Seville, Spain The critically endangered species Patella ferruginea (Gastropoda, Patellidae), endemic to the western Mediterranean, has breeding populations in both natural and artificial habitats, the latter of which are generally linked to port infrastructures. Over the past decade, the temporal change of this species’ population has been monitored (structure and density) using exhaustive censuses along Ceuta’s coast (Strait of Gibraltar), one of the few stronghold populations within the entire Mediterranean basin. This study focuses on the population dynamics of P. ferruginea in Ceuta and the environmental factors that affect the structure of this population, such as wave exposure, coastline heterogeneity, substratum roughness, substratum lithology, and chlorophyll-a concentration. Different potential negative interactions were also considered: angling, shell fishing, bathing in the intertidal, bathing near the intertidal, recreational boating and temporary migrant campsites nearby. The results have shown in the period 2011-2021, the estimated size of P. ferruginea population has increased by 200 %, from 55,902 to 168,463 individuals (of which 131,776 are adults). The subpopulation with the greatest increase in these years was the one settled on dolomitic rip-raps inside the Ceuta’s harbor, with an increase of 1,288%. The results of the present study indicate that Ceuta hosts the main population of this endangered species through its distributional range (Western Mediterranean), being a source population on the Southern Iberian Peninsula that its preservation must be prioritized. Statistical modelling has shown that the adult density of P. ferruginea is positively influenced by coastal heterogeneity, habitat area and substratum roughness, but negatively by vertical inclination, concentration of chlorophyll-a, and anthropogenic impact. These results also support the concept of ¨Artificial Marine Micro-Reserves¨ as a new area-based conservation measure according with the IUCN guidelines, as these will contribute to setting up a network of these source populations that promote genetic flow among populations, with eventual recolonization throughout its original distribution. KEYWORDS Patella ferruginea, patellogastropoda, conservation, extinction risk, population structure, artificial marine micro-reserves, artificial substratum, source population Frontiers in Marine Science frontiersin.org01 OPEN ACCESS EDITED BY Alan Hodgson, Rhodes University, South Africa REVIEWED BY Francesco Tiralongo, University of Catania, Italy Mariachiara Chiantore, University of Genoa, Italy *CORRESPONDENCE E. Ostale ´-Valriberas [email protected] RECEIVED 19 December 2022 ACCEPTED 08 June 2023 PUBLISHED 12 July 2023 CITATION Ostale ´-Valriberas E, Sabino-Lorenzo A ´, Ali-Ahmed A, Pavo ´n-Paneque A, Sempere-Valverde J, Espinosa F and Garcı ´a-Go ´mez JC (2023) When the population of an endangered marine mollusc (Patella ferruginea) increases almost three-fold in ten years. Reality or fiction? Front. Mar. Sci. 10:1127630. doi: 10.3389/fmars.2023.1127630 COPYRIGHT © 2023 Ostale ´-Valriberas, Sabino-Lorenzo, Ali-Ahmed, Pavo ´n-Paneque, Sempere-Valverde, Espinosa and Garcı ´a-Go ´mez. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. TYPE Original Research PUBLISHED 12 July 2023 DOI 10.3389/fmars.2023.1127630
103 When the population of an endangered marine mollusc (Patella ferruginea) increases almost three-fold in ten years. Reality or fiction? E. Ostale ´-Valriberas*,A ´ . Sabino-Lorenzo, A. Ali-Ahmed, A. Pavo ´n-Paneque, J. Sempere-Valverde, F. Espinosa and J. C. Garcı ´a-Go ´mez Laboratorio de Biologı ´a Marina de la Universidad de Sevilla (LBMUS)/ A ´rea de Investigacio ´n I+D+i del Acuario de Sevilla/ Estacio ´n de Biologı ´a Marina del Estrecho (Ceuta), Universidad de Sevilla, Seville, Spain The critically endangered species Patella ferruginea (Gastropoda, Patellidae), endemic to the western Mediterranean, has breeding populations in both natural and artificial habitats, the latter of which are generally linked to port infrastructures. Over the past decade, the temporal change of this species’ population has been monitored (structure and density) using exhaustive censuses along Ceuta’s coast (Strait of Gibraltar), one of the few stronghold populations within the entire Mediterranean basin. This study focuses on the population dynamics of P. ferruginea in Ceuta and the environmental factors that affect the structure of this population, such as wave exposure, coastline heterogeneity, substratum roughness, substratum lithology, and chlorophyll-a concentration. Different potential negative interactions were also considered: angling, shell fishing, bathing in the intertidal, bathing near the intertidal, recreational boating and temporary migrant campsites nearby. The results have shown in the period 2011-2021, the estimated size of P. ferruginea population has increased by 200 %, from 55,902 to 168,463 individuals (of which 131,776 are adults). The subpopulation with the greatest increase in these years was the one settled on dolomitic rip-raps inside the Ceuta’s harbor, with an increase of 1,288%. The results of the present study indicate that Ceuta hosts the main population of this endangered species through its distributional range (Western Mediterranean), being a source population on the Southern Iberian Peninsula that its preservation must be prioritized. Statistical modelling has shown that the adult density of P. ferruginea is positively influenced by coastal heterogeneity, habitat area and substratum roughness, but negatively by vertical inclination, concentration of chlorophyll-a, and anthropogenic impact. These results also support the concept of ¨Artificial Marine Micro-Reserves¨ as a new area-based conservation measure according with the IUCN guidelines, as these will contribute to setting up a network of these source populations that promote genetic flow among populations, with eventual recolonization throughout its original distribution. KEYWORDS Patella ferruginea, patellogastropoda, conservation, extinction risk, population structure, artificial marine micro-reserves, artificial substratum, source population Frontiers in Marine Science frontiersin.org01 OPEN ACCESS EDITED BY Alan Hodgson, Rhodes University, South Africa REVIEWED BY Francesco Tiralongo, University of Catania, Italy Mariachiara Chiantore, University of Genoa, Italy *CORRESPONDENCE E. Ostale ´-Valriberas [email protected] RECEIVED 19 December 2022 ACCEPTED 08 June 2023 PUBLISHED 12 July 2023 CITATION Ostale ´-Valriberas E, Sabino-Lorenzo A ´, Ali-Ahmed A, Pavo ´n-Paneque A, Sempere-Valverde J, Espinosa F and Garcı ´a-Go ´mez JC (2023) When the population of an endangered marine mollusc (Patella ferruginea) increases almost three-fold in ten years. Reality or fiction? Front. Mar. Sci. 10:1127630. doi: 10.3389/fmars.2023.1127630 COPYRIGHT © 2023 Ostale ´-Valriberas, Sabino-Lorenzo, Ali-Ahmed, Pavo ´n-Paneque, Sempere-Valverde, Espinosa and Garcı ´a-Go ´mez. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. TYPE Original Research PUBLISHED 12 July 2023 DOI 10.3389/fmars.2023.1127630
104 1 Introduction Coastal areas host half of the world’s cities and more than half of the world’s population, with population density near the coast three times higher than the global average (Creel, 2003;Small and Nicholls, 2003;Airoldi and Beck, 2007). Shoreline urbanization combined with the increase of tourist, recreational and commercial activities, has resulted in the introduction and proliferation of artificial structures in marine coastal habitats worldwide (Bulleri and Chapman, 2010;Firth et al., 2016). The human impact associated with these structures has been reported to affect biological processes on all spatial and temporal scales (Airoldi et al., 2005). Among them, fragmentation of natural habitats by urbanization processes can cause a reduction in population size and connectivity of species, and thus increase their risk of extinction in the face of certain permanent disturbances (Aguilera et al., 2020; Chase et al., 2020). Limpets are considered keystone species in rocky coastal ecosystems as they maintain the composition and structure of the biological community and, when they disappear from their habitats, cause a cascading effect on them (Raffaelli and Hawkins, 1996). Therefore, limpets may be the most important group of grazers in temperate rocky intertidal zones, because their feeding activity limits the growth of macroalgae and controls barnacle numbers (Branch, 1981). Among limpets, the larger species are frequently the most ecologically relevant, being defined as ‘giant limpets’(shell length greater than 100 mm). With this classification a total of 14 species in the world can be found, three of them catalogued as threatened (Espinosa and Rivera-Ingraham, 2017). Patella ferruginea Gmelin, 1791 (Gastropoda: Patellidae) belongs to this classification, as it achieves a maximum recorded shell length of 115 mm (Supplementary Figure 1-S). It is endemic to the Western Mediterranean Sea and it is considered the most endangered marine invertebrate (Ramos, 1998), together with Pinna nobilis, within the European coastline (Vazquez-Luis et al., 2017;Lattos et al., 2021). Like other limpet species, P. ferruginea is a broadcast spawner with external fertilization so that the urban development of coastal areas has dramatically fragmented its habitat (Airoldi et al., 2005; Firth et al., 2016). Moreover, the conspicuous star‐shaped shell and large sizes that P. ferruginea can reach has made this species the target of human collection since the Quaternary (Espinosa, 2006; Espinosa et al., 2009;Rivera-Ingraham et al., 2011a;Guallart et al., 2013a). On account of these anthropogenic impacts, its distribution range has progressively been contracted, and P. ferruginea has nearly disappeared from European continental coasts, except for the small and fragmented populations present in Andalusia Southern Spain, Liguria (Italy) and Southern France (Cottalorda et al., 2004;Espinosa et al., 2014b;Luque et al., 2018;Ferranti et al., 2019;CMAOT, 2020). The remaining most notable populations are found in scattered North African gated communities: Ceuta, Melilla, Chafarinas Islands, Habibas Islands, and the island of Zembra (Espinosa et al., 2014b;Luque et al., 2018). In this regard, it has recently been identified that possibly the population located in Ceuta (Strait of Gibraltar, North Africa) plays the role of source population in the area, maintaining nearby sink populations in the south of the Iberian Peninsula (Espinosa et al., 2018) according to the “source-sink population model”(see Pulliam, 1988; Pulliam, 1996). This study focuses on the population dynamics of P. ferruginea in Ceuta and the environmental factors that shape the population size structure. Consequently, the objectives of the present study are i) to determine the current status of this P. ferruginea population, ii) track the any change in the population in the last 10 years, iii) to confirm the result of the ¨population viability analysis¨ (PVA) prediction method performed by Espinosa et al. (2018) of the P. ferruginea population in Ceuta and iv) explore the environmental factors affecting the populations of P. ferruginea. 2 Materials and methods 2.1 Study area The Strait of Gibraltar is a very important geological region, bordering by the Mediterranean, Lusitanian and Mauritanian biogeographic provinces, so it is a zone in which marine flora and fauna from the Mediterranean and Atlantic overlap (Coll et al., 2010). Likewise, it is one of the world’s busiest hubs for maritime traffic, as it is a place where many commercial routes converge and where important harbors are present (Algeciras, Gibraltar and Tangier Med), which makes it an area with high risk of disturbances, impacts and environmental disasters (Piniella and Walliser, 2013:Nachite et al., 2020). The harbor of Ceuta, a Spanish city in North Africa, has an unusual structure, because it is located between two bays (North and South) connected to both by the Royal Moat (Figure 1A). This defensive construction, built by the Portuguese during the 16 th century, increases water movement and exchange within the structure (shorting the residence time of the water mass), when compared to other conventional harbors, maintaining moderate oxygen levels in the water and sediment (Guerra-Garcı a et al., 2004a;Guerra-Garcia and Garcı a-Gomez, 2005;Sanchez-Badorrey et al., 2021). 2.2 Sampling methods 2.2.1 Patella ferruginea census A census on P. ferruginea population in Ceuta was carried out during 2019 and 2020 (14 months). To estimate the status and evolution of the P. ferruginea population, the sampling methodology repeated the one carried out by Rivera-Ingraham et al. (2011b) in 2010 in the same area. The complete coastline was divided into 18 sectors; accounting for the type of substratum (natural, dolomitic rip-rap and concrete cubes) and its geographic orientation (see sectors at Figure 1B). To know the ¨population size structure¨ of P. ferruginea’s population, the 20% of the entire rocky midlittoral, where the species occurs, was sampled at each sector. Ten meter linear transects were proportionally distributed within each sector separated by 40 m. The shell length of the specimens found Ostale ´-Valriberas et al. 10.3389/fmars.2023.1127630 Frontiers in Marine Science frontiersin.org02 within the intertidal at each transect were measured to the nearest millimetre using a calliper (Guerra-Garcı a et al., 2004b;Espinosa, 2009b;Rivera-Ingraham et al., 2011b). Finally, 4,560 m of rocky midlittoral coastline were sampled out of a total of 23,617 m of rocky coastline present in the city of Ceuta (Table 1). To estimate the total number of individuals in each sector and thus of the population, the results were extrapolated from the total length (m -1 ) of P. ferruginea habitat in the sector. In the present study, recruits were defined as individuals smaller than 30 mm and adults greater than or equal to 30 mm (Espinosa et al., 2006) and the “class size”was categorize for every 10 mm of shell length (e.g., class size 3 pertains to individuals from 21mm to 30mm). To track any change of the population structure in the last 10 years, it has been considered that in the preceding work performed by Rivera-Ingraham et al. (2011b). In the said study, the total length of rocky shoreline where the species could potentially be present was calculated by using 1:9,000 scale maps obtained using Google Earth © . Therefore, the estimations from the previous census have been recalculated, according to the used estimate of coastline length in the present work (10 m resolution), in order to make both estimations comparable and to be able to evaluate the percent increase or decrease of the population in each sector. The percentage change in the number of individuals (%) between both studies was calculated using the equation: Percentage change (%)=(estimation 2020 estimation 2010 )x 100) −100 2.2.2 Environmental factors Once the sampling of P. ferruginea was completed, the environmental factors were studied. All environmental factors were studied in the same transect that were randomly selected in each sector (three transects per sector, 54 transects in total) in July of 2022. Substratum lithology of each sector was characterized by collecting three rock chips from each sector, which were powdered in the laboratory using a ball mill with stainless steel balls as grinding media. Each rock chip was obtained by hammer and chisel. The elemental composition and calcination percentage of each sample was quantified by X- ray fluorescence (XRF) using an AXIOS spectrometer. Mineralogic absorption spectra were detected by X- ray diffraction (XRD) using a powder diffractometer (Bruker D8 Advance) equipped with a high temperature chamber (Anton Paar XRK 900) and a fast response/high sensitivity detector (Bruker Vantec 1) with radial Soller slits (full methodology can be accessed in Valverde et al., 2015). Afterwards, XRF and XRD data were interpreted to quantify the crystallinity and lithology composition of each sample using DRIFAC.EVA.4.1 software. To assess the influence of microalgal abundance on P. ferruginea demographic, the chlorophyll-a concentration on the substratum surface was estimated in the same rock samples used to study lithology. The resulting slurry was treated with 20 ml of 100% ethanol to extract the pigments. Then, samples were frozen and maintained in darkness until analysis (minimum of 48 h) according with the protocol used by Kido and Murray (2003). Samples were filtered through a Whatman GF/C filter and measurements of absorbance were carried out with a spectrophotometer (Pharmacia Biotech Novaspec II). Given the large extension of the study area, some environmental factors like chlorophyll a were collected once, being a snapshot of the environment. Moreover, for the Chl-a we took the 54 samples in two consecutive days of July 2020 using a zodiac and sampling in FIGURE 1 (A) Location of Ceuta, inside the black circle can be found the royal Moat; (B) Sectorization of the coastline to estimate the population size distribution of P. ferruginea. Source: Google Earth. Ostale ´-Valriberas et al. 10.3389/fmars.2023.1127630 Frontiers in Marine Science frontiersin.org03
105 1 Introduction Coastal areas host half of the world’s cities and more than half of the world’s population, with population density near the coast three times higher than the global average (Creel, 2003;Small and Nicholls, 2003;Airoldi and Beck, 2007). Shoreline urbanization combined with the increase of tourist, recreational and commercial activities, has resulted in the introduction and proliferation of artificial structures in marine coastal habitats worldwide (Bulleri and Chapman, 2010;Firth et al., 2016). The human impact associated with these structures has been reported to affect biological processes on all spatial and temporal scales (Airoldi et al., 2005). Among them, fragmentation of natural habitats by urbanization processes can cause a reduction in population size and connectivity of species, and thus increase their risk of extinction in the face of certain permanent disturbances (Aguilera et al., 2020; Chase et al., 2020). Limpets are considered keystone species in rocky coastal ecosystems as they maintain the composition and structure of the biological community and, when they disappear from their habitats, cause a cascading effect on them (Raffaelli and Hawkins, 1996). Therefore, limpets may be the most important group of grazers in temperate rocky intertidal zones, because their feeding activity limits the growth of macroalgae and controls barnacle numbers (Branch, 1981). Among limpets, the larger species are frequently the most ecologically relevant, being defined as ‘giant limpets’(shell length greater than 100 mm). With this classification a total of 14 species in the world can be found, three of them catalogued as threatened (Espinosa and Rivera-Ingraham, 2017). Patella ferruginea Gmelin, 1791 (Gastropoda: Patellidae) belongs to this classification, as it achieves a maximum recorded shell length of 115 mm (Supplementary Figure 1-S). It is endemic to the Western Mediterranean Sea and it is considered the most endangered marine invertebrate (Ramos, 1998), together with Pinna nobilis, within the European coastline (Vazquez-Luis et al., 2017;Lattos et al., 2021). Like other limpet species, P. ferruginea is a broadcast spawner with external fertilization so that the urban development of coastal areas has dramatically fragmented its habitat (Airoldi et al., 2005; Firth et al., 2016). Moreover, the conspicuous star‐shaped shell and large sizes that P. ferruginea can reach has made this species the target of human collection since the Quaternary (Espinosa, 2006; Espinosa et al., 2009;Rivera-Ingraham et al., 2011a;Guallart et al., 2013a). On account of these anthropogenic impacts, its distribution range has progressively been contracted, and P. ferruginea has nearly disappeared from European continental coasts, except for the small and fragmented populations present in Andalusia Southern Spain, Liguria (Italy) and Southern France (Cottalorda et al., 2004;Espinosa et al., 2014b;Luque et al., 2018;Ferranti et al., 2019;CMAOT, 2020). The remaining most notable populations are found in scattered North African gated communities: Ceuta, Melilla, Chafarinas Islands, Habibas Islands, and the island of Zembra (Espinosa et al., 2014b;Luque et al., 2018). In this regard, it has recently been identified that possibly the population located in Ceuta (Strait of Gibraltar, North Africa) plays the role of source population in the area, maintaining nearby sink populations in the south of the Iberian Peninsula (Espinosa et al., 2018) according to the “source-sink population model”(see Pulliam, 1988; Pulliam, 1996). This study focuses on the population dynamics of P. ferruginea in Ceuta and the environmental factors that shape the population size structure. Consequently, the objectives of the present study are i) to determine the current status of this P. ferruginea population, ii) track the any change in the population in the last 10 years, iii) to confirm the result of the ¨population viability analysis¨ (PVA) prediction method performed by Espinosa et al. (2018) of the P. ferruginea population in Ceuta and iv) explore the environmental factors affecting the populations of P. ferruginea. 2 Materials and methods 2.1 Study area The Strait of Gibraltar is a very important geological region, bordering by the Mediterranean, Lusitanian and Mauritanian biogeographic provinces, so it is a zone in which marine flora and fauna from the Mediterranean and Atlantic overlap (Coll et al., 2010). Likewise, it is one of the world’s busiest hubs for maritime traffic, as it is a place where many commercial routes converge and where important harbors are present (Algeciras, Gibraltar and Tangier Med), which makes it an area with high risk of disturbances, impacts and environmental disasters (Piniella and Walliser, 2013:Nachite et al., 2020). The harbor of Ceuta, a Spanish city in North Africa, has an unusual structure, because it is located between two bays (North and South) connected to both by the Royal Moat (Figure 1A). This defensive construction, built by the Portuguese during the 16 th century, increases water movement and exchange within the structure (shorting the residence time of the water mass), when compared to other conventional harbors, maintaining moderate oxygen levels in the water and sediment (Guerra-Garcı a et al., 2004a;Guerra-Garcia and Garcı a-Gomez, 2005;Sanchez-Badorrey et al., 2021). 2.2 Sampling methods 2.2.1 Patella ferruginea census A census on P. ferruginea population in Ceuta was carried out during 2019 and 2020 (14 months). To estimate the status and evolution of the P. ferruginea population, the sampling methodology repeated the one carried out by Rivera-Ingraham et al. (2011b) in 2010 in the same area. The complete coastline was divided into 18 sectors; accounting for the type of substratum (natural, dolomitic rip-rap and concrete cubes) and its geographic orientation (see sectors at Figure 1B). To know the ¨population size structure¨ of P. ferruginea’s population, the 20% of the entire rocky midlittoral, where the species occurs, was sampled at each sector. Ten meter linear transects were proportionally distributed within each sector separated by 40 m. The shell length of the specimens found Ostale ´-Valriberas et al. 10.3389/fmars.2023.1127630 Frontiers in Marine Science frontiersin.org02 within the intertidal at each transect were measured to the nearest millimetre using a calliper (Guerra-Garcı a et al., 2004b;Espinosa, 2009b;Rivera-Ingraham et al., 2011b). Finally, 4,560 m of rocky midlittoral coastline were sampled out of a total of 23,617 m of rocky coastline present in the city of Ceuta (Table 1). To estimate the total number of individuals in each sector and thus of the population, the results were extrapolated from the total length (m -1 ) of P. ferruginea habitat in the sector. In the present study, recruits were defined as individuals smaller than 30 mm and adults greater than or equal to 30 mm (Espinosa et al., 2006) and the “class size”was categorize for every 10 mm of shell length (e.g., class size 3 pertains to individuals from 21mm to 30mm). To track any change of the population structure in the last 10 years, it has been considered that in the preceding work performed by Rivera-Ingraham et al. (2011b). In the said study, the total length of rocky shoreline where the species could potentially be present was calculated by using 1:9,000 scale maps obtained using Google Earth © . Therefore, the estimations from the previous census have been recalculated, according to the used estimate of coastline length in the present work (10 m resolution), in order to make both estimations comparable and to be able to evaluate the percent increase or decrease of the population in each sector. The percentage change in the number of individuals (%) between both studies was calculated using the equation: Percentage change (%)=(estimation 2020 estimation 2010 )x 100) −100 2.2.2 Environmental factors Once the sampling of P. ferruginea was completed, the environmental factors were studied. All environmental factors were studied in the same transect that were randomly selected in each sector (three transects per sector, 54 transects in total) in July of 2022. Substratum lithology of each sector was characterized by collecting three rock chips from each sector, which were powdered in the laboratory using a ball mill with stainless steel balls as grinding media. Each rock chip was obtained by hammer and chisel. The elemental composition and calcination percentage of each sample was quantified by X- ray fluorescence (XRF) using an AXIOS spectrometer. Mineralogic absorption spectra were detected by X- ray diffraction (XRD) using a powder diffractometer (Bruker D8 Advance) equipped with a high temperature chamber (Anton Paar XRK 900) and a fast response/high sensitivity detector (Bruker Vantec 1) with radial Soller slits (full methodology can be accessed in Valverde et al., 2015). Afterwards, XRF and XRD data were interpreted to quantify the crystallinity and lithology composition of each sample using DRIFAC.EVA.4.1 software. To assess the influence of microalgal abundance on P. ferruginea demographic, the chlorophyll-a concentration on the substratum surface was estimated in the same rock samples used to study lithology. The resulting slurry was treated with 20 ml of 100% ethanol to extract the pigments. Then, samples were frozen and maintained in darkness until analysis (minimum of 48 h) according with the protocol used by Kido and Murray (2003). Samples were filtered through a Whatman GF/C filter and measurements of absorbance were carried out with a spectrophotometer (Pharmacia Biotech Novaspec II). Given the large extension of the study area, some environmental factors like chlorophyll a were collected once, being a snapshot of the environment. Moreover, for the Chl-a we took the 54 samples in two consecutive days of July 2020 using a zodiac and sampling in FIGURE 1 (A) Location of Ceuta, inside the black circle can be found the royal Moat; (B) Sectorization of the coastline to estimate the population size distribution of P. ferruginea. Source: Google Earth. Ostale ´-Valriberas et al. 10.3389/fmars.2023.1127630 Frontiers in Marine Science frontiersin.org03
112 substratum (sectors: R, B, D and G) and the lowest (marked in red in Table 1-S) correspond to the artificial substratum (sectors: N, O, K and L) (see Table 1 and Figure 2). The adult density did not show any significant correlation with the variables area of habitat, wave exposure (fetch) and percentage of calcium oxide in the substratum (CaO %). The results of the environmental factors used in the GLM are shown as Supplementary Material (Table 1-S). The results of impact human activity (Supplementary Table 2-S) and rock elemental composition (elemental composition, Supplementary Table 3-S); mineralogy composition, Supplementary Table 4-S)wereshowlike Supplementary Material. 4 Discussion The results have shown that from 2011 to 2021 the population or P. ferruginea increased by about 200%. Currently, the population numbers 168,464 individuals, of which 131,776 are adults. In about a decade, the population has grown from 55,902 to 168,464 individuals. Recent studies have shown that there has been recolonization and repopulation of P. ferruginea in some localities of the Andalusia, Melilla, Alboran and Chafarinas island (Casado et al., 2017;Maestre et al., 2018;CMAOT, 2020). Therefore, Ceuta’s population could be an important contributor to the recolonization of these areas, especially when considering that nearly 80% of its individuals are adults. Nevertheless, the situation of P. ferruginea is still critical because the individuals settled in Andalucı a are the last stronghold of continental Europe, depending heavily on recruits from North African populations (CMAOT, 2020). These results show that the area of Ceuta is a ¨stronghold¨ for this endangered species and support the hypothesis that this population has the role of a ¨source population¨ of new recruits for other nearby ¨sink populations¨ in the metapopulation of the Alboran Sea supporting the hypothesis proposed by Espinosa et al., 2018. These conclusions can be supported by different oceanographic and biological studies carried out in this biogeographic area. In this sense, it is known that all P. ferruginea populations from the Alboran Sea and North Africa up to Tunisia belong to the same genetic cluster (Casu et al., 2011). Dispersal studies showed that the directionality of the surface currents of the Alboran Sea, especially those near the Strait of Gibraltar in its first loop go from south to north (therefore, the potential larval input should go from south to north and not the other way around, at least from the coast of Ceuta) (see Periañez, 2007). Likewise, dispersal studies of P. ferruginea larvae in the Alboran Sea show simulated regional trajectories for virtual larvae released from Ceuta with strong prevailing westerly wind at high and low spring tide conditions with a Pelagic Larval Duration of 14 days during January 2016 can cross and complete the first loop of the Alboran Sea (Stephen Warr unpublished data). The settlement ability of larvae of this species is reached 3-4 days after fertilization, depending on water temperature, and crawling and swimming pediveliger larvae have a phase of 7-32 days (probably up to 40 days) until metamorphosis to juvenile occurs (Ferranti et al., 2022), which would argue that the population studied in Ceuta should be classified as a “source population”according to the “source-sink population model”(see Pulliam, 1988;Pulliam, 1996). Although the sampling effort was larger than previous studies, in light of the results a review of the existing literature, reveals that the population in Ceuta is the largest within the species’natural distribution (see Table 4). The mean density of the population has increased from 2.33 ind/m in 2010 (Rivera-Ingraham et al., 2011b) to 7.39 ind/m in 2020. This is in agreement with the output of the population viability analysis (PVA) model carried out by Espinosa et al. (2018), and based on monitoring during a ten-year period. This model indicates the unlikeliness of the population in Ceuta facing extinction within the next 50 years. This confirms the effectiveness of the control and temporary monitoring programs of the population proposed in Spain’s National Conservation Strategy for P. ferruginea, established in 2008 by the Spanish Ministry of Environment (MMAMRM, 2008). The increase of Ceuta’s population could be due to two different factors. Firstly, there are some littoral zones with difficult or restricted access, such as sectors H and I, which are a natural cliffs, and sectors K, L and M, which are access-restricted areas in the commercial harbor of artificial structure type riprap (great heterogeneity, macroscale and microscale). These sectors would be therefore protected from anthropogenic impact, which has been identified as the main factor promoting the decline of the species (Ostale-Valriberas et al., 2022 and references therein). Secondly, there has been an improvement in social awareness of the conservation status of this endangered species, promoted by dissemination activities performed by NGOs and the environmental administration, and increased enforcement by local authorities. In this sense, many projects and news have been published in social media publications (Mar, 2020), giving notoriety to P. ferruginea and turning it into a flagship species. In this sense, flagship species attract funding, increase awareness, and promote the conservation of habitats, acting as umbrella species (Smith and Sutton, 2008;Home et al., 2009). An analysis of the evolution of the population of P. ferruginea over the last two decades in a biggest area distribution, the Alboran Sea, shows an increase in the number of individuals (Maestre et al., 2018;CMAOT, 2022). The control by the local authorities (environmental administration and security forces) in the application of the strict legislation that protects the species (community, national and regional regulations), in addition to the increase in the awareness of the local population through environmental education, together with the advances in research on the species give an impression of good results. Statistical modeling has shown that P. ferruginea adult density increases with coastal heterogeneity (macroscale in meters) and substratum roughness (microscale in cm), and decreases with slope, chlorophyll-a concentration and anthropogenic impact. Among the different environmental factors, the coastal heterogeneity (m) has the most impact on the adult density. A one-point increase in the macroscale value favors adult density by 10.52 while a one-point increase in the microscale value (cm) favors it only by 1.27. Therefore, coastal and substratum heterogeneity at multiple scales must be taken into consideration for designing sites for further Ostale ´-Valriberas et al. 10.3389/fmars.2023.1127630 Frontiers in Marine Science frontiersin.org10 protection (Marine protected areas or Area-based conservation measures such as Artificial marine micro-reserves), to establish critical areas for its conservation or for future translocation procedures for reinforcement and/or reintroduction, or due to destruction of the original habitat (see MMAMRM, 2008;Garcı a- Gomez et al., 2011;Garcı a-Gomez et al., 2015;IUCN-WCPA, 2019; Agung et al., 2022;Ostale-Valriberas et al., 2022). The vertical slope of the coastline negatively influences the density of P. ferruginea adults. Within vertical substrata such as cliffs or seawalls, a smaller surface (area) of settlement for planktonic larvae is available, which explains the result. A practical example of these results has been shown in the different abundances between the subpopulation settled inside the harbor (sectors L and L’). Yet still sharing the same environment, the subsector of dolomitic rip-rap (L) and the vertical concrete wall (L’) show the most different results according to the population structure (number of individuals in each size class) (see Figures 5,6). Analyzing the results obtained for the Chl-a concentration in each sector, it is observed that there are other environmental factors that more strongly affect the species. According to the results of previous studies, the accessibility and visitation of the coastal areas negatively affect limpet populations of P. ferruginea, biasing the populations structure via harvesting of the greatest sizes (mostly females) and therefore affecting the adult density (see Figure 7;Table 2-S)(Espinosa et al., 2009;Ostale- Valriberas et al., 2022). In fact, the results of the present study show that a one-point decrease in the value of accessibility increases the adult density by 0.96. 5 Conservational implications The results indicate that Ceuta is the main population of this endangered species in its entire range, being a source population on the Southern Iberian Peninsula that should be conserved as a priority. According to the Spanish National Conservation Strategy, sectors H, I, K, L and M have the highest number of adults and should therefore be categorized and managed as Critical Areas (MMAMRM, 2008; see Supplementary Figure 2-S). It could benefit many species of conservation concern also settled in the TABLE 4 Current known distribution of the P. ferruginea specie in the Western Mediterranean sea. Country Area Source Year of sampling Mean density (ind/m) Estimated total population Spain Andalucı aCMAOT, 2019 2019 0.63 ind/m*17,032** Ceuta Present study 2019-2020 7.28-5.56*ind/m 131,775** Melilla Guallart et al., 2013b 2010 2.82 ind/m*32,821** Chafarinas Guallart and Templado, 2016 2000 4.36 ind/m*42,230** AlboranCMAOT, 2019 2018 115** Morocco MPA of Al Hoceima (Cala Iris Islet) Bazairi et al., 2012 2012 1.22 ind/m 576 MPA of Al Hoceima (El Jebha) Bazairi et al., 2012 2012 3.66 ind/m Cape Three Forks Espinosa et al., 2014a 2012 from 0.36 to 0.83 ind./ m Algeria Plane Island Kallouche et al., 2020 2019 1.78 ind/m 3,993 Habiba Island Espinosa, 2009b 2008 4.8 –3.23*ind/m 50,400 Rachgoun Island Taibi et al., 2014 3-10 ind/m 2 Tunisia Zembra Zarrouk et al., 2016 2015 2.83 ind/m 2 *40,404** North-East Tunisian coast Tlig-Zouari et al., 2010 2006 0.025-4.5 ind/m 2 Italy Sinis Peninsula MPA (Sardinia) Coppa et al., 2012 2009 0.02 ind/m 196 Gulf of Olbia (Sardinia) Cristo et al., 2007 2007 0.023 ind/m 69 Maddalena Archipelago (Sardinia) Cossu et al., 2006 2005 0.028 ind/m 736 Mal di Ventre Island & Cape San Marco (central-western Sardinia) Marra et al., 2016 2013-2014 0.009 & 0.004 ind/m Lingurian coasts Ferranti et al., 2019 2017-2018 0.005 ind/m*32 France Port Cros Cottalorda et al., 2004 <0.01 ind/m 2 Cap Corse/Bastia harbour (Corsica) Vela and Leoni, 2007 0.2 ind/m 2 *, Adult mean density (ind/m); **, Estimated adult population. Ostale ´-Valriberas et al. 10.3389/fmars.2023.1127630 Frontiers in Marine Science frontiersin.org11
113 protection (Marine protected areas or Area-based conservation measures such as Artificial marine micro-reserves), to establish critical areas for its conservation or for future translocation procedures for reinforcement and/or reintroduction, or due to destruction of the original habitat (see MMAMRM, 2008;Garcı a- Gomez et al., 2011;Garcı a-Gomez et al., 2015;IUCN-WCPA, 2019; Agung et al., 2022;Ostale-Valriberas et al., 2022). The vertical slope of the coastline negatively influences the density of P. ferruginea adults. Within vertical substrata such as cliffs or seawalls, a smaller surface (area) of settlement for planktonic larvae is available, which explains the result. A practical example of these results has been shown in the different abundances between the subpopulation settled inside the harbor (sectors L and L’). Yet still sharing the same environment, the subsector of dolomitic rip-rap (L) and the vertical concrete wall (L’) show the most different results according to the population structure (number of individuals in each size class) (see Figures 5,6). Analyzing the results obtained for the Chl-a concentration in each sector, it is observed that there are other environmental factors that more strongly affect the species. According to the results of previous studies, the accessibility and visitation of the coastal areas negatively affect limpet populations of P. ferruginea, biasing the populations structure via harvesting of the greatest sizes (mostly females) and therefore affecting the adult density (see Figure 7;Table 2-S)(Espinosa et al., 2009;Ostale- Valriberas et al., 2022). In fact, the results of the present study show that a one-point decrease in the value of accessibility increases the adult density by 0.96. 5 Conservational implications The results indicate that Ceuta is the main population of this endangered species in its entire range, being a source population on the Southern Iberian Peninsula that should be conserved as a priority. According to the Spanish National Conservation Strategy, sectors H, I, K, L and M have the highest number of adults and should therefore be categorized and managed as Critical Areas (MMAMRM, 2008; see Supplementary Figure 2-S). It could benefit many species of conservation concern also settled in the TABLE 4 Current known distribution of the P. ferruginea specie in the Western Mediterranean sea. Country Area Source Year of sampling Mean density (ind/m) Estimated total population Spain Andalucı aCMAOT, 2019 2019 0.63 ind/m*17,032** Ceuta Present study 2019-2020 7.28-5.56*ind/m 131,775** Melilla Guallart et al., 2013b 2010 2.82 ind/m*32,821** Chafarinas Guallart and Templado, 2016 2000 4.36 ind/m*42,230** AlboranCMAOT, 2019 2018 115** Morocco MPA of Al Hoceima (Cala Iris Islet) Bazairi et al., 2012 2012 1.22 ind/m 576 MPA of Al Hoceima (El Jebha) Bazairi et al., 2012 2012 3.66 ind/m Cape Three Forks Espinosa et al., 2014a 2012 from 0.36 to 0.83 ind./ m Algeria Plane Island Kallouche et al., 2020 2019 1.78 ind/m 3,993 Habiba Island Espinosa, 2009b 2008 4.8 –3.23*ind/m 50,400 Rachgoun Island Taibi et al., 2014 3-10 ind/m 2 Tunisia Zembra Zarrouk et al., 2016 2015 2.83 ind/m 2 *40,404** North-East Tunisian coast Tlig-Zouari et al., 2010 2006 0.025-4.5 ind/m 2 Italy Sinis Peninsula MPA (Sardinia) Coppa et al., 2012 2009 0.02 ind/m 196 Gulf of Olbia (Sardinia) Cristo et al., 2007 2007 0.023 ind/m 69 Maddalena Archipelago (Sardinia) Cossu et al., 2006 2005 0.028 ind/m 736 Mal di Ventre Island & Cape San Marco (central-western Sardinia) Marra et al., 2016 2013-2014 0.009 & 0.004 ind/m Lingurian coasts Ferranti et al., 2019 2017-2018 0.005 ind/m*32 France Port Cros Cottalorda et al., 2004 <0.01 ind/m 2 Cap Corse/Bastia harbour (Corsica) Vela and Leoni, 2007 0.2 ind/m 2 *, Adult mean density (ind/m); **, Estimated adult population. Ostale ´-Valriberas et al. 10.3389/fmars.2023.1127630 Frontiers in Marine Science frontiersin.org11
114 same habitat (“umbrella effect”), as demonstrated by Ostale- Valriberas et al. (2022). Previous studies have shown that 90% of the populations of a metapopulation are usually “sink populations”and only 10% are “source populations”(Pulliam, 1988), so this population is of great ecological relevance for this species. The results also support the concept of “Artificial Marine Micro-Reserves”as a new area-based management tool for marine conservation, establishing a network of these source populations that promote gene flow between populations with eventual recolonization of their original distribution (Garcı a- Gomez et al., 2011;Ostale-Valriberas et al., 2022)(Supplementary Figure 2-S). Finally, for future translocation procedures, the reported results could serve as a guide to select the most suitable receptor sites. Such areas should have high values of macro- or microscale heterogeneity and, similarly, should avoid vertical substrata and areas with anthropogenic impact. Data availability statement The original contributions presented in the study are included in the article/Supplementary Material. Further inquiries can be directed to the corresponding author. Author contributions EO-V, JS-V, FE, G-GJ conceptualization of the work and development the methodology. EO-V, FE application of statistical, mathematical, computational, or other formal techniques to analyze or synthesize study data. EO-V, AL, AA-A, JS-V, AP-P: Conducting a research and investigation process, specifically performing the experiments, or data/evidence collection. EO-V writhing the original draft, visualization work and supervision. AP-P, JS-V, FE, G-GJ writing -review & editing. EO-V, AL Management and coordination responsibility for the research activity planning and execution. EO-V, G-GJ acquisition of the financial support for the project leading to this publication. All authors contributed to the article and approved the submitted version. Funding The present study was financed with the Cooperation Agreement between two public administrations, the Sociedad, Obras, Infraestructuras y Medio Ambiente de Ceuta S.A.U. (OBIMASA) and the Fundacio n de Investigacio ndela Universidad de Sevilla (FIUS). We are grateful to Ana Garciaand Francisco Javier Martı nez-Medina for their work in the Cooperation Agreement. JS-V was supported by a FPI Grant (PRE2018-086266) from Ministerio de Ciencia, Innovaciony Universidades (Project CGL 2017-82739-P) co-financed by ERDF European Union and Agencia Estatal de Investigacion, Gobierno de España. Acknowledgments The authors would like to express their gratitude to our colleague Celeste Dominguez-Monge from the Laboratorio de Biologı a Marina of the University of Sevilla who helped us in the sampling process and in the mineral analysis. We are also particularly grateful for the assistance given by the diving center WaterGame Gran Azul, especially by Javier Ibañez and JoseManuel A vila. We also thank the editor of Frontiers in Marine Science, Professor Alan Hodgson, and the two reviewers for their constructive comments, which considerably improved the first version of the manuscript. Conflict of interest The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Publisher’s note All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher. Supplementary material The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fmars.2023.1127630/ full#supplementary-material References Aguilera, M. A., Tapia, J., Gallardo, C., Nuñez, P., and Varas-Belemmi, K. (2020). Loss of coastal ecosystem spatial connectivity and services by urbanization: natural-to- urban integration for bay management. J. Environ. Manage. 276, 111297. doi: 10.1016/ j.jenvman.2020.111297 Agung, M. F., Adhuri, D. S., Ferse, S. C., Sualia, I., Andradi-Brown, D. A., Campbell, S. J., et al. (2022). Marine conservation beyond MPAs: towards the recognition of other effective area-based conservation measures (OECMs) in Indonesia. Mar. Policy 137, 104939. doi: 10.1016/j.marpol.2021.104939 Ostale ´-Valriberas et al. 10.3389/fmars.2023.1127630 Frontiers in Marine Science frontiersin.org12
115 same habitat (“umbrella effect”), as demonstrated by Ostale- Valriberas et al. (2022). Previous studies have shown that 90% of the populations of a metapopulation are usually “sink populations”and only 10% are “source populations”(Pulliam, 1988), so this population is of great ecological relevance for this species. The results also support the concept of “Artificial Marine Micro-Reserves”as a new area-based management tool for marine conservation, establishing a network of these source populations that promote gene flow between populations with eventual recolonization of their original distribution (Garcı a- Gomez et al., 2011;Ostale-Valriberas et al., 2022)(Supplementary Figure 2-S). Finally, for future translocation procedures, the reported results could serve as a guide to select the most suitable receptor sites. Such areas should have high values of macro- or microscale heterogeneity and, similarly, should avoid vertical substrata and areas with anthropogenic impact. Data availability statement The original contributions presented in the study are included in the article/Supplementary Material. Further inquiries can be directed to the corresponding author. Author contributions EO-V, JS-V, FE, G-GJ conceptualization of the work and development the methodology. EO-V, FE application of statistical, mathematical, computational, or other formal techniques to analyze or synthesize study data. EO-V, AL, AA-A, JS-V, AP-P: Conducting a research and investigation process, specifically performing the experiments, or data/evidence collection. EO-V writhing the original draft, visualization work and supervision. AP-P, JS-V, FE, G-GJ writing -review & editing. EO-V, AL Management and coordination responsibility for the research activity planning and execution. EO-V, G-GJ acquisition of the financial support for the project leading to this publication. All authors contributed to the article and approved the submitted version. Funding The present study was financed with the Cooperation Agreement between two public administrations, the Sociedad, Obras, Infraestructuras y Medio Ambiente de Ceuta S.A.U. (OBIMASA) and the Fundacio n de Investigacio ndela Universidad de Sevilla (FIUS). We are grateful to Ana Garciaand Francisco Javier Martı nez-Medina for their work in the Cooperation Agreement. JS-V was supported by a FPI Grant (PRE2018-086266) from Ministerio de Ciencia, Innovaciony Universidades (Project CGL 2017-82739-P) co-financed by ERDF European Union and Agencia Estatal de Investigacion, Gobierno de España. Acknowledgments The authors would like to express their gratitude to our colleague Celeste Dominguez-Monge from the Laboratorio de Biologı a Marina of the University of Sevilla who helped us in the sampling process and in the mineral analysis. We are also particularly grateful for the assistance given by the diving center WaterGame Gran Azul, especially by Javier Ibañez and JoseManuel A vila. We also thank the editor of Frontiers in Marine Science, Professor Alan Hodgson, and the two reviewers for their constructive comments, which considerably improved the first version of the manuscript. Conflict of interest The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Publisher’s note All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher. Supplementary material The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fmars.2023.1127630/ full#supplementary-material References Aguilera, M. A., Tapia, J., Gallardo, C., Nuñez, P., and Varas-Belemmi, K. (2020). Loss of coastal ecosystem spatial connectivity and services by urbanization: natural-to- urban integration for bay management. J. Environ. Manage. 276, 111297. doi: 10.1016/ j.jenvman.2020.111297 Agung, M. F., Adhuri, D. S., Ferse, S. C., Sualia, I., Andradi-Brown, D. A., Campbell, S. J., et al. (2022). Marine conservation beyond MPAs: towards the recognition of other effective area-based conservation measures (OECMs) in Indonesia. Mar. Policy 137, 104939. doi: 10.1016/j.marpol.2021.104939 Ostale ´-Valriberas et al. 10.3389/fmars.2023.1127630 Frontiers in Marine Science frontiersin.org12 Airoldi, L., Abbiati, M., Beck, M. W., Hawkins, S. J., Jonsson, P. R., Martin, D., et al. (2005). An ecological perspective on the deployment and design of low-crested and other hard coastal defence structures. Coast. Eng. 52, 1073–1087. doi: 10.1016/ j.coastaleng.2005.09.007 Airoldi, L., and Beck, M. W. (2007). 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Res. 12 (9), 917–931. doi: 10.1080/ 17451000.2016.1213396 Ostale ´-Valriberas et al. 10.3389/fmars.2023.1127630 Frontiers in Marine Science frontiersin.org14 Supplementary Material Table 1-S: Results of the population structure of P. ferruginea and environmental factors for each sector (highest values are marked in green and the lowest are marked in red). For elemental composition only data with percentage of substrate oxides (>3%) are shown. CP: Percentage of calcination. SECTOR Mean Density (ind/m) Adult mean density (ind/m) Individual > 60 mm (ind/m) Mean size (mm) Adult mean size (mm) Macroscale roughness (m) Microscale roughness (cm) Area of P. ferruginea habitat Inclination of the substratum (degree) Chl-a (µg/cm²) Human activity Fetch (Fe) SiO2 (%) Al2O3 (%) Fe2O3 (%) MgO (%) CaO (%) K2O (%) P.C. A 1.05 0.87 0.27 30.74 27.48 1.43 30.76 27.48 30.07 0.77 53.83 199.51 36.00 8.70 1.97 6.85 17.00 2.32 25.99 B 3.38 3.38 0.94 42.09 47.55 1.25 31.17 14.62 13.44 1.30 35.50 213.42 42.66 10.57 3.15 5.98 12.92 2.08 20.95 C 5.04 3.88 0.88 42.58 48.00 1.59 32.41 19.82 21.14 0.87 58.83 203.13 0.42 0.19 0.09 17.25 33.64 0.07 48.11 D 6.06 5.30 1.37 41.86 45.27 1.28 31.37 9.00 16.36 1.15 18.17 99.11 1.47 0.15 0.14 7.96 44.03 0.04 45.93 E 4.95 4.68 2.18 58.41 60.29 1.23 31.78 19.43 18.79 0.90 20.67 176.29 41.88 9.86 2.42 7.19 12.72 2.92 21.29 F 5.46 5.01 1.86 49.57 52.54 1.19 31.95 24.25 17.63 0.80 26.00 303.89 70.91 12.84 0.83 0.68 1.78 3.46 6.29 G 5.06 4.39 1.56 51.01 53.64 1.25 31.24 34.55 18.04 1.32 12.17 299.86 63.53 12.69 1.28 0.43 4.99 5.51 8.77 H 8.82 7.89 2.22 51.82 54.17 1.12 32.59 23.14 19.61 0.84 18.83 492.95 64.55 13.24 1.82 0.62 4.06 3.48 8.87 I 10.47 8.81 1.61 45.81 49.25 1.33 30.64 25.50 28.01 0.64 13.83 1003.83 67.87 13.45 2.15 0.46 1.78 5.31 5.97 J 0.84 0.77 0.18 45.66 47.19 1.17 29.60 15.82 21.11 0.67 39.67 54.49 65.57 14.43 4.38 1.45 1.09 3.58 6.99 K 20.29 15.35 1.09 38.73 42.98 1.53 32.80 15.53 17.41 0.68 5.17 71.46 0.09 0.03 0.23 19.59 31.39 0.01 48.53 L 32.20 19.58 4.13 43.83 52.02 1.44 30.29 8.11 15.79 0.69 4.33 1.33 0.14 0.07 0.05 19.17 31.73 0.02 48.71 M 13.33 9.01 0.64 35.82 42.43 1.48 31.72 53.37 26.91 1.00 4.33 278.90 0.35 0.13 0.08 16.28 35.68 0.03 47.32 N 6.68 4.79 1.07 38.23 45.13 1.52 29.57 11.67 33.13 0.37 7.17 86.80 4.44 0.76 0.69 13.34 35.53 0.09 44.39 O 13.22 9.04 1.58 38.88 44.86 1.52 32.32 40.98 23.41 0.60 18.00 22.14 0.18 0.06 0.16 12.14 40.25 0.01 47.04 P 7.27 5.21 0.80 40.67 47.60 1.35 31.11 8.75 12.57 0.95 31.17 204.63 58.74 7.17 2.65 0.98 12.24 1.41 15.46 Q 2.45 1.95 0.31 39.41 42.27 1.19 29.57 16.85 19.37 0.90 19.83 1100.90 71.56 5.68 2.07 1.11 6.57 1.18 10.71 R 0.84 0.77 0.32 41.95 42.55 1.42 31.19 13.10 36.17 2.29 14.33 105.83 50.38 0.90 1.44 6.13 16.06 0.20 24.26
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