New records of copepods associated with marine invertebrates from the Strait of Gibraltar and nearby areas

Miscel.lania Zoologica 20.1 (1997) 101 New records of copepods associated with marine invertebrates from the Strait of Gibraltar and nearby areas P. J. López-González, M. Conradi & J.C. García-Gómez López-González, P J , Conradi, M, & García-Gómez, J C , 1997 New records of Copepods associated with marine invertebrates from the Strait of Gibraltar and nearby areas Mrsc Zool, 20 1 101-110 New records of Copepods assoc~ated wrth rnarrne rnvertebrates frorn the Strart of Grbraltar and nearby areas - In this work, 16 species of commensal or parasitic copepods associated with marine invertebrates from the Strait of Gibraltar are recorded Eleven species are included into the order Cyclopoida, three into Poecilostomatoida, one into Siphonostomatoida, and another into a family rncertae sedrs They have been found mainly associated with Ascidians, but also in Pelecypods, Polychaetes, Opisthobranch molluscs, Ophiuroids and Anthozoans Among these, 13 are new records for the Iberian peninsula fauna, and three are also new for the African coasts Moreover five species, Haplostornella rnalacocera Chatton & Harant, 1924, Haplostornella tuberculata Chatton & Harant, 1924, Periproctra falsrarcuata Stock, 1967, Anthessrus arcuatus López-González, Conradi, Naranjo & Garcia-Gomez, 1992 and Botryllophrlus conrcus Conradi, López-González & García-Gómez, 1994, are recorded for the first time since their original descriptions Furthermore, new hosts and bathymetrical data of most of the species are provided Key words Copepoda, Cyclopoida, Poecilostomatoida, Siphonostomatoida, Strait of Gibraltar, New records (Rebut: 12 1 96; Acceptació condicional: 7 X 96; Acc. definitiva: 29 IV 97) i? l. López-González, M. Conradi & l. C. García-Gómez, Lab. de Biología Marina, Fac. de Biología, Univ de Sevilla, Apdo. 1095, 4 1080 Sevilla, España (Spain). This study is part of the research project 'Estudio biológico de las comunidades bentónicas de la Bahía de Algeciras' supported by the Compañía Española de Petróleos, S A, Fundación Sevillana de Electricidad, Excmo Ayuntamiento de los Barrios, Mancomunidad de Municipios del Campo de Gibraltar y Agencia de Medio Ambiente (Junta de Andalucía) O 1997 Museu de Zoologia l López-González et al. lntroduction British and West-Eastern Mediterranean faunas of copepods associated with marine invertebrates are relatively well-known (HUMES & STOCK, 1973; Gorro, 1961, 1966, 1993; among others). Nevertheless, with the exception of several publications on symbiotic copepods from the Strait of Gibraltar, most studies have been carried out on molluscs, fishes and other commercial species (CORDERO et al., 1994). The Strait of Gibraltar is a biogeographically interesting region since it is the meeting point of three marine biogeographical regions: the Lusitanic, Mauritanic, and Western Mediterranean areas, thus inducing an overlapping of its respective faunas. Its exceptional situation offers the opportunity to study distributional processes of the species. It has been considered one of the areas with the highest biodiversity of al1 European coasts (TEMPLADO et al., 1993). However, the fauna of copepods associated peninsula Atlantic Mediterranean Ocean Sea Fig. 1. Sampling localities. Huelva: 1. El Portil; 2. Punta Umbría. Cádiz: 3. La Caleta; 4. Tarifa Island; 5. Punta Carnero; 6. Getares.; 7. San García; 8. El Saladillo and Algeciras Harbour; 9. Thermal power plant harbour; 10. C.E.P.S.A. harbour; 11. El Campamento; 12. San Felipe; 13. Gibraltar harbour. Ceuta: 14. Benzú Bay. Morocco: 15. Cabo Negro. Localidades de muestreo. Huelva: 1. El Portil; 2. Punta Umbría. Cádiz: 3. La Caleta; 4. Isla Tarifa; 5. Punta Carnero; 6. Getares.; 7. San García; 8. El Saladillo y Puerto de Algeciras; 9. Puerto central térmica; 10. Puerto C.E.P.S.A.; 11. El Campamento; 12. San Felipe; 13. Puerto de Gibraltar. Ceuta: 14. Bahía de Benzú. Marruecos: 15. Cabo Negro. Miscel.lania Zoologica 20.1 (1997) with marine invertebrates at this narrow communication between the Atlantic Ocean and the Mediterranean Sea is relatively unknown. Little is yet known about the presence and distribution of the copepod fauna from the Strait of Gibraltar and lberian peninsula. Although 230 species of copepods associated with marine invertebrates have been cited from the British islands (Gorro, 1993), no more than 20 species have been reported in the lberian peninsula. Recently, CORDERO et al. (1994) cited a total of seven copepod species associated with marine invertebrates in his catalogue of lberian zooparasites. None of the species reported from the Strait of Gibraltar by the authors of the present work were included. The Laboratorio de Biología Marina of the Universities of Sevilla and Cadiz (S Spain) has initiated a program to study the copepod fauna in the Strait of Gibraltar and nearby areas. So far, four marine biological expeditions have been carried out within a more comprehensive programme of marine benthos: 'Bahía 90' and 'Bahía 91' in Algeciras Bay (Southern lberian peninsula), and 'Ceuta 91' and 'Marruecos 93' in North Africa. Many shorter (seven days) sampling expeditions were also accomplished during the development of the marine biological project 'Estudio Biológico de las comunidades bénticas de la Bahía de Algeciras'. Sporadically, there have been other collections in various localities along the Atlantic coast of Cádiz and Huelva (South-eastern lberian peninsula). Some results from these expeditions have now been published: CONRADI et al., 1992, 1993, 1994a, 1994b; CONRAD~ & L~PEZ-GONZÁLEZ, 1996; L~PEZ-GONZÁLEZ et al., 1992a. 1992b, 1993, in press; LÓPEZ-GONZÁLEZ & CONRADI, 1995. The airn of the present article was to further our knowledge of symbiotic copepods from the Strait of Gibraltar, to include the whole Iberian peninsula and North Africa. In addition to the faunistic data, sorne ecological aspects are also discussed, mainly regarding the host specificity shown by the different copepods species. Biogeographical comments on these symbiotic copepods are incomplete due to the scarce data available. However, the collected species may be included into biogeographical categories, and their relationship with host specificity is discussed. Material and methods Marine invertebrates, hosts of the symbiotic copepods, were collected by hand in the mediolittoral zone, and by SCUBA diving, van veen dredge and box corer in the infralittoral zone. The sampling localities are shown in figure 1. Hosts were isolated in plastic flasks to avoid contamination and ensure the true copepod-host relationship. When possible, the marine invertebrates were immediately relaxed by the addition of crystal of menthol to the sea-water. Later, the hosts were fixed adding 35-40 % formalin to the seawater to reach the usual proportions for this fixative (4-6 %). Commensal and most ectoparasitic copepods were obtained by sieving the formalin through a 100 pm mesh, after washing. Other ectoparasitic copepods were carefully removed directly from their hosts. Endoparasitic copepods were obtained by dissection of marine invertebrates under a dissecting microscope. All copepods were preserved in 70% ethanol. Copepods were cleared in lactic acid, slightly stained with clorazole black, and dissected under a stereomicroscope. Semipermanent preparations were made in lactophenol. Results Table 1 summarizes the parasitic or commensal copepods reported, number of specimens studied, date of collection, locality where found, depth range observed, hosts, main references (with complete description, or with interesting anatomical characteristics or ecological data), and general distribution. Discussion The present study has shown severa1 copepod species to have a larger host range than was previously reported. Gunenotophorus globularis is recorded for the first time associated with an ascidian species belonging to the genus Pseudodistoma (see ILLG, 1958; GOTTO, 1993). Haplostomella malacocera was originally described by CHATTON & HARANT 104 López-González et al. Table 1. Species of parasitic or commensal copepods collected from the Strait of Gibraltar and nearby areas: * New records for the lberian fauna; + New records for the African fauna; 99 Ovigerous females; dd Adult males; 9 Young females; cop. Copepodid. (For locality codes see figure 1.) Specimens Date Locality Order Cyclopoida Burmeister, 1834 Family Notodelphyidae Dana, 1853 Genus Doropygus Thorell, 1859 Doropygus pulex Thorell, 1859 (*) 14 99 V 1992 1 Genus Pachypygus G.O. Sars, 1921 Pachypygus gibber (Thorell, 1859) (*) 1 99 24Vlll1991 12 Genus Botachus Thorell, 1859 - Botachus cylindratus Thorell, 1859 (*) 11 99,16"0" 23 VI 1991 7 4 99 24 Vlll 1991 12 Genus Gunenotophorus Buchholz, 1869 Gunenotophorus globularis Buchholz, 1869 (*)1 99 25 11 1992 12 Genus Doroixys Kerschner, 1879 Doroixys uncinata Kershner, 1879 (+) 25 99 Vlll 1993 15 Genus Peri~roctia Stock, 1967 Periproctia falsiarcuata Stock, 1967 (*) 8 ?? 27 IX 1993 7 - - Family Ascidicolidae Thorell, 1859 Subfamily Ascidicolinae Thorell, 1859 Genus Ascidicola Thorell, 1859 Ascidicola rosea Thorell, 1859 (*) 1 99 9 VI1 1991 11 1 99 4 VI 1993 4 Subfamily Haplostominae Chatton & Harant, 1924 Genus Ha~lostomella Chatton and Harant, 1924 Haplostomella malacocera Chatton & Harant, 1924(*) 1 1 99 23 XI 1991 13 Miscel.lania Zoologica 20.1 (1997) 105 Especies de copépodos parásitos o comensales recolectados en el estrecho de Gibraltar y áreas próximas: * Nuevas citas para la península ibérica; + Nuevas citas para la fauna africana; 99 Hembras ovígeras; 88 Machos adultos; 9 Hembras jóvenes; cop. Copepodito. (Para códigos de localidades ver figura 1.) Depth Hosts References Distribution 0.5 m Styela plicata SARS, 1921; ILLG, 1958; Mediterranean, North (Lesueur) ILLG & DUDLEY, 1961; Atlantic, West Africa, Gorro, 1993 Barbados, Japan,Srilanka, Australia, New Zealand ti m Phallusia fumigata ILLG, 1958; Ooa~i, 1961; Mediterranean, North- (Grübe) Gorro, 1993 eastern Atlantic, Japan, Australia? 3 m Ascidia mentula SARS, 1921; ILLG, 1958; Mediterranean, North- Müller ILLG & DUDLEY, 1961; eastern Atlantic 6 m Phallusia fumigata Gorro, 1993 (Grübe) 5 m Molgula bleizi CANU, 1892; SARS, 1921; Mediterranean, North- (Lacaze-Duthiers) ILLG, 1958; Gorro, 1993 eastern Atlantic, Florida Southern Africa, lndic 3-6 m Pseudodistoma CANU, 1892; ILLG, 1958; Mediterranean, Northobscurum Péres Gorro, 1993 eastern Atlantic 9 m Polysincraton lacazej ILLG & DUDLEY, 1961 (as Western Mediterranean Giard Bonnierilla arcuata 10-15 m Brément, 1909); STOCK, 1967 5 m Molgula sp. CANU, 1892; CHATTON & Mediterranean, North- 15 m Halocynthia papillosa BRÉMENT, I~~~;SARS, 1921; eastern Atlantic California, (Linné) MONNIOT, 1961; ILLG & Canada, Antarctic DUDLEY, 1980 2-6 m Aplidinium elegans CHA~ON & HARANT, 1924; Western Mediterranean (Giard, 1872) OOISHI & ILLG, 1977; ILLG & DUDLEY, 1980 6 m 106 López-González et al. Table 1 (cont.) Specimens Date Locality Haplostomella tubercula ta 6 99 Vlll 1991 14 Chatton & Harant, 1924 (*+) 5 99 22 VI1 1994 5 Subfamily Botryllophilinae Sars, 1921 Genus Botr~llophilus Sars, 1921 Botryllophilus conicus Conradi, López-González & García-Gómez, 1994 53 99 IX 1993 6 - Family Mesoglicolidae Zulueta, 191 1 Genus Mesoqlicola Quidor, 1906 Mesoglicola delagei Quidor, 1906 (*) 19~9,1488 VI1 1991 1 O 499, 4 83 8 5 99, 3 9 1099, 83d* XI1993 7 Orden Poecilostomatoida Thorell, 1859 Family Sabelliphilidae Gurney, 1927 Genus Hermanella Canu, 1891 - Herrmanella rostrata Canu, 1891 (*) 25 99 VI1 1995 2 Family Nereicolidae Claus, 1875 Genus Nereicola Keferstein, 1863 - Nereicola ovatus Keferstein, 1863 (*) 3 99. 22 VI1 1995 3 1 cop. Family Anthessiidae Humes, 1985 Genus Anthessius Della Valle, 1880 Anthessius arcuatus López-González, Conradi, Naranjo & García-Gomez, 1992 (+) 4 99, 25 88, 18 Vlll 1991 14 40 COP. Orden Siphonostomatoida Latreille, 1829 Family Cancerillidae Giesbrecht, 1897 Genus Cancerilla Dalyell, 1851 Cancerilla tubulata Dalyell, 1851 (*) 1 99 XI 1992 12 1 99 VI1 1993 8 Family incertae sedis Family Antheacheridae M. Sars, 1870 Genus Staurosoma Will, 1844 Staurosoma parasiticum Will, 1844 (*) 5 99, 5 88 VI1 1995 11 Miscel.lania Zoologica 20.1 (1997) Depth Hosts References Distribution 5 m Aplidium elegans CHATTON & HARANT, 1924; Western Mediterranean (Giard) OOISHI & ILLG, 1977; ILLG & 5-7 m Pseudodistoma DUDLEY, 1980 obscurum Peres 8 m Aplidium conicum CONRADI et al., 1994a Strait of Gibraltar (Olivi) 20 m Corynactis viridis QUIDOR, 1906, 1922, 1936; Western editerranean, Allman TATON, 1934; HAEFELFINGER North-eastern Atlantic 5-9 m & LAUBIER, 1965; CONRADI 9 m & LÓPEZ-GONZÁLEZ, 1996 7 m 0.5 m Mactra coralina CANU, 1892; HUMES & Mediterranean, North- (Linné) STOCK, 1973; Gorro, 1993 eastern Atlantic 5 m Platynereis dumerilii KEFERSTEIN, 1863; STOCK, Mediterranean, Black Sea, (Audouin & Milne 1966; Gorro, 1993 North-eastern Atlantic Edwards) 8 m Berthellina sp. LÓPEZ-GONZÁLEZ et al., Strait of Gibraltar 199213 5 m Amphipholis CARTON, 1968; KENSLEY, Mediterranean, Northsquamata Delle 1970; Gorro, 1993 eastern Atlantic, North- Chiaje eastern Pacific, South- 4 m eastern Africa 0.5 m Anemonia sulcata CAULLERY MESNIL, 1902; Mediterranean, North- Pennant ZULUETA, 191 1; LAUBIER eastern Atlantic, Red Sea SCHMIDT, 1971; Gorro, 1993 López-González et al. (1924) but it was not assigned to any host species since the authors only commented 'dans un Aplidien'. In the present study the species was found associated with the compound ascidian Aplidium elegans. Haplostomella tuberculata was found for the first time associated with in Aplidium elegans and with a Pseudodistoma species (see CHATTON & HARANT, 1924; OOISHI & ILLG, 1977). Finally, the recently described species A. arcuatus originally associated with the opistobranch molluscs Bertella stellata (see L~PEZ-GONZALEZ et al., 1992b) was found associated with a related host genus, Bertellina. According to these records, 13 of the 16 species of commensal or parasitic copepods associated with marine invertebrates are new records for the lberian peninsula fauna, and three are also new for the African coasts (see table 1). Moreover five species: H. malacocera, H. tuberculata, I? falsiarcua ta, A. arcua tus, and B. conicus, are recorded for the first time since their original descriptions. The species collected can be included into three different geographical categories according to previous bibliographical data (see ILLG & DUDLEY, 1961; 1980; Gorro, 1993): cosmopolite (C), neighbouring Atlantic and Mediterranean (AM), and Western Mediterranean (WM). In addition, a further subdivision can be introduced with respect to the host range observed for the different copepod species: a wide range of hosts (WH), severa1 genera of hosts (SH), and high specificity of hosts (HH). The species reported in this paper may thus be arranged as follows: C-WH: D. pulex, I? gibber, G. globularis, A. rosea; AM-SH: B. cylindratus, D. uncinata, H. rostrata; AMHH: M. delagei, N. ovatus, S. parasiticum (plus Red Sea), C. tubulata (plus Southern Africa); WM-SH: P. falsiarcuata; WM-HH: H. malacocera, H. tuberculata, B. conicus, A. arcua tus. It is not unexpected that those species with a wide distributional range also have a wide host range. Most species included in this category are associated with ascidian species usually found in fouling studies, attached to commercial ships or related with rafting processes. Moreover, most of the species here cited are included in AM and WM geographical categories, with SH and HH. However, it is expected to find more cosmopolitan species in future research. Although the majority of these copepods are probably scientifically known and reported mainly from the European and North African coasts, it is likely that, in the next few years, new species from material obtained in the lberian peninsula will be described. It will be possible to discuss the relationship between lberian fauna and those from the other countries or regions once more data from the lberian peninsula becomes available. Acknowledgements The authors wish to thank the many researchers from different institutions and countries for their valuable collaboration with information and literature in order to improve the knowledge of the lberian fauna of commensal and parasitic copepods. We also thank Drs. Rocío Juan and Cesar Megina for their help during the collecting period. Resumen Nuevos datos de copépodos asociados a invertebrados marinos en el estrecho de Gibraltar y áreas próximas En este trabajo se citan 16 especies de copépdos comensales o parásitos asociados a invertebrados marinos en el estrecho de Gibraltar y áreas próximas (fig. 1, tabla 1). Once de ellas pertenecen al orden Cyclopoida, tres a Poecilostomatoida, una a Siphonostomatoida, y otra a una familia de posición incierta. La mayoría de estas especies han sido halladas asociadas a ascidias, aunque también se citan copépodos asociados a bivalvos, poliquetos, moluscos opistobranquios, ofiuroideos y antozoos. Se aportan nuevos datos sobre el rango de hospedadores de Gunenotophorus globularis, Haplostomella malacocera, H. tuberculata y Anthessius arcuatus. De las 16 especies incluidas en este estudio, 13 son citadas por primera vez para la península ibérica, y tres lo son Miscel.lania Zoologica 20.1 (1997) también para la fauna africana. Además cinco especies son citadas por primera vez desde su descripción original: Haplostomella malacocera Chatton & Harant, 1924; Haplostomella tuberculata Chatton & Harant, 1924; Periproctia falsiarcuata Stock, 1967; Anthessius arcuatus López-González, Conradi, Naranjo & García-Gómez, 1992 y Botryllophilus conicus Conradi, López- González & García-Gómez, 1994. Desde un punto de vista zoogeográfico resulta prematuro concluir afinidades faunísticas del estrecho de Gibraltar con regiones biogeográficas colindantes. El conocimiento de esta fauna en la península ibérica es aún insuficiente, y esperemos que en nuevos trabajos se sigan citando especies de copépodos simbiontes para alcanzar un nivel de conocimiento comparable, al menos, al de otras regiones del Atlántico nordeste. References CANU, E., 1892. Les copépodes du Boulonnais. Morphologie, embryologie, taxonomie. Trav. Lab. Zool. marit. Wimereux, 6: 1- 354. CARTON, Y., 1968. 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