Studying exotics in their native range: Can introduced fouling amphipods expand beyond artificial habitats?

Depósito de investigación de la Universidad de Sevilla https://idus.us.es/ “This version of the article has been accepted for publication, after peer review (when applicable) and is subject to Springer Nature’s AM terms of use, but is not the Version of Record and does not reflect post-acceptance improvements, or any corrections. The Version of Record is available online at: https://doi.org/10.1007/s10530-016-1191-5 ” 1 Studying exotics in their native range: can introduced fouling amphipods expand beyond artificial habitats? Macarena Rosa*, Mariana B. Lacerdab, Maite Vázquez-Luisc, Setuko Masunarib and José M. Guerra-Garcíaa aLaboratorio de Biología Marina, Departamento de Zoología, Facultad de Biología, Universidad de Sevilla, Avda. Reina Mercedes 6, 41012, Sevilla, Spain. bDepartamento de Zoologia, Universidade Federal do Paraná, Caixa Postal 19023, Curitiba, Paraná, Brazil. cInstituto Español de Oceanografía, Centre Oceanogràfic de les Balears, Moll de Ponent s/n, 07015 Palma de Mallorca, Spain. *Corresponding author: [email protected], +34 954556229 Running head: Introduced mobile invertebrates beyond artificial habitats Abstract Knowledge of the habitat use patterns of introduced species in their native or naturalized range can provide unique insights into processes of secondary dispersal and colonization of natural habitats. Caprellid amphipods are small mobile marine epibionts with limited natural dispersal. The global distribution of some caprellid species is mostly the result of anthropogenic transport; however, their subsequent spread beyond artificial habitats is poorly understood. A biogeographic approach, mainly focused on the native-range ecology of introduced and common fouling caprellid amphipods of southern Europe, was used to understand the implications of habitat use patterns for predicting their spread in the introduced regions. Specifically, abundance and composition of caprellid populations were compared among different primary habitats including artificial (floating pontoons), sheltered and wave-exposed rocky shores along the southern and southeastern coasts of Brazil. The findings indicated that artificial habitats act as reservoirs for globally distributed species in both their native and introduced ranges, while endemic species are more scarcely represented. Environmental conditions provided by primary habitats appear important in structuring caprellid assemblages on 2 secondary substrata (basibiont species). Most wide-ranging caprellids were negatively correlated with the level of wave exposure, being more abundant in sheltered (artificial or natural) than in exposed habitats. In this context, Caprella scaura and Paracaprella pusilla, the two introduced caprellids recorded in the Mediterranean, where they are virtually restricted to artificial habitats, may become established in sheltered and even highly polluted natural habitats but hardly colonize wave-exposed rocky shores. Keywords Invasive species; Crustacea; Habitat use; Artificial substrata; Fouling community; Secondary spread. Introduction One of the major challenges for predicting the future trends of biological invasions is to understand the factors that limit species distributions and those that promote their invasion success (Guo, 2006). Given that biological invasions operate on a global scale, a biogeographic perspective seems necessary to properly understand the factors driving this process. Efforts so far to address this issue have focused primarily on areas of introduction rather than native ranges (Hierro et al. 2005). However, information from native populations and habitats are critical for investigating the causes of species invasiveness and for expanding management efforts in the invaded ranges (Hierro et al. 2005; Guo, 2006). In this context, studying the patterns of habitat use of newly introduced species in their native or naturalized range, where they are presumably close to equilibrium with controlling factors, can provide major insights for identifying limiting factors and for predicting which types of habitats will be more susceptible to invasion (Hierro et al. 2005; Guo 2006; Chavanich et al. 2006; Hejda et al. 2009; van Kleunen et al. 2010). A better understanding of the native-range ecology of terrestrial non-indigenous species (NIS), especially plants, has provided valuable information on how some species successfully invade new habitats (e.g. Pyšek et al. 2009, 2014; Castro-Díez et al. 2011; Hui et al. 2011). However, this issue has been poorly studied in marine ecosystems. In fact, the ecology of marine NIS in their home range is poorly studied (Chavanich et al. 2006; Parker et al. 2013) and native-invaded comparisons are extremely rare (Lohrer et al. 2000). More specifically, few studies have compared differences in both habitat use 3 patterns and abundances of introduced species between their native and invaded ranges (but see Davidson et al. 2008; Gribben et al. 2013). Several studies have shown that intertidal assemblages on artificial structures and those on nearby rocky shores are different (Connell and Glasby 1998; Bulleri and Chapman 2004). Part of these differences is the higher abundance of NIS in artificial habitats in comparison to the natural surrounding habitat (Glasby et al. 2007; Marins et al. 2010). However, surveys of artificial structures (primary habitats) are mostly focused on sessile benthic invertebrates or seaweeds. Smaller mobile organisms inhabiting the secondary substrata provided by fouling animals and seaweeds (secondary habitat) are generally overlooked (Chapman et al. 2005; People 2006; Wilhelmsson and Malm 2008; Marzinelli et al. 2009). Furthermore, the respective roles of primary and secondary habitat in structuring epifouling assemblages remain unclear. This is particularly relevant in groups such as caprellid amphipods, because although most caprellids can inhabit different substrata, the existence of substrata affinities has been shown for many species (e.g. Keith 1971; Lacerda and Masunari 2011). These small crustaceans often dominate the mobile invertebrate fauna associated with artificial structures of harbours and marinas, where they can reach densities of >3000 individuals per m2 (Buschbaum and Gutow 2005). Within these habitats, non-indigenous caprellids can contribute to an increase in the biotic resistance of fouling communities by hindering the settlement of larvae of invasive sessile species (Collin and Johnson 2014; Rius et al. 2014), but they also have the ability to displace ecologically similar congeners (Boos 2009; Shucksmith et al. 2009; Ros et al. 2015), posing a risk to native communities. Despite not having a larval stage, introduced caprellids can be anthropogenically dispersed over long distances in association with ship-related vectors such as ballast water and hull fouling (Gollasch et al. 2002; Ashton et al. 2014). On a local scale, while recreational boating seems effective in the transport of exotic caprellids among marinas, it fails to spread them from these habitats to intertidal rocky shores (Ros et al. 2013a). Thus, introduced caprellids seem virtually restricted to artificial habitats in their invaded range, indicating the existence of a limiting step in their invasion dynamic, the causes of which are still unknown. It has been suggested that anthropogenic vectors are more likely to be used as long distance dispersal mechanisms by species that are better adapted to particular habitats, such as those that are sheltered (Ruiz et al. 2009) or frequently disturbed by human activity (Byers 2002; Bulleri and Airoldi 2005; Piola and Johnston 2008). Wave exposure 4 and patterns of water transport are major determinants of community composition in general (Southward and Orton 1954; Lewis 1964; Underwood 1981; Bulleri and Chapman 2004) and amphipod communities in particular (Fenwick 1976; Takeuchi et al. 1990; Guerra-García and García-Gómez 2001). These factors may be especially important for caprellid species, many of which obtain their food from suspended material in the water column (Guerra-García and Tierno de Figueroa 2009). However, the role of wave exposure in the invasion dynamic of introduced caprellids has not yet been investigated. Despite the difficulty in determining the origin of anthropogenically dispersed species (see Carlton 1996), the southeastern coast of Brazil is considered to be part of the potential native range of the two caprellid species introduced in the Mediterranean: Caprella scaura Templeton, 1836 and Paracaprella pusilla Mayer, 1890. Paracaprella pusilla was first described in Brazil and C. scaura, although it was first described in Mauritius, was also recorded in Brazil only two years later by Dana (1853) (see Ros et al. 2014a for further details). Thus, both species have long been established in this tropical area, like other wide-ranging caprellids, such as Caprella dilatata Krøyer, 1843 (also first described in Brazil) or Caprella equilibra Say, 1818 (described in the North West Atlantic coast). The latter two species are traditionally considered as native in the Atlantic Ocean and the Mediterranean Sea because they have been established in these regions for hundreds of years (McCain and Steinberg 1970). Along with a wide distribution and a human-mediated dispersion, all of these four species (hereinafter referred to as target species) have in common that they are much more abundant in artificial than in natural environments in the Mediterranean Sea (Bellan-Santini and Ruffo 1998; Ros et al. 2013a). In this study, we used a biogeographic approach mainly focused on the nativerange ecology of four targeted fouling caprellid species to understand the role that habitat use patterns play in their current distribution and the factors that may favor or hinder their successful establishment in natural habitats. Additionally, we analyze the invasive potential of P. pusilla and C. scaura through a standardized invaded-native range comparison. Specifically, we tested the following hypotheses: 1) that caprellid assemblages differ among habitat types in their native range in Brazil. Particularly, the target species (C. scaura, P. pusilla, C. dilatata and C. equilibra) would be more abundant in artificial than in natural habitats and, within sheltered natural habitats compared to exposed ones; 2) that the influence of primary habitat (artificial structure vs sheltered 5 rocky shore vs wave-exposed rocky shore) is important in determining the distribution of caprellid species living on secondary substrata (in this case the hydroid Eudendrium sp.); 3) that within the same primary habitat (artificial structures present in marinas) and the same secondary substratum (the bryozoan Bugula neritina or the hydroid Eudendrium sp.), the abundance of C. scaura and P. pusilla is similar in their invaded and native range. Material and methods Field survey and laboratory processing Habitat use patterns in the native range (hypothesis 1) The sampling survey was carried out in October and November 2012 (spring/summer). Four localities, separated from each other by hundreds of kilometers (L1: Arraial do Cabo, L2: São Sebastião, L3: Paranaguá Bay, L4: Bombinhas-Porto Belo), were surveyed along the southeast (Rio de Janeiro and São Paulo) and south (Paraná and Santa Catarina states) coasts of Brazil (Fig. 1, Table 1). In each locality, three habitat types, separated by thousands of meters, were selected for comparison: artificial habitats, consisting of floating pontoons present in marinas (or in close proximity, as was the case of Bombinhas-Porto Belo); natural sheltered habitats, consisting of rocky shores protected from wave action; and wave-exposed natural habitats, consisting of rocky shores well exposed to wave action. Localities were selected with the aim to cover a regional scale of comparison. In each habitat type, three sites separated by tens of meters were surveyed, and three replicates were taken per site. Replicates were chosen to adequately sample caprellid diversity, avoid patchiness, and make the three habitat types comparable. Hence, three replicates each consisting of arborescent substrata (including hydroids, bryozoans and seaweeds) were randomly collected per site, preferentially on vertical surfaces, until a volume of approximately 750 ml per replicate was completed (see Thiel et al. 2003; Guerra-García et al. 2010; Ros et al. 2013b for method adequacy). Nine replicates were therefore collected per habitat type. All three habitat types were sampled in each locality on the same or consecutive days. For this survey and those described below, samples were collected directly by hand from the lateral surface of the floating pontoons (close to the water surface) and from intertidal rocky shores at low tide, while snorkeling was used to collect samples at high tide. Just after collection, samples were preserved in 70% ethanol. At the laboratory, all caprellids were sorted and identified 6 to species level. Moreover, these caprellid species were classified in the following geographical distribution groups (modified from Guerra-García et al. 2009): I, Endemic to Brazil; II, Endemic to Atlantic; III, Endemic to Atlantic and Mediterranean; IV, Cosmopolitan. Total volume of substratum per replicate was estimated as the difference between the initial and final volume when placed into a graduated cylinder with a fixed amount of water. The abundance of caprellids was expressed as the number of individuals/1,000 ml of substratum displacement. Influence of primary habitat on caprellids living on secondary substrata (hypothesis 2) To investigate the importance of primary habitats in structuring caprellid assemblages on secondary substrata, sampling efforts were focused on a well-defined basibiont species, the hydroid Eudendrium sp. This hydroid was selected due to its ability to grow in different habitat types and because it is a suitable habitat for caprellid species (e.g. Bavestrello et al. 1996; Ros et al. 2013b; Navarro-Barranco et al. 2014). Unfortunately, Eudendrium sp. was only present in the three habitat types within one locality (L3: Paranaguá Bay). No other substratum species was present in all three habitat types within a one locality. Thus, three replicates each consisting of a well developed colony of Eudendrium sp were also collected from each site of Paranaguá Bay (caprellids associated with twenty seven hydroid colonies were therefore analyzed in total) during the survey described above. Invaded-native range comparison (hypothesis 3) For comparison of the abundance of the two caprellid species introduced in the Mediterranean in native and invaded areas of their distribution, artificial structures (floating pontoons) were selected as the primary habitat (since P. pusilla and C. scaura are present in these structures in the two distribution ranges but are absent in the other habitats in their invaded range). The secondary substratum species selected was Eudendrium sp. in the case of P. pusilla (because it is considered the preferred basibiont species for this species in the Mediterranean Sea and nearby areas; Ros and Guerra-García 2012; Ros et al. 2013b) and the bryozoan Bugula neritina for C. scaura (for the same reason as in P. pusilla; see Ros et al. 2014a). In the introduced range (Mediterranean), a field survey was conducted in five marinas from the Western Mediterranean coast from May to July 2012 (spring/summer). Palma marina in Mallorca Island (Spain, 39º 34’N, 2º 38’E) and Ibiza Yacht Club in Ibiza Island (Spain, 38º 54’ N, 1º 26’ E) were selected for the native vs introduced range comparison of P. pusilla (since these are the only 7 marinas where the species has been found in the Mediterranean). In the case of C. scaura, Mahón maritime Club in Menorca Island (Spain, 39º 52’ N, 4º 18’ E), Civitavecchia marina (Italy, 42º 05’ N, 11º 47’ E) and Gzira marina (Malta, 35º 54’ N, 14º 29’ E) were selected in order to cover a wide range of its distribution in the Mediterranean (the number of marinas was selected based on the number of marinas in which C. scaura was present in Brazil to develop a balanced analysis). Three colonies of B. neritina and Eudendrium sp. for C. scaura and P. pusilla respectively were collected in these artificial habitats. In the native range (Brazil), Eudendrium sp. colonies were collected during the Brazilian survey described above from the artificial habitats at L2 (São Seastião) and L3 (Paranaguá Bay) (Fig. 1, Table 1) for P. pusilla. In the case of C. scaura, B. neritina colonies collected from the artificial habitats at L1 (Arraial do Cabo), L2 and L4 (Bombinhas-Porto Belo) were used for comparison. Substrata colonies were collected in the same season (spring/summer) and in the same way (see above) in the two distribution ranges. Wave exposure analysis Quantification of wave exposure in each station was based on a fetch model index developed by Howes et al. (1994). Fetch models provide good quantitative approximations of wave exposure to predict marine community patterns (e.g. Burrows et al. 2008; Hill et al. 2010). This model relies on two indices of fetch: modified effective fetch and maximum fetch. Combination of the two indices allows determining the wave exposure class of each station (Table 2) and is calculated from the following equation: Fe= [Σ (cosθi) x Fi] / Σ cosθi where Fe is the effective fetch in km, θi is the angle between the shore-normal and the direction (0°, 45° to the left and 45° to the right), and Fi is the fetch distance in km along the relevant vector. Maximum fetch is defined as the maximum fetch distance in km measured from the point of interest. A value of 1,000 km is conventionally used when open-ocean fetches occur. The mean value in km of modified-effective fetch and maximum fetch (hereafter average fetch) for each station was used as a continuous variable in subsequent analyses. Statistical analysis Differences in the composition of caprellid assemblages among habitat types in Brazil (hypothesis 1) were tested by the use of a permutational multivariate analysis of 8 variance (PERMANOVA) with three factors: ‘habitat’, fixed with three levels (artificial structure, sheltered and wave-exposed); ‘locality’, random and orthogonal with ‘habitat’, with four levels (L1: Arraial do Cabo, L2: São Sebastião, L3: Paranaguá Bay, L4: Bombinhas-Porto Belo); and ‘site’, random and nested within habitat and locality, with three levels. Analysis was based on Bray-Curtis dissimilarities. Significance P-values were obtained by computing 9999 permutations of residuals under a reduced model (Anderson and Legendre 1999). Pairwise comparisons were then used between factors to determine where significant differences occurred within the caprellid assemblage. To test differences of caprellid assemblage multivariate dispersions and composition among habitats a PERMDISP was applied and further illustrated with nMDS (based on Bray- Curtis dissimilarities). We may expect less variance on artificial habitats due to greater homogeneity in physical structure than on natural habitats. To specifically explore the abundance patterns of the target caprellid species (P. pusilla, C. scaura, C. dilatata, C. equilibra) along the Brazilian coast a three-factor univariate analysis of variation (ANOVA) was used. The experimental design was the same as used for the PERMANOVA. Prior to ANOVA, heterogeneity of variance was tested using Cochran's C-test and data were transformed if variances were significantly different. Where variance remained heterogeneous, untransformed data were analysed as ANOVA is a robust statistical test and is relatively unaffected by heterogeneity of variances, particularly in balanced experiments (Underwood 1997). However, in such cases to reduce type I error, the level of significance was reduced to <0.01. Where ANOVA indicated a significant difference for a given factor, the source of difference was identified using Student– Newman–Keuls (SNK) tests. To further explore any significant correlation between the abundance of each target species and wave exposure, a Spearman rank correlation was used. To explore the role of primary habitat in structuring caprellid assemblages inhabiting the same secondary substratum (hypothesis 2), a two-factor ANOVA was used. Thus, variation on a local scale in the abundance of each caprellid species inhabiting the hydroid Eudendrium sp. was examined in response to the factors ‘habitat’, fixed with three levels (artificial structure, sheltered and wave-exposed) and ‘site’, random, nested with habitat, with three levels. Finally, variation in the abundance of the two introduced caprellids recorded in artificial habitats between their native and invasive range (hypothesis 3) were determined 15 the abundance between native and introduced populations were mainly driven by a lack of parasites in the introduced distribution range. When the abundance patterns of C. scaura and P. pusilla were compared in the same habitat (i.e. marinas) in their native and introduced range, we found that P. pusilla was much more abundant in its native range (Brazil) than in its introduced range (Western Mediterranean), showing limited invasive potential. By contrast, C. scaura was far more abundant in its introduced range than in its native range, coinciding with a rapid expansion along the whole coast of the Mediterranean (Ros et al. 2014a). This caprellid is the dominant mobile epifouling species in many marinas of this region and is considered a potential agent of displacement of other caprellid species traditionally associated with the same spatial niche (Ros et al. 2015). The next step is to understand why C. scaura and other invasive species are able to attain such dominance in recipient vs. native communities. Conclusions In summary, this study indicates that artificial structures and wave exposure may affect the invasion dynamic of introduced caprellid species in a different way. Artificial habitats harbored high densities of caprellid species with a widespread distribution, while endemic species were scarcely represented. On the other hand, most of these wideranging caprellids were negatively correlated with the level of wave exposure, being more abundant in sheltered (artificial or natural) than in exposed habitats. Thus, wave exposure could be considered a limiting factor for the distribution of Caprella scaura and Paracaprella pusilla, the two introduced caprellids recorded in the Mediterranean Sea, while artificial floating structures facilitate their successful spread. On this basis, these caprellid species could be able to establish in sheltered and even highly polluted rocky shores of the Mediterranean coast over time, but they may fail to establish in waveexposed habitats. The abundance of C. scaura was higher in the invaded range compared to the native range, but we obtained the opposite pattern for P. pusilla. Further studies are necessary to understand why C. scaura is able to attain such dominance in artificial habitats located in its introduced range. Acknowledgements 16 We are very grateful to the members of the Laboratory for Systematic and Ecology of Crustacea, Laboratory for Cnidaria Studies and Laboratory for Ecology and Systematic of Ascidiacea, all belonging to the Federal University of Paraná for their kind assistance during the field work developed in Brazil. We are also indebted to Marcela B. Lacerda and M. G. G. Nascimento for their help during the field survey in Santa Catarina, to Luciana Atlvater and Alexandre D. Kassuga for all their support and valuable advice during the survey developed in Arraial do Cabo and to Gàlia Banach for her help during the field work in Malta. We thank Martin Thiel, the associate editor Jeff Wright and the anonymous reviewers whose helpful comments improved the manuscript. This work was funded by a predoctoral grant from the Ministerio de Educación (Reference AP-2009- 3380) and by the Junta de Andalucía: projectos de excelencia (Project P11-RNM-7041). Table legends Table 1 Sampling localities coordinates, collection dates, wave fetch values and wave exposure class (see Table 2). Habitat: a, artificial; p, sheltered; e, wave-exposed. Wave exposure classes: VP, very protected; P, protected; SP, semi-protected; E, exposed. Table 2 Wave exposure classes based on the modified-effective fetch and maximum fetch matrix (after Howes et al. 1994). VP: very protected; P: protected; SP: semi-protected; SE: semi-exposed; E: exposed. Table 3 Mean abundance of each caprellid species found in each habitat type throughout the study area. BG: biogeographical distribution groups; I, Endemic to Brazil; II, Endemic to the Atlantic; III, Endemic to the Atlantic and Mediterranean; IV, Cosmopolitan. Table 4 Summary of PERMANOVA examining variation in caprellid assemblages among habitat and each locality, Pairwise tests among habitats within each location and PERMDISP results for the factor “habitat”. Abbreviations: Habitat: a, artificial; p, sheltered; e, wave-exposed. Asterisks indicate significant differences: * P < 0.05, ** P < 0.01 and *** P < 0.001. Table 5 Summary of ANOVA examining the caprellid species richness, total caprellid abundance and abundance of dominant species (Paracaprella pusilla, Caprella scaura, C. dilatata and C. equilibra) among habitat types. Abbreviations: n.s., non significant; MS, mean square. Asterisks indicate significant differences: * P < 0.05, ** P < 0.01 and *** P < 0.001. 17 Table 6 ANOVA results of the abundance values of each caprellid species inhabiting Eudendrium colonies among habitat types in Paranaguá Bay. Abbreviations: Habitat: a, artificial; p, sheltered; e, wave-exposed; n.s., non significant. Asterisks indicate significant differences: * P < 0.05, ** P < 0.01. Table 7 ANOVA results of the abundance values of P. pusilla and C. scaura between artificial habitats located in its introduced (Western Mediterranean) and native range (southern Brazil). Abbreviations: n.s., non significant. Asterisks indicate significant differences: * P < 0.05. Figure legends Figure 1 Study area showing the four sampling localities in Brazil and the habitats surveyed in each locality at the native range of studied caprellid species. Figure 2 Non-transformed abundance nMDS plot for caprellid assemblages (habitat x locality interaction). Each point represents a replicate (n= 180). Figure 3 Mean (±SE) total caprellid abundance, species richness and abundance of four target species (fourth root individuals per 1, 000 ml of substrata) in each habitat type and each locality. Letters represent the SNK results done within the habitat x locality interaction (see Table 5). Asterisks indicate significant differences: * P < 0.05, ** P < 0.01 Figure 4 Relationship between the total caprellid abundance and average wave fetch in km. Spearman rank order correlation coefficient is reported for the total abundance per replicate (n=36). Asterisks indicate significant differences: * P < 0.05, ** P < 0.01 Figure 5 Mean (±SE) abundance of each caprellid species inhabiting the Eudendrium colonies collected in each habitat type from Paranaguá Bay; the bars represent Standard Error. References Ashton G, Davidson I, Ruiz G (2014) Transient small boats as a long-distance coastal vector for dispersal of biofouling organisms. Estuaries Coasts 37:1572–1581 Anderson MJ (2005) PERMANOVA: a FORTRAN computer program for permutational multivariate analysis of variance. Department of Statistics, University of Auckland, New Zealand 18 Anderson MJ, Legendre P (1999) An empirical comparison of permutation methods for tests of partial regression coefficients in a linear model. J Stat Comput Simul 62:271–303 Ayala Y, Martín A (2003) Relaciones entre la comunidad de anfípodos y las macroalgas a las que están asociados, en una plataforma rocosa del litoral central de Venezuela. Bol Inst Esp Oceanogr 19:171–183 Bavestrello G, Cerrano C, Cattaneo-Vietti R, Sara M (1996) Relations between Eudendrium glomeratum (Cnidaria, Hydromedusae) and its associated vagile fauna. Sci Mar 60:137–143 Bellan-Santini D, Ruffo S (1998) Faunistics and Zoogeography. In: Ruffo S (ed.) The Amphipoda of the Mediterranean, Part 4. Mémoires de l’Institut Océanographique (Monaco) 13:895–911 Boos K (2009) Mechanisms of a successful immigration from north-east Asia: population dynamics, life history traits and interspecific interactions in the caprellid amphipod Caprella mutica Schurin 1935 (Crustacea, Amphipoda) in European coastal waters. PhD Dissertation, Freie Universität Berlin, Berlin Bulleri F, Airoldi L (2005) Artificial marine structures facilitate the spread of nonindigenous green alga, Codium fragile ssp. tomentosoides, in the north Adriatic Sea. J Appl Ecol 42:1063–1072 Bulleri F, Chapman MG (2004) Intertidal assemblages on artificial and natural habitats in marinas on the north-west coast of Italy. Mar Biol 145:381–391 Burrows MT, Harvey R, Robb L (2008) Wave exposure indices from digital coastlines and the prediction of rocky shore community structure. Mar Ecol Prog Ser 353:1– 12 Buschbaum C, Gutow L (2005) Mass occurrence of an introduced crustacean (Caprella cf. mutica) in the south-eastern North Sea. Helg Mar Res 59:252–253 Byers JE (2002) Impact of non-indigenous species on natives enhanced by anthropogenic alteration of selection regimes. Oikos 94:449–458 Bynum KH (1980) Multivariate assessment of morphological variation in Caprella penantis Leach, 1814 (Amphipoda: Caprellidae). Estuar Coast Mar Sci 10:225–237 Caine EA (1989) Relationship between wave activity and robustness of caprellid amphipods. J Crust Biol 9:425–431 19 Carlton JT (1979) History, biogeography, and ecology of the introduced marine and estuarine invertebrates of the Pacific coast of North America. PhD Dissertation, University of California, CA Carlton JT (1996) Biological invasions and cryptogenic species. Ecology 77:1653–1655 Castro-Díez P, Godoy O, Saldana A, Richardson DM (2011) Predicting invasiveness of Australian acacias on the basis of their native climatic affinities, life history traits and human use. Divers Distrib 17:934–945 Chapman MG, People J, Blockley D (2005) Intertidal assemblages associated with natural Corallina turf and invasive mussel beds. Biodivers Conserv 14:1761–1776 Chavanich S, Harris LG, Je JG, Kang RS (2006) Distribution pattern of the green alga Codium fragile (Suringar) Hariot, 1889 in its native range, Korea. Aquat Invasions 1:99–108 Clarke KR, Gorley RN (2006) PRIMER v6: User manual/tutorial. PRIMER-e, Plymouth, UK, 192pp Cohen AN, Carlton JT (1998) Accelerating invasion rate in a highly invaded estuary. Science 279:555–557 Collin SB, Johnson EL (2014) Invasive species contribute to biotic resistance: negative effect of caprellid amphipods on an invasive tunicate. Biol Invasions 16:2209–2219 Connell SD, Glasby TM (1998) Do urban structures influence local abundances and diversity of subtidal epibiota? A case study from Sydney Harbour, Australia. Mar Environ Res 47:1–15 Crooks JA, Chang AL, Ruiz GM (2011) Aquatic pollution increases the relative success of invasive species. Biol Invasions 13:165–176 Daehler CC, DR Gordon (1997) To introduce or not to introduce: trade-offs of nonindigenous organisms. Trends Ecol Evol 12:424–425 Dana JD (1853) Crustacea Part II. United States Exploring Expedition 14:689–1618 Davidson TM, Hewitt CL, Campbell M (2008) Distribution, density, and habitat use among native and introduced populations of the Australasian burrowing isopod Sphaeroma quoianum. Biol Invasions 10:399–410 Davis AY, Malas N, Minor ES (2014) Substitutable habitats? The biophysical and anthropogenic drivers of an exotic bird’s distribution. Biol Invasions 16:415–427 20 Dean RL, Connell JH (1987) Marine invertebrates in algal succession. II. Tests of hypotheses to explain changes in diversity with succession. J Exp Mar Biol Ecol 109:217–247 Dumont CP, Harris LG, Gaymer CF (2011) Anthropogenic structures as a spatial refuge from predation for the invasive bryozoans Bugula neritina. Mar Ecol Prog Ser 427:95–103 Edgar GL (1983) The ecology of south-east Tasmanian phytal animal communities. III. Patterns of species diversities. J Exp Mar Biol Ecol 70:181–203 Fenwick GD (1976) The effect of wave exposure on the amphipod fauna of the alga Caulerpa brownii. J Exp Mar Biol Ecol 25:1–18 Forrest BM, Fletcher LM, Atalah J, Piola RF, Hopkins GA (2013) Predation Limits Spread of Didemnum vexillum into Natural Habitats from Refuges on Anthropogenic Structures. PloS one 8:e82229 Glasby TM, Connell SD, Holloway M, Hewitt C (2007) Nonindigenous biota on artificial structures: could habitat creation facilitate biological invasions? Mar Biol 151:887– 895 Gollasch S, Macdonald E, Belson S, Botnen H, Christensen JT, Hamer JP, Houvenaghel G, Jelmert A, Lucas I, Masson D, McCollin T, Olenin S, Persson A, Wallentinus I, Wetsteyn LPMJ, Wittling T (2002) Life in Ballast Tanks. In: Leppakoski E, Gollasch S, Olenin S (eds) Invasive Aquatic Species of Europe: Distribution, Impacts and Management. Kluwer Academic Publishers, Dordrecht, The Netherlands Gribben PE, Simpson M, Wrigh J (2015) Relationships between an invasive crab, habitat availability and intertidal community structure at biogeographic scales. Mar Environ Res 111:124–131 Guerra-García JM, García-Gómez JC (2001) The spatial distribution of Caprellidea (Crustacea: Amphipoda): a stress bioindicator in Ceuta (North Africa, Gibraltar area). Mar Ecol PSZNI 22:357–367 Guerra-García JM, Cabezas MP, Baeza-Rojano E, Espinosa F, García-Gómez J C (2009) Is the north side of the Strait of Gibraltar more diverse than the south side? A case study using the intertidal peracarids (Crustacea: Malacostraca) associated to the seaweed Corallina elongata. J Mar Biol Assoc UK 89:387–397 21 Guerra-García JM, Tierno de Figueroa JM (2009) What do caprellids (Crustacea: Amphipoda) feed on? Mar Biol 156:1881–1890 Guerra-García JM, Ros M, Gordillo I, Cabezas MP, Baeza-Rojano E, Izquierdo D, Corzo J, Domínguez J, Varona S (2010) Distribution patterns of intertidal and shallow water caprellids associated with macroalgae along the Iberian Peninsula. Zoologica baetica 21:101–109 Guo Q (2006) Intercontinental biotic invasions: what can we learn from native populations and habitats? Biol invasions 8:1451–1459 Hacker S, Steneck R (1990) Habitat architecture and the abundance and body-size- dependent habitat selection of a phytal amphipod. Ecology 71:2269–2285 Hejda M, Pyšek P, Pergl J, Sádlo J, Chytrý M, Jarošík V (2009) Invasion success of alien plants: do habitat affinities in the native distribution range matter? Global Ecol Biogeogr 18:372–382 Hierro J L, Maron JL, Callaway RM (2005) A biogeographical approach to plant invasions: the importance of studying exotics in their introduced and native range. J Ecol 93:5–15 Hill NA, Pepper AR, Puotinen ML, Hughes MG, Edgar GJ, Barrett NS, Stuart-Smith RD, Leaper R (2010) Quantifying wave exposure in shallow temperate reef systems: applicability of fetch models for predicting algal biodiversity. Mar Ecol Prog Ser 417:83–95 Howes DE, Harper JR, Owens EH (1994) Physical shore-zone mapping system for British Columbia. Technical Report by the Coastal Task Force of the Resource Inventory Committee (RIC), R. I. C. Secretariat. Victoria, B. C. 97pp Hui C, Richardson DM, Robertson MP, Wilson JRU, Yates CJ (2011) Macroecology meets invasion ecology: linking native distribution of Australian acacias to invasiveness. Divers Distrib 17:872–883 Johnston EL, Piola RF, Clark GF (2009) The role of propagule pressure in invasion success. In: Rilov G, Crooks JA (eds) Biological invasions of marine ecosystems: ecological, management and geographic perspectives. Springer, Heidelberg, pp 133–151 Keith DE (1971) Substrate selection in caprellid amphipods of Southern California with emphasis on Caprella californica Stimpson and Caprella equilibra Say (Amphipoda). Pac Sci 25:387–394 22 Lacerda BM, Masunari S (2011). Substrate selection of the caprellid Caprella dilatata (Crustacea, Amphipoda). Rev Biol Mar Oceanogr 46:207–218 Lewis JR (1964) The ecology of rocky shores. English Universities Press, London. Lohrer AM, Whitlatch RB, Wada K, Fukui Y (2000) Home and away: comparisons of resources utilization by a marine species in native and invaded habitats. Biol Invasions 2:41–57 Marins FO, Novaes RLM, Rocha RM, Junqueira AOR (2010) Non indigenous ascidians in port and natural environments in a tropical Brazilian bay. Zoologia (Curitiba) 27:213–221 Marzinelli EM, Zagal CJ, Chapman MG, Underwood AJ (2009) Do modified habitats have direct or indirect effects on epifauna? Ecology 90:2948–2955 McCain JC, Steinberg JE (1970) Amphipoda-I, Caprellidea-I. In: Gruner HE, Holthuis LB (eds.) Crustaceorum Catalogus 2:1–78 Megina C, González-Duarte MM, López-González PJ, Piraino S (2013) Harbours as marine habitats: hydroid assemblages on sea-walls compared with natural hábitats. Mar Biol 160:371–381 Navarro-Barranco C, Guerra-García JC, Sánchez-Tocino L, García-Gómez JC (2014) Mobile epifaunal community in marine caves in comparison to open habitats. Aquat Biol 20:101–109 Parker JD, Torchin ME, Hufbauer RA, Lemoine NP, Alba C, Blumenthal DM et al. (2013) Do invasive species perform better in their new ranges? Ecology 96:985– 994 People J (2006) Mussel beds on different types of structures support different macroinvertebrate assemblages. Austral Ecol 31:271–281 Preisler RK, Wasson K, Wolff W, Tyrrell MC (2009) Invasions of estuaries versus the adjacent open coast: a global perspective. In: Rilov G and Crooks JA (eds.) Biological invasions in marine ecosystems. Ecological, management, and geographic perspectives. Springer, Heidelbderg Piola RF, Johnston EL (2008) Pollution reduces native diversity and increases invader dominance in marine hard-substrate communities. Divers Distrib 14:329–342 Pyšek P, Jarošík V, Pergl J, Randall R, Chytrý M, Kühn I, Tichý L, Danihelka J, Chrtek J Jr, Sádlo J (2009) The global invasion success of Central European plants is 23 related to distribution characteristics in their native range and specie traits. Divers Distrib 15:891–903 Pyšek P, Jarošík V, Pergl J, Moravcová L, Chytrý M, Kühn I (2014) Temperate trees and shrubs as global invaders: the relationship between invasiveness and native distribution depends on biological traits. Biol Invasions 16:577–589 Rius M, Potter EE, Aguirre JD, Stachowicz J (2014) Mechanisms of biotic resistance across complex life cycles. J Anim Ecol 83:296–395 Ros M, Guerra-García, JM (2012) On the occurrence of the tropical caprellid Paracaprella pusilla Mayer, 1890 (Crustacea: Amphipoda) in Europe. Mediterr Mar Sci 13:134–139 Ros M, Vázquez-Luis M, Guerra-García JM (2013a) The role of marinas and recreational boating in the occurrence and distribution of exotic caprellids (Crustacea: Amphipoda) in the Western Mediterranean: Mallorca Island as a case study. J Sea Res 83:94–103 Ros M, Guerra-García JM., González-Macías M et al. (2013b) Influence of fouling communities on the establishment success of alien caprellids (Crustacea: Amphipoda) in Southern Spain. Mar Biol Res 9:293–305 Ros M, Guerra-García JM, Navarro-Barranco C, Cabezas MP, Vázquez-Luis M (2014a) The spreading of the non-native caprellid (Crustacea: Amphipoda) Caprella scaura Templeton, 1836 into southern Europe and northern Africa: a complicated taxonomic history. Mediterr Mar Sci 15:145–155 Ros M, Tierno de Figueroa M, Guerra-García JM, Navarro-Barranco C, Lacerda M, Vázquez-Luis M, Masunari S (2014b) Exploring trophic strategies of exotic caprellids (Crustacea: Amphipoda): comparison between habitat types and native vs introduced distribution ranges. Estuar Coast Shelf Sci 139:88–98 Ros M, Vázquez-Luis M, Guerra-García JM (2015) Environmental factors modulating the extent of impact in coastal invasions: The case of a widespread invasive caprellid (Crustacea: Amphipoda) in the Iberian Peninsula. Mar Poll Bull 98:247– 258 Ruiz GM, Freestone A, Fofonoff P, Simkanin C (2009) Habitat distribution and heterogeneity in marine invasion dynamics: the importance of hard substrate and artificial structure. In: Wahl W (ed) Marine Hard Bottom Communities: Patterns, 24 Dynamics, Diversity and Change. Springer Series: Ecological Studies, Springer- Verlag, Berlin Heidelberg, pp 321–332 Shucksmith R, Cook EJ, Hughes DJ, Burrows MT (2009) Competition between the nonnative amphipod Caprella mutica and two native species of caprellids Pseudoprotella phasma and Caprella linearis. J Mar Biol Assoc UK 89:1125–1132 Simkanin C, Davidson IC, Dower JF, Jamieson G, Therriault TW (2012) Anthropogenic structures and the infiltration of natural benthos by invasive ascidians. Mar Ecol 33:499–511 Simkanin C, Dower JF, Filip N, Jamieson G, Therriault TW (2013) Biotic resistance to the infiltration of natural benthic habitats: Examining the role of predation in the distribution of the invasive ascidian Botrylloides violaceus. J Exp Mar Biol Ecol 439:76–83 Southward AJ, Orton JH (1954) The effects of wave-action on the distribution and numbers of the commoner plants and animals living on the Plymouth breakwall. J Mar Biol Assoc UK 33:1–19 Takeuchi I, Yamakawa H, Fujiwara M (1990) The Caprellidea (Crustacea: Amphipoda) inhabiting the green alga Cladophora wrightiana: The influence of wave exposure on species composition. La mer 28:139–145 Teodoro AC, Duleba W, Gubitoso S, Prada SM, Lamparelli CC, Bevilacqua J E (2010) Analysis of foraminifera assemblages and sediment geochemical properties to characterise the environment near Araçá and Saco da Capela domestic sewage submarine outfalls of São Sebastião Channel, São Paulo State, Brazil. Mar Poll Bull 60:536–553 Thiel M, Guerra-García JM, Lancellotti DA, Vásquez N (2003) The distribution of littoral caprellids (Crustacea: Amphipoda: Caprellidea) along the Pacific coast of continental Chile. Rev Chil Hist Nat 76:203–218 Underwood AJ (1981) Structure of a rocky intertidal community in New South Wales: patterns of vertical distribution and seasonal changes. J Exp Mar Biol Ecol 51:57– 85 Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge: Cambridge University Press 31 Table 3 Table 4 Table 5 HABITAT Artificial structure Natural sheltered Natural wave-exposed CAPRELLID SPECIES BG L1 L2 L3 L4 L1 L2 L3 L4 L1 L2 L3 L4 Aciconula tridentata Guedes-Silva and Souza-Filho, 2013 I Caprella danilevskii Czerniavski, 1868 IV Caprella dilatata Krøyer, 1843 III Caprella equilibra Say, 1818 IV Caprella scaura Templeton, 1836 IV Paracaprella pusilla Mayer, 1890 IV Paracaprella dubiaski Lacerda and Masunari, 2014 I Pseudaeginella montoucheti (Quitete, 1971) I 1-100 Pseudaeginella sp. I 100-1000 Phtisica marina Slabber, 1769 III 1000-10000 > 10000 Source of variation df MS Pseudo-F P(perm) MS Pseudo-F P(perm) Abundance (non transformed) Composition (presence/absence) Habitat = Ha 2 45023.000 2.536 0.0232* 54293.000 7.350 0.007** Locality = Lo 3 15209.000 3.940 <0.001*** 16209.000 12.040 <0.001*** Site (Ha x Lo) 24 3863.000 3.830 <0.001*** 1346.000 5.530 <0.001*** Ha x Lo 6 17758.000 4.600 <0.001*** 7367.900 5.470 <0.001*** Residual 72 1009.400 243.340 PERMDISP (Ha) F = 68.718 (P < 0.001) F = 69.588 (P < 0.001) Pairwise testsa (Ha x Lo): L1: a = e ≠ p L1: a ≠ p ≠ e L2: a ≠ p ≠ e L2: a ≠ p ≠ e L3: a ≠ p = e L3: a ≠ p ≠ e L4: a = p ≠ e L4: a = p ≠ e aMonte Carlo P values were used in pairwise test due to low number of unique permutations (Anderson, 2005) Source of variation df MS F P MS F P MS F P F vs. Caprellid species richness Total caprellid abundance Paracaprella pusilla Habitat = Ha 2 33.400 3.200 0.113 6139419.570 1.940 0.224 652957.950 1.360 0.326 Ha x Lo Locality = Lo 3 4.230 5.130 0.007** 7446380.580 10.770 <0.001*** 4979842.400 5.210 0.007** Si (Ha x Lo) Site (Ha x Lo) 24 0.820 4.940 <0.001*** 678229.220 3.810 <0.001*** 7474288.000 1.410 0.136 Res Ha x Lo 6 10.440 12.660 <0.001*** 2772004.870 8.870 <0.001*** 9936895.310 5.010 0.002** Si (Ha x Lo) Residual = Res 72 0.170 5150241.490 6834781.560 Cochran's C-test C = 0.235 (P < 0.05) C = 0.685 (P < 0.01) C = 0.802 (P < 0.01) Transformation None None None Caprella scaura C. dilatata C. equilibra F vs. Habitat = Ha 2 12178.605 0.780 0.500 540361.340 0.160 0.856 6415941.840 1.590 0.279 Ha x Lo Locality = Lo 3 13001.820 17.41 <0.001*** 8159511.210 2.650 0.072 7082171.790 16.850 <0.001*** Si (Ha x Lo) Site (Ha x Lo) 24 746.928 3.620 <0.001*** 5711124.900 3.490 <0.001*** 8659940.990 1.790 0.031 Res Ha x Lo 6 15611.203 20.900 <0.001*** 4050002.520 6.380 <0.001*** 2534868.510 16.420 <0.001*** Si (Ha x Lo) Residual = Res 72 206.463 7366981.330 1180852.230 Cochran's C-test C = 0.189 (ns) C = 0.346 (P < 0.01) C = 0.634 (P < 0.01) Transformation Sqrt (X +1) None None 32 Table 6 Table 7 Source of variation df MS F P MS F P MS F P F vs. Paracaprella pusilla Caprella dilatata Caprellaequilibra F vs. Habitat = Ha 2 1264276.930 6.410 0.032* 4456550.480 8.850 0.001** 114770.010 6.630 0.030* Site (Ha) Site (Ha) 6 7081892.590 1.580 0.210 7719891.740 1.070 0.415 17317.960 3.500 0.018* Res Residual = Res 18 7533846.850 9054044.370 4919.970 Cochran's C-test C = 0.660 (P < 0.01) C = 0.516 (P < 0.05) C = 0.317 (ns) Transformation None None Sqrt (X + 1) SNK Ha: a > p = e Ha: a < p = e Ha: a > p = e F-value in bold was calculated with pooling of Site (Ha) becouse this source of variation showed a P >0.25 Source of variation df MS F P df MS F P F vs. Paracaprella pusilla Caprella scaura Range = Ra 1 7534380.080 9.000 0.013* 1 41197.393 15.600 0.017* Locality (Ra) Locality (Ra) 2 3110934.080 0.470 0.641 4 2641.375 2.460 0.102 Res Residual 8 3901057.080 12 1073.742 Cochran's C-test C = 0.529 (ns) C = 0.594 (ns) Transformation None Sqrt (X + 1) SNK Ra: Native > Introduced Ra: Native < Introuced F-value in bold was calculated with pooling of Locality (Ra) becouse this source of variation showed a P>0.25