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Full Text in Pdf Format Vol. 20: 101–109, 2014 AQUATIC BIOLOGY Published online February 6 doi: 10.3354/ab00551 Aquat Biol Mobile epifaunal community in marine caves in comparison to open habitats Carlos Navarro-Barranco1,*, José Manuel Guerra-García1, Luis Sánchez-Tocino2, José Carlos García-Gómez1 1Laboratorio de Biología Marina, Dpto. Zoología, Facultad de Biología, Universidad de Sevilla, Avda Reina Mercedes 6, 41012 Sevilla, Spain 2Departamento de Biología Animal, Facultad de Ciencias, Universidad de Granada, Campus Universitario de Fuentenueva, s/n., 18071 Granada, Spain ABSTRACT: Mobile epifauna is an essential component of rocky reef ecosystems. In spite of this and the great scientific interest that the study of marine caves has aroused in the last decades, lit- tle research has been conducted on the macrofauna associated with animal substrates in subma- rine caves. This study explores the main differences between marine caves and open habitats in terms of species composition and diversity patterns of epifaunal communities in 4 different shal- low marine caves in southern Spain. Colonies of Eudendrium sp., a marine hydroid widely distrib- uted in the Mediterranean Sea, were taken from inside and outside each cave, and all associated mobile fauna were sorted and identified. More than 90% of organisms were crustaceans, with Amphipoda as the dominant group. Although the main species did not vary significantly in abun- dance between open and cave habitats, multivariate analysis carried out for the entire amphipod community showed significant differences between these 2 habitats. nMDS analysis showed that marine cave assemblages were also characterized by a higher degree of individuality, and uni- variate analysis showed a decrease in Shannon diversity and species richness with distance into the caves, a consistent pattern for all caves studied. Although the possible role of predation pres- sure in the structure of such assemblages was also discussed, we propose that the absence of plant substrates inside the caves, in conjunction with oligotrophic conditions and low siltation, are the main factors responsible for the impoverishment of the epifaunal community. The near lack of photosynthetic activity reduced the presence of herbivorous species, while the rich detritus-feeder community supported by the animal substrates was limited by the low rate of sedimentation. KEY WORDS: Epifauna · Marine caves · Amphipods · Hydroids · Mediterranean Sea Resale or republication not permitted without written consent of the publisher INTRODUCTION term stability, similarity to the bathyal zone and pres- ence of strong environmental gradients on spatial Marine caves constitute a typical feature of the scales of only a few meters, marine caves have long Mediterranean coastline. Because of their high vul- been considered as environments of great taxonomic nerability and important role as a biodiversity reser- and ecologic interest (Vacelet et al. 1994, Benedetti- voir (Gerovasileiou & Voultsiadou 2012), marine cave Cecchi et al. 1997, Hiscock & Breckels 2007). Several habitats are protected by the European Community comparative studies have been done to explore the (Habitat Directive 92/43 EEC). Darkness is not the differences in distribution of organisms inside marine only peculiarity of this ecosystem; because of their caves versus open habitats (e.g. Zabala et al. 1989, isolation, lack of photosynthetic production, long- Harmelin 1997, Martí et al. 2004, Bussotti & Guidetti *Corresponding author: [email protected] © Inter-Research 2014 · www.int-res.com 102 Aquat Biol 20: 101–109, 2014 2009, Janssen et al. 2013). However, only a few of Cnidarian colonies can support a highly diverse these studies have taken into account the epifaunal epifaunal community, as has been shown in gorgon- community inhabiting animal or plant substrates ian gardens and scleractinian reefs (Stella et al. 2010, (Ledoyer 1966, True 1970, Scipione et al. 1981). Thus, Carvalho et al. 2014). Hydroids are also considered to this type of assemblage remains poorly known, be a foundation species of littoral communities in although it is essential to consider this part of the temperate habitats (Bavestrello et al. 1996). Simkina marine cave community in order to understand the (1980) pointed out that hydroid colonies can consti- behavior of these systems. Epifauna associated with tute the major regulators of zooplankton in some hard-bottom substrates are major contributors to the areas, playing an important role in the mass devel - flux of materials in rocky habitats, providing up to opment of copepod species. They also act as a food 99% of total secondary productivity, and acting as a supply for many species, such as nudibranchs and prey source for the majority and most productive amphipods (Bavestrello et al. 1996). Moreover, spe- demersal fishes (Taylor 1998a, Edgar & Aoki 1993). cific studies have highlighted the biodiversity in - However, they have usually been excluded in trophic crease of epifauna in rocky habitats when hydroid models (Taylor 1997). colonies were present (Bradshaw et al. 2003). Euden- Although a decrease in species richness, diversity drium is a common and widely distributed hydroid and coverage of benthic organisms is a well-known genus in both natural and polluted Mediterranean phenomenon in the inner part of marine caves environments, forming large arborescent colonies (Zabala et al. 1989, Bussotti et al. 2006), the existence which support a rich community of sessile and mobile of the same pattern for the epifaunal community has epibiontic organisms (Bavestrello et al. 1996, Romag- not been tested. The presence of sessile species has a noli et al. 2007, Di Camillo et al. 2008). Among its positive effect on the diversity of associated assem- mobile epifauna, crustaceans (mainly copepods and blages, which is evident when we compare them to amphipods) comprise more than 90% of individuals bare rock and sedimentary environments (Chapman (Bavestrello et al. 1996); a common feature in most et al. 2005, Birdsey et al. 2012). Thus, one could benthic substrates and habitats (and also inside mar- expect that because of the oligotrophic conditions ine caves) (Martin-Smith 1993, Taylor 1997, Fredrik- and high percentage of bare substrate in these habi- sen et al. 2005, Guerra-García et al. 2011, Navarro- tats, caves might support a poor assemblage of Barranco et al. 2012). Because of their abundance, mobile organisms. However, the decline in competi- ubiquity, importance in the structure of benthic tion for substrate by algae in the semi-dark areas of assemblages and sensitivity to environmental changes, marine caves often allows for the development of a amphipod crustaceans are often used as a model rich and heterogeneous community dominated by group in ecological studies (Sánchez-Moyano & sessile invertebrates (Bussotti et al. 2006). García-Gómez 1998, Duffy & Hay 2000, Guerra-García With respect to differences in species composition, & García-Gómez 2001). obviously if the benthic community is different be - The main objective of this study was to explore the tween marine caves and open habitats, the associ- ecological patterns that characterize mobile epifau- ated epifauna will likely also differ (Birdsey et al. nal communities in marine caves. For that, we used 2012). Previous studies have highlighted how the amphipod community associated with Euden- macroinfauna associated with soft sediments inside drium sp. as a model, studying the possible existence marine caves was different from those present out- of differences in the abundance, number of species, side them (Bamber et al. 2008, Navarro-Barranco et diversity and species composition in the epifauna al. 2013). However, it is difficult to establish how associated with hard-bottom communities between many of those differences in community are due to marine caves and open habitats. habitat, because of the presence of confounding fac- tors such as changes in the granulometry or the chemical properties of the sediment. Thus, in the MATERIALS AND METHODS present study we explore the mobile organisms asso- ciated with Eudendrium sp. (Cnidaria, Hydrozoa), a Study site and sampling collection substrate present in both habitats (semi-dark and open). By using the same substrate, we can identify Four shallow marine caves were selected and sam- the extent the environment (and not the change of pled between 20 and 28 August 2012 in La Her- substrate) plays in determining changes in epifaunal radura (southern Spain): ‘Cueva de la Punta del composition and biodiversity patterns. Vapor’ (36°43’22’’N, 3°42’35’’W), ‘Cueva del Jarro’ Navarro-Barranco et al.: Epifaunal community in marine caves 103 (36°43’11’N, 3°43’48’W), ‘Cueva de los Gigantes’ the power of the statistical analysis (Huitema 2011, (36°43’20’’N, 3°44’08’’W), and ‘Cueva de Cerro- Quinn & Keough 2002). Heterogeneity of variance Gordo’ (33°43’46’’N, 3°45’56’’W). All of these caves was checked using Cochran’s test, and transforma- are shallow (samples were taken between 6 and 12 m tions were applied when necessary (Underwood deep) and showed a similar topography in their semi- 1997). When variances remained heterogeneous, dark areas. Two sampling stations were selected in untransformed data were analyzed, as ANOVA is each location: one in the exterior area (approximately robust enough to support conclusions based on this 5 m outside the cave mouth) and another inside the assumption—particularly in a balanced design with cave. The abundance of Eudendrium sp. decreases in sufficient replicates (Underwood 1997). In such the inner part of the caves, being absent in the com- cases, special care was taken in the interpretation pletely dark areas. Therefore, the cave samples were of results, and in order to reduce Type I errors, the taken in the semi-dark area (approximately 10 m level of significance was reduced to 0.01. Prior to from the entrance), where the abundance of Euden- analysis, heterogeneity of slopes was also tested by drium sp. remains similar to that present outside the crossing the covariate with the interaction of the caves. Although the distance between the 2 stations other 2 factors and checking for significant inter - in each cave was only ca.
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