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Amphipods from marine cave sediments of the southern Iberian Peninsula: diversity and ecological distribution

Carlos Navarro-Barranco 1, José Manuel Guerra-García 1, Luis Sánchez-Tocino 2,
José Carlos García-Gómez 1

1 Laboratorio de Biología Marina, Dpto. Zoología, Facultad de Biología, Universidad de Sevilla. Avda Reina Mercedes 6, 41012 Sevilla, Spain. E-mail: carlosnavarro@us.es
2 Departamento de Biología Animal, Facultad de Ciencias, Universidad de Granada. Campus Universitario de Fuentenueva, s/n., 18071 Granada, Spain.

Summary: The present study explores the amphipod assemblages of six marine caves on the Mediterranean coast of southern Spain. Replicate samples were taken both inside and outside each marine cave in order to characterize the amphipod fauna and the physicochemical properties of the sediment. As a result, 44 amphipods species were identified. The high number of species found in a relatively limited area highlighted the richness of the Alboran Sea fauna, which is mainly due to the mixture of species from different biogeographic areas. Harpinia genus was the dominant amphipod taxa inside marine caves and Perioculodes longimanus was also very abundant in the caverns. On the other hand, external communities were dominated by Siphonoecetes sabatieri, Metaphoxus fultoni and Photis longipes. There was a high degree of variability in both the internal and the external stations. Only the external station situated at low-medium depth showed a relatively homogeneous amphipod assemblage. The structure and behaviour of soft-bottom communities inside marine caves is difficult to predict because their environmental conditions depend on a particular combination of factors such as topography, depth and orientation. Therefore, no constant patterns were observed for species richness, Shannon diversity and abundance of amphipods in marine caves in comparison with open habitats. According to canonical correspondence analysis, sediment granulometry, organic matter and nitrogen concentration were the parameters that best explained the distribution of amphipods. Species were also classified by their tolerance to environmental pollution according to criteria followed by the Azti Marine Biotic Index and the BENTIX index. The great abundance of sensitive species at both the internal and external stations indicates the good ecological quality of the soft bottom studied. However, the suitability of biotic indices in marine caves should be tested in future studies.

Keywords: marine caves; soft-bottom communities; Amphipoda; benthic ecology; Mediterranean Sea.

Anfípodos en sedimentos de cuevas submarinas del Sur de la Península Ibérica: diversidad y distribución ecológica

Resumen: En el presente trabajo se estudia la fauna de anfípodos presente en el sustrato blando de seis cuevas submarinas de la costa Mediterránea del sur de España. Con el objetivo de caracterizar tanto la comunidad biótica como las características físico-químicas del sedimento, se tomaron muestras de sedimento a la salida y en el interior de las cuevas submarinas. Como resultado, se identificaron un total de cuarenta y cuatro especies de anfípodos diferentes. Este elevado número de especies encontrado en un área relativamente limitada pone de manifiesto la riqueza faunística del Mar de Alborán, la cual se atribuye principalmente a la mezcla de especies de diferentes áreas biogeográficas. El género Harpinia fue el taxón dominante en el interior de las cuevas, junto con Perioculodes longimanus. Por otro lado, la comunidad en las zonas externas estaba dominada por Siphonoecetes sabatieri, Metaphoxus fultoni y Photis longipes. Se observó un alto grado de variabilidad tanto en las estaciones internas como externas. Solo las estaciones externas situadas a profundidades bajas-medias mostraron una fauna relativamente homogénea. La estructura y el comportamiento de las comunidades que habitan los sustratos blandos en el interior de cuevas submarinas es difícil de predecir, ya que las condiciones ambientales dependen de sus particulares características en cuanto a topografía, profundidad y orientación. Por ello, no ha podido extraerse ningún patrón constante de la comparación de comunidades internas y externas para el número de especies, diversidad de Shannon o abundancia de anfípodos. La granulometría y los porcentajes de materia orgánica y nitrógeno en el sedimento fueron los parámetros que mejor explicaban la distribución de los anfípodos, de acuerdo con los resultados del análisis CCA. Las especies también fueron clasificadas en base a su tolerancia a la polución ambiental, siguiendo los criterios establecidos por los índices AMBI y BENTIX. La gran abundancia de especies sensibles refleja el buen estado ecológico de los sedimentos estudiados. Sin embargo, la aplicabilidad de los índices bióticos en cuevas submarinas debería ser testada en futuros estudios.

Palabras clave: cuevas submarinas; comunidades de sustrato blando; Amphipoda; ecología bentónica, mar Mediterráneo.

Citation/Como citar este artículo: Navarro-Barranco C., Guerra-García J.M., Sánchez-Tocino L., García-Gómez J.C. 2014. Amphipods from marine cave sediments of the southern Iberian Peninsula: diversity and ecological distribution. Sci. Mar. 78(3): 000-000. doi: http://dx.doi.org/10.3989/scimar.04043.28E

Editor: J.S. Troncoso.

Received: February 25, 2014. Accepted: May 28, 2014. Published: July 28, 2014.

Copyright: © 2014 CSIC. This is an open-access article distributed under the Creative Commons Attribution-Non Commercial Lisence (by-nc) Spain 3.0.

Contents

Summary
Resumen
Introduction
Materials and methods
Results
Discussion
Acknowledgements
References

INTRODUCTIONTop

Marine caves support diverse and distinctive communities, often acting as biodiversity reservoirs for many marine groups (Riedl 1966Riedl R. 1966. Biologie der Meereshöhlen. Verlag Paul Parey, Hamburg and Berlin, 702 pp., Gerovasileiou and Voutsiadou 2012Gerovasileiou V., Voultsiadou E. 2012. Marine caves of the Mediterranean Sea: a sponge biodiversity reservoir within a biodiversity hotspot. PLoS ONE, 7 (7), e39873. ). Because of the importance and peculiarity of these communities, marine caves are also an interesting environment to conduct biological studies. However, in the last few years there has been an increase in the evidence of impact by human activities on cave communities, including alterations by scuba diving activities, coastal pollution and global warming (Chevaldonné and Lejeusne 2003Chevaldonné P., Lejeusne C. 2003. Regional warming-induced species shift in north-west Mediterranean marine caves. Ecol. Lett. 6: 371-379., Di Franco et al. 2010Di Franco A., Milazzo M., Baiata P., et al. 2010. Can recreational scuba divers alter natural gross sedimentation rate? A case study from a Mediterranean deep cave. ICES J. Mar. Sci. 67: 871-874., Parravicini et al. 2010Parravicini V., Guidetti P., Morri C., et al. 2010. Consequences of sea water temperature anomalies on a Mediterranean submarine cave ecosystem. Est. Coast. Shelf Sci. 86: 276-282., Guarnieri et al. 2012Guarnieri G., Terlizzi A., Bevilacqua S., et al 2012. Increasing heterogeneity of sensitive assemblages as a consequence of human impact in submarine caves. Mar. Biol. 159: 1155-1164.). Owing to their high natural stability, these ecosystems show low resilience and a high vulnerability to disturbances (Vacelet et al. 1994Vacelet J., Boury-Esnault N., Harmelin J.G. 1994. Hexactinellid cave, a unique deep-sea habitat in the scuba zone. Deep-Sea Res. 41 (7): 965-973.), so they are considered as priority conservation areas according to Directive 92/43/EEC of the European Community and there is an urgent need to understand their biodiversity and organization. Though many ecological and taxonomical studies have been conducted in marine caves, their soft-bottom communities have often been overlooked. The sediment assemblages inhabiting marine caves often show a distinctive species composition and usually hold many new and endemic species (Bamber et al. 2008Bamber R.N., Evans N.J., Robbins R.S. 2008. The marine soft-sediment benthic communities of Hong Kong: a comparison of submarine cave and open habitats. J. Nat. Hist. 42(9): 953-965.; Horton 2008Horton T. 2008. Amphipoda from marine caves of Hong Kong Island. J. Nat. Hist. 42(9-12): 825-854.). Within them, crustaceans (and mainly amphipods) are the dominant taxa in both abundance and number of individuals (Navarro-Barranco et al. 2012Navarro-Barranco C., Guerra-García J.M., Sánchez-Tocino L., et al. 2012. Soft-bottom crustacean assemblages in Mediterranean marine caves: the cave of Cerro Gordo (Granada, Spain) as case study. Helgol. Mar. Res. 66(4): 567-576.).

In recent years, and especially since the establishment of the European Water Framework Directive (WFD), many biotic indices for evaluating the environmental quality of estuarine and coastal waters have been developed. To evaluate the suitability of these biotic indices it is necessary to test their effectiveness in different regions and environments, and against different types of impact (Diaz et al. 2004Diaz R.J., Solan M., Valente R.M. 2004. A review of approaches for classifying benthic habitats and evaluating habitat quality. J. Environ. Manage. 73: 165-181., Borja et al. 2009Borja A., Miles A., Occhipinti-Ambrogi A., et al. 2009. Current status of macroinvertebrate methods used for assessing the quality of European marine waters: implementing the Water Framework Directive. Hydrobiologia 633: 181-196.). They have not yet been tested in marine caves.

Given the sensitivity of most amphipods to different kinds of pollution, their abundance, their ecological importance, their relatively low mobility and their close relation with the sediment, they are often considered as good ecological indicators (Gómez-Gesteira and Dauvin 2000Gómez-Gesteira J.L., Dauvin J.C. 2000. Amphipods are good bioindicators of the impact of oil spills on soft-bottom macrobenthic communities. Mar. Pollut. Bull. 40: 1017-1027., Guerra-García and García-Gómez 2001Guerra-García J.M., García-Gómez J.C. 2001. The spatial distribution of Caprellidea (Crustacea: Amphipoda): a stress bioindicator in Ceuta (North Africa, Gibraltar area). PSZN Mar. Ecol. 22: 357-367., de-la-Ossa-Carretero et al. 2011de-la-Ossa-Carretero J.A., Del-Pilar-Ruso Y., Giménez-Casalduero F., et al. 2011. Sensitivity of amphipods to sewage pollution. Est. Coast. Shelf Sci. 96(1): 129-138.). They are therefore used by many indices (e.g. AMBI, BENTIX, MEDOCC and BOPA) to establish the environmental quality of coastal soft-bottom communities (Borja et al. 2000Borja A., Franco J., Pérez V. 2000. A marine biotic index to establish the ecological quality of soft-bottom benthos within European estuarine and coastal environments. Mar. Pollut. Bull. 40: 1100-1114., Simboura and Zenetos 2002Simboura N., Zenetos A. 2002. Benthic indicators to use in ecological quality classification of Mediterranean soft bottom marine ecosystems, including a new biotic index. Med. Mar. Sci. 3(2): 77-111., Pinedo and Jordana 2007Pinedo S., Jordana E. 2007. Spain (Catalonia and Balearic Islands). In: Carletti A., Heiskanen A.S. (eds), Water Framework Directive Intercalibration Technical Report Part 3: Coastal and Transitional waters. JRC Scientific and Technical Reports, JRC and IES, pp. 62-70, Dauvin and Ruellet 2007Dauvin J.C., Ruellet T. 2007. Polychaete/amphipod ratio revisited. Mar. Pollut. Bull. 55: 215-224.). However, it is essential to know the environmental preferences and tolerances of each taxon, as discrepancies about the assignation of the same species to different ecological groups contribute to variations in the results obtained with each index (de-la-Ossa-Carretero et al. 2011de-la-Ossa-Carretero J.A., Del-Pilar-Ruso Y., Giménez-Casalduero F., et al. 2011. Sensitivity of amphipods to sewage pollution. Est. Coast. Shelf Sci. 96(1): 129-138., Pinedo et al. 2012Pinedo S., Jordana E., Salas F., et al. 2012. Testing MEDOCC and BOPA indices in shallow softbottom communities in the Spanish Mediterranean coastal waters. Ecol. Indic. 19: 98-105.). Marine caves are therefore suitable places to conduct these studies, since small-scale topographic variability within them generates sharp environmental gradients, allowing a great spatial heterogeneity of environmental conditions and benthic assemblages.

Finally, the patterns in presence of taxa among different marine caves are also of great biogeographic interest. Marine caves are usually considered as islands supporting isolated populations. The existence of species with disjunct distributions in distant marine caves raises questions about how these species can keep their metapopulation dynamics. It has been suggested that a stepping stones model, with larvae moving passively from one cryptic habitat to another, was plausible for some cases (Manconi et al. 2006Manconi R., Serusi A., Pisera A. 2006. A new Mediterranean ‘lithistid’ sponge, Aciculites mediterranea sp. nov. (Porifera, Demospongiae) from a dark marine cave in Sardinia. J. Mar. Biol. Assoc. UK. 86: 691-698., 2009Manconi R, Ledda F.D, Serusi A, et al. 2009. Sponges of marine caves: Notes on the status of the Mediterranean palaeoendemic Petrobiona massiliana (Porifera: Calcarea: Lithonida) with new records from Sardinia. Ital. J. Zool. 76(3): 306-315.). Recent discoveries highlight that these cave-exclusive species are often deep-water species that have denser populations in bathyal areas but are also able to colonize shallow cavernicolous habitats (Bakran-Petricioli et al. 2007Bakran-Petricioli T., Vacelet J., Zibrowius H., et al. 2007. New data on the distribution of the ‘deep-sea’ sponges Asbestopluma hypogea and Oopsacas minuta in the Mediterranean Sea. Mar. Ecol. 28(1): 10-23.). All these aspects have often been investigated in taxa with free-swimming larvae such as sponges and bryozoans (Vacelet et al. 1994Vacelet J., Boury-Esnault N., Harmelin J.G. 1994. Hexactinellid cave, a unique deep-sea habitat in the scuba zone. Deep-Sea Res. 41 (7): 965-973., Harmelin 1997Harmelin J.G. 1997. Diversity of bryozoans in a Mediterranean sublittoral cave with bathyal-like conditions; role of dispersal processes and local factors. Mar. Ecol. Prog. Ser. 153: 139-152.). Organisms with a direct development and relatively low dispersion capabilities, such as amphipods, can be expected to show different patterns. All previous studies of peracarid crustaceans of marine caves correspond to taxonomic studies focusing on single marine caves. Therefore, the ability of amphipods to colonize these habitats and the extent to which marine caves are isolated habitats for these organisms with low mobility have not been tested yet.

The main objective of this article is to study the whole soft-bottom amphipod community from submarines caves of southern Spain in order to characterize their unexplored diversity, their distributional patterns and their environmental requirements.

MATERIALS AND METHODSTop

Study site and sampling collection

Our study locations were situated along the coast of Granada (Mediterranean coast of southern Spain). This area is characterized by the abundance of cliffs composed of carbonate rocks, which allow the presence of many marine caves. Six caves were studied: Cueva de Calahonda (36°42’46”N, 3°22’18”W), Cueva de la Punta del Vapor (36°43’22”N, 3°42’35”W), Raja de la Mona (36°43’10”N, 3°44’6”W), Cueva de los Treinta Metros (36°43’12”N, 3°44’9”W), Cueva de Cantarriján (36°44’16”N, 3°46’41”W) and Cueva de las Gorgonias (36°44’17”N, 46°46’42”W) (see also Navarro-Barranco et al. 2013). All of them show a similar topographic profile, with a single submerged entrance followed by a rectilinear blind-ending tunnel. These locations comprise a wide range of depth (from 6 to 32 m deep) and a heterogeneous granulometry (from coarse sand to predominantly muddy sediments).

During July and August 2011, two stations were established and sampled at each location, one inside the cave and one in the exterior area (each one approximately 10 m from the cave entrance). Seven replicate samples were taken at each station using a hand-held rectangular core of 0.025 m2 to a depth of 10 cm by SCUBA diving. Three of these samples were immediately frozen for physicochemical characterization of each station. Granulometric parameters were determined following the methodology proposed by Guitián and Carballas (1976)Guitián F., Carballas T. 1976. Técnicas de análisis de suelos, 2nd ed. Pico Sacro, Santiago de Compostela, 276 pp.. Organic matter and major, minor and trace element concentrations in sediments were determined following the methodology presented in Navarro-Barranco et al. (2012)Navarro-Barranco C., Guerra-García J.M., Sánchez-Tocino L., et al. 2012. Soft-bottom crustacean assemblages in Mediterranean marine caves: the cave of Cerro Gordo (Granada, Spain) as case study. Helgol. Mar. Res. 66(4): 567-576.. Four replicate samples were used for the biological study of the soft-bottom community. Samples were sieved through a 0.5-mm mesh sieve and preserved in 70% ethanol stained with Rose Bengal. In the laboratory, all amphipod species were sorted, counted and identified to species level when possible using binocular microscopes.

Data analysis

Mean values ± standard deviation (SD) of number of species, total abundance, Shannon-Wiener diversity index (Shannon-Weaver 1963Shannon C.E., Weaver N. 1963. The Mathematical Theory of Communication. University of Illinois Press, Urbana, 111 pp.) and abundance of each amphipod species were calculated for each station. Differences between external and internal stations for these indices were tested using an analysis of variance (ANOVA) with two factors: Position (Po) and Site (Si). Po was a fixed factor with two levels (internal and external stations). Si was a fixed factor, orthogonal with Po, with six levels (each marine cave). Four samples were considered in each position (n=4). Prior to analysis, homogeneity of variances was checked using Cochran’s test and transformations were applied when necessary (Underwood 1997Underwood A.J. 1997. Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge, 504 pp.). A preliminary correlation analysis was done to determine which chemical variables were highly correlated with each other (p<0.05) and these were eliminated from later analyses to reduce the number of variables considered. Correlation analyses were also done to evaluate the relationship between environmental (depth, granulometry and chemical data) and biological variables (abundance, species richness and Shannon diversity). A permutational analysis of multivariate dispersions (PERMDISP) was carried out to test differences in the variation of the amphipod community between internal and external habitats. Finally, the relationships between environmental variables and the amphipod species were explored by a canonical correspondence analysis (CCA). The species with very low abundances (those with five or fewer individuals) were not included in the analysis.

Univariate analyses were performed using the GMAV5 program (Underwood et al. 2002Underwood A.J., Chapman M.G., Richards S.A. 2002. GMAV-5 for Windows. An Analysis of Variance Programme. University of Sydney, Australia.) for ANOVA and the SPSS.15 program for the correlations. CCA was carried out using the PC-ORD program (McCune and Mefford 1997McCune B., Mefford M.J. 1997. PC-ORD. Multivariate scaling. Sage Publications, Beverly Hills, California, 60 pp.), and the PRIMER v.6 + PERMANOVA package (Clarke and Gorley 2001Clarke K.R., Gorley R.N. 2001. PRIMER (Plymouth Routines in Multivariate Ecological Research) v5: User Manual/Tutorial. PRIMER-E Ltd., Plymouth, 91 pp.) was used for PERMDISP.

Species were classified in ecological groups in function of their sensitivity to contamination, following the criteria of the Azti Marine Biotic Index (AMBI) and the BENTIX index and classification lists (Borja et al. 2000Borja A., Franco J., Pérez V. 2000. A marine biotic index to establish the ecological quality of soft-bottom benthos within European estuarine and coastal environments. Mar. Pollut. Bull. 40: 1100-1114., Simboura and Zenetos, 2002Simboura N., Zenetos A. 2002. Benthic indicators to use in ecological quality classification of Mediterranean soft bottom marine ecosystems, including a new biotic index. Med. Mar. Sci. 3(2): 77-111.). Both indices are among the most widely used and require classification to species level. AMBI is the most applied index and classifies the amphipods into three groups: sensitive, indifferent and tolerant species. On the other hand, BENTIX is a biotic index specifically designed for the Mediterranean Sea and only discriminates between sensitive and tolerant species, including the indifferent species (those always present in low densities and with no significant variations in time) in the sensitive group. The percentage of species belonging to each group was calculated for internal and external stations.

Species were also assigned to different biogeographic regions on the basis of information and classifications in Ruffo (1982-1998)Ruffo S. 1982-1998. The Amphipoda of the Mediterranean: Parts 1–4. Mém. Inst. Océanogr. Monaco 13: 1-959., Conradi and López-González (1999)Conradi M., López-Gónzalez P.J. 1999. The benthic Gammaridea (Crustacea, Amphipoda) fauna of Algeciras Bay (Strait of Gibraltar): distributional ecology and some biogeographical considerations. Helgol. Mar. Res. 53: 2-8., Guerra-García et al. (2009)Guerra-García J.M., Cabezas P., Baeza-Rojano E., et al. 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(2): 387-397. and the World Register of Marine Species (WoRMS) (www.marinespecies.org). The following groups were established:

Mediterranean endemic
Mediterranean and Atlantic Ocean
Mediterranean, Atlantic and Indo-Pacific Ocean
Mediterranean, Atlantic and Arctic Ocean
Cosmopolitan

RESULTSTop

Forty-four different species were found in the whole study, belonging to 36 genera and 21 families (Fig. 1). At the external stations, amphipod assemblages were greatly dominated by Siphonoecetes sabatieri de Rouville, 1894, which comprised 68% of all individuals. The second most dominant species, Metaphoxus fultoni (Scott, 1890), showed much lower abundances, with 5% of the individuals. Inside the caves, the community was dominated by the genus Harpinia. Four of the seven most abundant species belongs to this genus: H. pectinata Sars, 1891, H. crenulata (Boeck, 1871), H. antennaria Meinert, 1890 and H. ala Karaman, 1987, in order of importance. Perioculodes longimanus (Bate and Westwood, 1868), with 20% of the individuals, was also very abundant at the internal stations.

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Fig. 1.Mean abundance (ind/m2) of the amphipod species at each sampling station.

According to univariate analyses, there were significant differences between external and internal stations in abundance, species richness and diversity (Fig. 2, Table 1). Although external stations often showed higher values in these parameters, no constant pattern was observed and ANOVA also determined that the factor Site and the interaction between the two factors (Po × Si) were significant (Table 1). However, the differences between positions were not significant for all the stations, and at some of them we found the opposite pattern, with higher values at the internal stations.

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Fig. 2. – Mean values ± SD of abundance of individuals, number of species and Shannon-Wiener diversity index for each sampling station. Significance of differences between positions is also represented. **, p<0.01; n.s., non significant.

Table 1. – Results of the two-factor ANOVA for abundance of individuals, species richness and Shannon-Wiener diversity. No transformations were necessary for diversity and abundance values. Species richness data were Ln(x) transformed; df, degrees of freedom; MS, mean square; p, level of significance; **, p<0.01; ***, p<0.001.

Abundance Species richness Shannon diversity
Source of variation df MS F p MS F p MS F p
Position = Po 1 223996.7 71.71 0.000*** 4.83 47.71 0.000*** 1.53 10.25 0.003**
Site = Si 5 8468.4 27.11 0.000*** 0.71 6.98 0.000*** 1.07 7.19 0.000***
Po × Si 5 125268.1 40.10 0.000*** 0.51 4.98 0.001** 1.27 8.50 0.000***
Residual 36 3123.7 0.10 0.15

The results of physicochemical variables are summarized in Table 2 and Figure 3. Correlation analyses conducted with chemical analysis helped to reduce the number of variables from 23 to 7: organic matter, P, N, Cu, Pb, S and Cr. Pb had a significant correlation (p<0.01) with As, Li and Zn. S was correlated (p<0.01) with B, Ca, Cd, Na and Sr, while Cr showed a strong correlation (p<0.01) with Al, N, Ba, Co, Fe, K, Mn, Ni, V and Zn. There were no significant correlations among the environmental variables and the abundance, species richness and diversity values.

Table 2. – Depth and mean values obtained for sediment variables at each sampling station. OM, organic matter. Depth was measured in meters, OM and N in percentage and the rest of elements in mg/kg.

Depth(m) OM(%) N(%) Al As B Ba Ca Cd Co Cr Cu Fe
Gorgonias Internal 6 0.84 0.04 18182.04 5.48 12.34 71.09 82963.75 0.10 8.37 24.48 12.15 18508.70
External 6 0.23 0.01 16669.01 4.58 3.93 61.91 49322.88 0.04 8.36 23.74 9.73 19074.20
Cantarriján Internal 8 0.74 0.02 18055.49 4.93 7.26 66.72 58619.00 0.17 8.64 24.94 12.31 19826.50
External 8 0.18 0.01 13712.99 4.72 3.06 42.09 47420.27 0.05 8.54 21.88 11.37 19404.90
Pta. Vapor Internal 12 0.76 0.05 24960.49 7.26 13.85 150.46 79923.38 0.06 13.66 43.98 15.39 29750.81
External 12 0.44 0.02 26043.12 5.65 7.11 172.97 53089.43 0.04 14.41 49.91 11.68 32208.23
Calahonda Internal 19 0.98 0.07 17663.12 7.39 10.77 41.82 60199.82 0.10 10.47 21.55 17.42 25212.95
External 19 0.40 0.03 6591.39 7.18 8.23 10.82 81739.77 0.11 7.00 9.73 7.86 17163.00
Treinta Metros Internal 30 1.86 0.12 25053.40 7.88 21.50 91.95 71626.79 0.14 11.27 35.18 19.02 25701.81
External 30 1.95 0.17 25902.39 7.28 17.17 61.46 67604.02 0.24 10.38 28.37 10.10 4456.48
Raja Mona Internal 32 0.79 0.08 3822.23 3.34 41.35 24.42 289776.85 0.23 1.77 6.12 9.81 4139.20
External 32 0.56 0.04 2834.40 3.41 43.64 22.33 303190.25 0.23 1.17 4.76 2.75 3374.96
Depth(m) K Li Mn Na Ni P Pb S Sr V Zn
Gorgonias Internal 6 5975.69 19.93 249.14 6003.37 17.02 448.49 9.27 1400.19 513.62 41.06 41.39
External 6 4526.50 18.02 253.69 3144.54 15.64 281.04 8.39 420.12 165.68 39.23 32.40
Cantarriján Internal 8 5336.79 18.73 261.27 4728.77 16.78 363.08 8.77 837.93 244.49 42.18 38.26
External 8 3385.46 15.73 236.45 2914.77 17.42 283.52 9.63 347.02 141.56 35.92 37.02
Pta. Vapor Internal 12 9896.94 21.78 426.01 4819.90 27.59 639.36 11.94 1582.53 611.31 65.18 90.92
External 12 10845.45 20.76 406.45 3609.38 27.63 408.11 7.81 818.66 427.42 70.55 65.29
Calahonda Internal 19 3759.01 33.44 263.56 5443.29 24.09 778.70 16.36 1140.75 342.73 38.75 75.40
External 19 1401.77 16.13 200.43 4755.77 17.19 506.33 9.05 999.94 579.19 22.38 44.03
Treinta Metros Internal 30 7746.73 30.80 279.39 7011.72 27.02 786.90 18.56 2049.61 523.70 54.44 79.19
External 30 5867.30 20.12 205.02 8306.28 20.00 579.36 15.38 3294.29 865.00 54.13 65.21
Raja Mona Internal 32 2047.58 5.46 105.88 6642.80 5.32 545.62 7.97 4071.12 3248.41 10.48 25.53
External 32 1779.27 4.24 102.48 8241.84 4.23 570.48 8.39 3895.80 3774.16 8.36 24.32

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Fig. 3. – Percentage of the different granulometric fractions at each sampling station.

According to CCA results (Fig. 4, Table 3), 59.4% of the total variation can be explained by measured environmental variables. The eigenvalues obtained for the three axes are fairly high, implying that these axes represent a strong gradient. All the environmental variables used in the analysis correlated significantly with at least one of the three axes. Axis 1 explained 21.1% of the species variance and was strongly correlated with the percentage of silt and clay, organic matter and nitrogen. The second axis, mainly associated negatively with the percentage of coarse sand and the concentration of sulfur, explained 19.5% of the species variance. The majority of stations, and hence also the species, are fairly separated in the graph (Fig. 4). Only the stations of Gorgonias, Cantarrijan, Punta del Vapor and Calahonda were closer in the graph, while the other two external stations (the deepest ones) were fairly separated. There was no clear separation between internal and external stations. PERMDISP analysis showed no significant differences in the variability between external and internal stations (F=0.32; p=0.61). CCA also showed the existence of some groups of species with a very similar relation to the environmental variables. One of them enclosed the species associated with the shallow and medium-depth external stations, including Siphonoecetes sabatieri, Bathyporeia guilliamsoniana (Bate, 1857), Pariambus tipicus (Krøyer, 1884) and Metaphoxus fultoni. On the other hand, the external station of Raja de la Mona showed a very characteristic community, with many species, such as Jassa sp. and Leptocheirus hirsutimanus (Bate, 1862), only present at this station. Besides being the deepest station, the peculiarity of this sampling point is due to the high percentage of coarse sand and gravels. The rest of the species were dispersed in the graph. Species of the Harpinia genus were always closely associated with internal stations but separated between those with higher abundances in muddy sediments (Harpinia antennaria or Harpinia crenulata) and those present in coarse sands (Harpinia ala and Harpinia sp.).

sm4043fig4.jpg

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Fig. 4. – Graphic representation of the stations, species and environmental variables with respect to the first two axes of the canonical correspondence analysis (CCA). SC (silt and clay), CS (coarse sand), OM (organic matter), Dp (depth), As (Ampelisca sp.), Bs (Bathyporeia sp.), Bg (Bathyporeia guilliamsoniana), Dg (Deflexilodes griseus), Gf (Gammarella fucicola), Ha (Harpinia antennaria), Hc (Harpinia crenulata), Hp (Hippomedon massiliensis), Hl (Harpinia ala), Hs (Harpinia sp.), Js (Jassa sp.), Lb (Lembos sp.), Lh (Leptocheirus hirsutimanus), Lp (Leptocheirus pectinatus), Ls (Leucothoe sp.), Ma (Microdeutopus algicola), Mf (Metaphoxus fultoni), Mm (Megaluropus monasteriensis), Ms (cf. Melita sp.), Pa (Pontocrates arenarius), Ph (Photis longipes), Pk, (Pseudolirius kroyeri), Pl (Perioculodes longimanus), Pm (Phtisica marina), Pt (Pariambus tipicus), Ss (Siphonoecetes sabatieri), Ue (Urothoe elegans).

Table 3. – Summary of the results of the CCA analysis. Only the variables that correlated with the first three axes were included. *, p<0.05; **, p<0.01; ***, p<0.001.

Axis 1 Axis 2 Axis 3
Eigenvalue 0.88 0.81 0.78
Species-environment correlation 1 1 1
Percentage of species variance 21.1 19.5 18.8
Correlation with environmental variables
OM (organic matter) (%) 0.90*** - –0.61*
N (%) 0.87*** - –0.60*
Cr (mg/kg) - - –0.55*
Cu (mg/kg) 0.56* 0.65* –0.59*
P (mg/kg) 0.80** - -
Pb (mg/kg) 0.85** - –0.76**
S (mg/kg) - –0.73** -
CS (coarse sand) (%) - –0.82*** -
SC (silt and clay) (%) 0.82*** - –0.63*
Depth (m) –0.61* –0.60* -

Species in the Atlantic-Mediterranean group were the majority (61.8%), followed by the Mediterranean endemic group (20.6%) (Fig. 5). The percentage of species belonging to each ecological group showed no great variations between stations, being clearly dominated by sensitive species at both external and internal stations (Fig. 6). The use of either the AMBI or the BENTIX biotic index does not seem to have a great influence on the results, since in both cases sensitive species were also dominant. However, though BENTIX includes the indifferent species as sensitive, the percentage of tolerant species was higher with this index.

sm4043fig5.jpg

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Fig. 5. – Percentage of recorded taxa belonging to the following groups of geographical distribution. I, Mediterranean endemic; II, Mediterranean and Atlantic Ocean; III, Mediterranean, Atlantic and Indo-Pacific Ocean; IV, Mediterranean, Atlantic and Artic Ocean; V, Cosmopolitan.

sm4043fig6.jpg

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Fig. 6. – Percentage of species belonging to ecological groups in function of their tolerance to environmental pollution.

DISCUSSIONTop

Internal vs external stations

Traditionally, the diversity impoverishment of cave faunas has been a widely accepted pattern. This fact was explained by the reduced trophic supply inside submarine caves (Zabala et al. 1989Zabala M., Riera T., Gili J.M., et al. 1989. Water flow, trophic depletion, and benthic macrofauna impoverishment in a submarine cave from the western Mediterranean. Mar. Ecol. 10: 271-287., Fichez 1990Fichez R. 1990. Decrease in allochthonous organic inputs in dark submarine caves, connection with lowering in benthic community richness. Hydrobiologia. 207: 61-69.). However, in recent years quantitative studies conducted simultaneously in different caves have highlighted the difficulty of finding general and consistent patterns in marine cave communities (Bussotti et al. 2006Bussotti S., Terlizzi A., Fraschetti S., et al. 2006. Spatial and temporal variability of sessile benthos in shallow Mediterranean marine caves. Mar. Ecol. Prog. Ser. 325: 109-119., Navarro-Barranco et al. 2013Navarro-Barranco C., Guerra-García J.M., Sánchez-Tocino L., et al. 2013. Soft bottom diversity patterns in marine caves; Lessons from crustacean community. J. Exp. Mar. Biol. Ecol. 446: 22-28.). In the present study, mean values of abundance, species richness and Shannon diversity were higher at external stations. However, although this trend has been observed in most studies of marine caves, it cannot be considered as a constant pattern. The finer sediments inside caves are often more stable and show a higher concentration of organic matter, often allowing the existence of complex and rich soft-bottom communities. For example, internal stations of the Cantarrijan cave showed abundances of amphipods more than ten times higher than external stations because of an unusually high density of Harpinia pectinata. We found another exception to the general pattern in Punta del Vapor, where samples showed lower diversity values at external stations, mainly because of the overwhelming numerical dominance of Siphonoecetes sabatieri. This lack of general patterns is not surprising. Despite their apparent environmental homogeneity, marine caves often show high variability because many complex mechanisms, both physical and biological, structure the soft-bottom communities (e.g. Morrisey et al. 1992Morrisey D.J., Howitt L., Underwood A.J., et al. 1992. Spatial variation in soft sediments benthos. Mar. Ecol. Prog. Ser. 81: 197-204., Snelgrove 1998Snelgrove P.V.R. 1998. The biodiversity of macrofaunal organisms in marine sediments. Biodivers. Conserv. 7: 1123-1132., Norén and Lindegarth 2005Norén K., Lindegarth M. 2005. Spatial, temporal and interactive variability of infauna in Swedish coastal sediments. J. Exp. Mar. Biol. Ecol. 317: 53-68.). Moreover, each marine cave has particular environmental conditions determined by features such as its topography, depth and orientation. As a result, the behaviour of the soft-bottom communities inside marine caves is difficult to predict.

Most of the species found inside the caves were also present at external stations. Among the species only found at external stations, some of them seemed to show a special avoidance of cave habitats. Siphonoecetes sabatieri, Urothoe elegans (Bate, 1857) and Pontocrates arenarius (Bate, 1858) are some of the species with a wider distribution in the study, being present in most of the sampling areas but with no single individual inside the caves. On the other hand, some species, such as Microdeutopus algicola Della Valle, 1893, Liljeborgia sp. and Gammarella fucicola (Leach, 1814), were only present at internal stations. Anyway, none of the species found in the present study are cave-exclusive, having all been previously cited in open habitats (Ruffo 1982-1998Ruffo S. 1982-1998. The Amphipoda of the Mediterranean: Parts 1–4. Mém. Inst. Océanogr. Monaco 13: 1-959.). This is a common feature in marine cave fauna, since most of the species only use the caverns for shelter and can also be found outside the caves in similar habitats (Scipione et al. 1981Scipione M.B., Taramelli E., Fresi E., et al. 1981. Distribuzione delle biocenosi bentoniche lungo un gradiente di luce in una grotta marina superficiale: Anfipodi. Memorie di Biologia Marina e di Oceanografia. 11(1): 1-16., Gerovasileiou and Voultsiadou 2012Gerovasileiou V., Voultsiadou E. 2012. Marine caves of the Mediterranean Sea: a sponge biodiversity reservoir within a biodiversity hotspot. PLoS ONE, 7 (7), e39873. ). The genus Harpinia, for example, was found predominantly inside marine caves, but was also present at some external stations, thus facilitating intercommunication among cave assemblages. Therefore, amphipod cave communities are not as isolated as could be expected, and the stepping stones model can probably be used to understand their population dynamics.

Biogeographical considerations

It was difficult to compare the diversity results obtained in the present study with those found in shallow soft-bottoms habitats of other localities of the Iberian Peninsula, since there is a great variation among studies in the sampling methodology (number of samples, degree of spatial and temporal replication, etc). Studies carried out in the Atlantic zone of the Iberian Peninsula found between 34 and 79 different amphipod species in the northwestern area (Cunha et al. 1999Cunha M.R., Sorbe J.C., Moreira M.H. 1999. Spatial and seasonal changes of brackish peracaridan assemblages and their relation to some environmental variables in two tidal channels of the Ria de Aveiro (NW Portugal). Mar. Ecol. Prog. Ser. 190: 69-87., Lourido et al. 2008Lourido A., Moreira J., Troncoso J.S. 2008. Assemblages of peracarid crustaceans in subtidal sediments from the Ría de Aldán (Galicia, NW Spain). Helgol. Mar. Res. 62: 289-301., Moreira et al. 2008Moreira J., Gestoso L., Troncoso J.S. 2008. Diversity and temporal variation of peracarid fauna (Crustacea: Peracarida) in the sallow subtidal of a sandy beach: Playa América (Galicia, NW Spain). Mar. Ecol. 29 (1): 12-18., Cacabelos et al. 2010Cacabelos E., Lourido A., Troncoso J.S. 2010. Composition and distribution of subtidal and intertidal crustacean assemblages in soft-bottoms of the Ria de Vigo (NW Spain). Sci. Mar. 74(3): 455-464.) and 93 species on the southern Portuguese coast (Carvalho et al. 2012Carvalho S., Cunha M.R., Pereira F., et al. 2012. The effect of depth and sediment type on the spatial distribution of shallow soft-bottom amphipods along the southern Portuguese coast. Helgol. Mar. Res. 66 (4): 489-501.). On the other hand, in the Mediterranean area, an inventory of soft-bottom amphipods from the east coast of the Iberian Peninsula revealed the presence of 55 different species (de-la-Ossa-Carretero et al. 2010de-la-Ossa-Carretero J.A., Dauvin J.C., Del-Pilar-Ruso Y., et al. 2010. Inventory of benthic amphipods from fine sand community of the Iberian Peninsula east coast (Spain), western Mediterranean, with new records. Mar. Biod. Rec. 3: 1-10.). This value is slightly higher than that found in the present work. However, taking into account the huge differences in the sampling effort between these two studies (40 stations along 250 km of coast were sampled during five consecutive years in the east coast study), the total amphipod species richness in shallow sediments could be expected to be higher in the Alboran Sea area. The relevance and high diversity of the Alboran Sea in comparison with other Mediterranean areas, mainly owing to the overlap of Atlantic and Mediterranean faunas, has already been reported (Guerra-García et al. 2009Guerra-García J.M., Cabezas P., Baeza-Rojano E., et al. 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(2): 387-397.). In this sense, only in the sediments of Ceuta Harbour and Algeciras Bay (both of them in the Strait of Gibraltar), 44 and 55 amphipod species were collected, respectively, by Conradi and López-Gónzalez (1999)Conradi M., López-Gónzalez P.J. 1999. The benthic Gammaridea (Crustacea, Amphipoda) fauna of Algeciras Bay (Strait of Gibraltar): distributional ecology and some biogeographical considerations. Helgol. Mar. Res. 53: 2-8. and Guerra-García and García-Gómez (2004)Guerra-García J.M., García-Gómez J.C. 2004. Crustacean assemblages and sediment pollution in an exceptional case study: a harbour with two opposing entrances. Crustaceana 77(3): 353-370.. Moreover, the existence of several upwelling areas in the littoral of southern Spain may also contribute to the high biological richness of this area (Delgado 1990Delgado M. 1990. Phytoplankton distribution along the Spanish coast of the Alboran Sea. Sci. Mar. 54(2): 169-178.).

Most of the species found have a wide range of distribution, present in more than one biogeographical region. However, only one species, Ampelisca brevicornis (Costa, 1853), can be considered cosmopolitan. The percentage of Mediterranean endemism (20.6%) was similar to that obtained in previous amphipod studies in the Strait of Gibraltar area (Conradi and López-Gónzalez 1999Conradi M., López-Gónzalez P.J. 1999. The benthic Gammaridea (Crustacea, Amphipoda) fauna of Algeciras Bay (Strait of Gibraltar): distributional ecology and some biogeographical considerations. Helgol. Mar. Res. 53: 2-8., Guerra-García et al. 2009Guerra-García J.M., Cabezas P., Baeza-Rojano E., et al. 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(2): 387-397.), but surprisingly higher than that obtained on the east coast of the Iberian Peninsula (12.7%) (de-la-Ossa-Carretero et al. 2010de-la-Ossa-Carretero J.A., Dauvin J.C., Del-Pilar-Ruso Y., et al. 2010. Inventory of benthic amphipods from fine sand community of the Iberian Peninsula east coast (Spain), western Mediterranean, with new records. Mar. Biod. Rec. 3: 1-10.).

Ecological quality and environmental preferences

All the variables included in the CCA were significant but sediment granulometry, organic matter and N concentration were the main parameters explaining the distribution of amphipods; this finding is a common feature in soft-bottom ecology studies (Pearson and Rosenberg 1978Pearson T.H., Rosenberg R. 1978. Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Oceanogr. Mar. Biol. 16: 229-311., Carvalho et al. 2012Carvalho S., Cunha M.R., Pereira F., et al. 2012. The effect of depth and sediment type on the spatial distribution of shallow soft-bottom amphipods along the southern Portuguese coast. Helgol. Mar. Res. 66 (4): 489-501.).

Regarding the ecological quality of the communities studied, the high abundance of sensitive species indicated the good state of the assemblages. The chemical data obtained agree with that conclusion, since almost all the values at all stations were far below the highest reference values tolerated in marine sediment quality guidelines (Grimwood and Dixon 1997Grimwood M.J., Dixon E. 1997. Assessment of risks posed by List II metals to Sensitive Marine Areas (SMAs) and adequacy of existing environmental quality standars (EQSs) for SMA protection. Report to English Nature., Long et al. 1998Long E.R., Field L.J., MacDonald D.D. 1998. Predicting toxicity in marine sediments with numerical sediment quality guidelines. Environ. Toxicol. Chem. 17: 714-727.). Thus, because of the lack of polluted stations, it is not possible for us to evaluate the suitability of the indices for detecting the anthropogenic impacts in marine caves. Although axis 1 in the CCA correlated significantly with the concentration of organic matter, N, P, Pb and Cu, this first axis does not represent a pollution gradient, since the concentration of heavy metals and the organic enrichment levels was not very high at any station. The rise in these concentrations is associated with the increase (mainly at internal stations) in the percentage of silt and clay, which have a higher capacity to retain elements. The a priori tolerant species, such as Gammarella fucicola, Pariambus typicus and Leptocheirus hirsutimanus, appear separated in the CCA. However, another way to evaluate the suitability of the indices is to analyse the level of agreement between results obtained by different indices (Borja and Dauer 2008Borja A., Dauer D.M. 2008. Assessing the environmental quality status in estuarine and coastal systems: comparing methodologies and indices. Ecol. Ind. 8: 331-337.). In this case, both indices showed similar results for the percentage of sensitive species and BENTIX showed slightly higher results for tolerant species. These small differences were due to some discrepancies in the assignment of ecological groups for some species. The caprellid Phtisica marina Slabber, 1769, for example, is classified as tolerant by BENTIX and sensitive by AMBI. The analysis of the ecology of soft-bottom caprellids in Southern Spain carried out by Guerra-García and García-Gómez (2001)Guerra-García J.M., García-Gómez J.C. 2001. The spatial distribution of Caprellidea (Crustacea: Amphipoda): a stress bioindicator in Ceuta (North Africa, Gibraltar area). PSZN Mar. Ecol. 22: 357-367. and Guerra-García et al. (2012)Guerra-García J.M., Navarro-Barranco C., Corzo J., et al. 2012. An illustrated key to the soft-bottom caprellids (Crustacea: Amphipoda) of the Iberian Peninsula and remarks to their ecological distribution along the Andalusian coast. Helgol. Mar. Res. 67(2): 321-336. supports the BENTIX classification, since it is able to tolerate conditions of high organic enrichment and low oxygen concentrations. The gammarid Perioculodes longimanus is considered a tolerant species by AMBI and a sensitive one by BENTIX. P. longimanus was present at most of the stations, regardless of the granulometry, depth or position (external or internal). Its abundance at these stations with high ecological quality was often very high, suggesting that P. longimanus should probably be considered an indifferent species in the AMBI’s list of species. Other discrepancies between indices occur for the gammarids Pontocrates arenarius, Leptocheirus pectinatus (Norman, 1869) and Microdeutopus algicola. However, since all our stations showed a good state of conservation and some of these species were in very low densities, we were unable to discriminate the tolerance of these species. The study area is subjected to a low anthropogenic influence and some of the caves are even inside a marine protected area (Rodriguez et al. 2003Rodriguez J., Molina F., Rodriguez M. 2003. Paraje Natural de los Acantilados de Maro-Cerro Gordo: nueva ZEPIM. Medio Ambiente 43: 16-19.). Future studies involving marine caves with a higher gradient of pollution stress would be very useful to properly evaluate the tolerances of different taxa and the suitability of biotic indices in marine caves.

ACKNOWLEDGEMENTSTop

Financial support for this work was provided by the Ministerio de Economía y Competitividad (Project CGL 2011-22474, internal reference 2011-707). It was co-financed by FEDER funds of the European Union and by the Consejería de Economía, Innovación, Ciencia y Empleo, Junta de Andalucía (Project P11-RNM-7041). Special thanks to Sara Cea and Pablo Jiménez-Prada for their help in the sorting the organisms and to two anonymous reviewers for their very helpful comments. This work is part of C.N-B’s PhD thesis, supported by the University of Seville (PIF Grant).

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