Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Assemblage structure and trophic ecology of deep-sea demersal cephalopods in the Balearic basin (NW Mediterranean)

Emanuela Fanelli A B , Joan E. Cartes A and Vanesa Papiol A

A ICM-CSIC Institut de Cienciès del Mar, P.g Maritim de la Barceloneta 37-49, Barcelona 08003, Spain.

B Corresponding author. Email: efanelli@icm.csic.es

Marine and Freshwater Research 63(3) 264-274 http://dx.doi.org/10.1071/MF11157
Submitted: 5 July 2011  Accepted: 17 November 2011   Published: 22 December 2011

Abstract

Despite the important ecological role of cephalopods in energy and material flow in marine ecosystems, they are poorly understood, particularly those inhabiting deep-sea bottoms below 800 m. To define cephalopod species assemblages from the upper to the lower slope, we conducted 13 oceanographic and trawl surveys in the Balearic basin (NW Mediterranean) in 1985–92 and 2007–10 at depths between 450 and 2200 m. Multivariate analysis suggests the existence of three assemblages on the upper (450–600 m), middle (650–1500 m) and lower (1600–2200 m) slopes. Although seasonal changes in species abundance and composition were evident, no significant variations in the assemblage structure were observed between the two time periods. Two main trophic pathways involving deep-sea cephalopods were apparent: species mainly linked to benthic resources and species mostly connected to the pelagic food web through active swimming and frequent vertical migrations. Accordingly, two environmental variables best explained the observed patterns: net primary production and river discharge. Phytoplankton availability controls the increase of zooplankton that influences the distribution and abundance of pelagic cephalopods. River discharge affects, in some instances with delays, transfer of organic matter to the benthic trophic pathway and thus to bottom-dwelling cephalopods.

Additional keywords: bathymetric distribution, diversity, food web, long-term changes.


References

Anderson, M. J. (2006). Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62, 245–253.
Distance-based tests for homogeneity of multivariate dispersions.CrossRef | open url image1

Anderson, M. J., and Willis, T. J. (2003). Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84, 511–525.
Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology.CrossRef | open url image1

Anderson, M. J., Gorley, R. N., and Clarke, K. R. (2008). ‘PERMANOVA +for PRIMER: Guide to Software and Statistical Methods.’ (PRIMER-E: Plymouth, UK.)

Bello, G. (1996). Teuthophagous predators as collectors of oceanic cephalopods: the case of the Adriatic Sea. Bollettino Malacologico 32, 71–78. open url image1

Bello, G. (1997). Cephalopods from the stomach contents of demersal chondrichthyans caught in the Adriatic Sea. Vie et Milieu 47, 221–227. open url image1

Béthoux, J. P., and Gentili, B. (1999). Functioning of the Mediterranean Sea: past and present changes related to freshwater input and climate changes. Journal of Marine Systems 20, 33–47.
Functioning of the Mediterranean Sea: past and present changes related to freshwater input and climate changes.CrossRef | open url image1

Boyle, P. R., and Rodhouse, P. G. (2005). ‘Cephalopods: Ecology and Fisheries.’ (Blackwell Science Ltd: Oxford.)

Cartes, J. E., and Carrassón, M. (2004). The influence of trophic variables in the depth-range distribution and zonation rates of deep-sea megafauna: the case of the Western Mediterranean assemblages. Deep-sea Research. Part I, Oceanographic Research Papers 51, 263–279.
The influence of trophic variables in the depth-range distribution and zonation rates of deep-sea megafauna: the case of the Western Mediterranean assemblages.CrossRef | open url image1

Cartes, J. E., and Sardà, F. (1993). Zonation of the deep-sea decapod fauna in the Catalan Sea (Western Mediterranean). Marine Ecology Progress Series 94, 27–34.
Zonation of the deep-sea decapod fauna in the Catalan Sea (Western Mediterranean).CrossRef | open url image1

Cartes, J. E., Company, J. B., and Maynou, F. (1994). Deep-water decapod crustacean communities in the Northwestern Mediterranean: influence of submarine canyons and season. Marine Biology 120, 221–229.
Deep-water decapod crustacean communities in the Northwestern Mediterranean: influence of submarine canyons and season.CrossRef | open url image1

Cartes, J. E., Maynou, F., Moranta, J., Massuti, E., Lloris, D., and Morales-Nin, B. (2004). Patterns of bathymetric distribution among deep-sea fauna at local spatial scale: comparison of mainland vs. insular areas. Progress in Oceanography 60, 29–45.
Patterns of bathymetric distribution among deep-sea fauna at local spatial scale: comparison of mainland vs. insular areas.CrossRef | open url image1

Cartes, J. E., Maynou, F., Fanelli, E., Papiol, V., and Lloris, D. (2009). Long-term changes in the composition and diversity of deep-slope megabenthos and trophic webs off Catalonia (western Mediterranean): are trends related to climatic oscillations? Progress in Oceanography 82, 32–46.
Long-term changes in the composition and diversity of deep-slope megabenthos and trophic webs off Catalonia (western Mediterranean): are trends related to climatic oscillations?CrossRef | open url image1

Cartes, J. E., Maynou, F., Lloris, D., Gil de Sola, L., and Garcia, M. (2009). Influence of trawl type on the composition, and diversity of deep benthopelagic fish and decapod assemblages off the Catalan coasts (western Mediterranean). Scientia Marina 73, 725–737.
Influence of trawl type on the composition, and diversity of deep benthopelagic fish and decapod assemblages off the Catalan coasts (western Mediterranean).CrossRef | open url image1

Cartes, J. E., Maynou, F., Fanelli, E., Romano, C., Mamouridis, V., and Papiol, V. (2009). The distribution of megabenthic, invertebrate epifauna in the Balearic Basin (Western Mediterranean) between 400 and 2300 m: environmental gradients influencing assemblages composition and biomass trends. Journal of Sea Research 61, 244–257.
The distribution of megabenthic, invertebrate epifauna in the Balearic Basin (Western Mediterranean) between 400 and 2300 m: environmental gradients influencing assemblages composition and biomass trends.CrossRef | open url image1

Caut, S., Angulo, E., and Courchamp, F. (2009). Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. Journal of Applied Ecology 46, 443–453.
Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction.CrossRef | 1:CAS:528:DC%2BD1MXkslGgu7k%3D&md5=ba24fce7f41ccc1fce298ce33e7fc850CAS | open url image1

Cherel, Y., Ridoux, V., Spitz, J., and Richard, P. (2009). Stable isotopes document the trophic structure of a deep-sea cephalopod assemblage including giant octopod and giant squid. Biology Letters 5, 364–367.
Stable isotopes document the trophic structure of a deep-sea cephalopod assemblage including giant octopod and giant squid.CrossRef | 1:STN:280:DC%2BD1MzjsFylsw%3D%3D&md5=3c3fa2cd6cd0c75ad702614d0a990900CAS | open url image1

Clarke, K. R., and Warwick, R. M. (2001). ‘Change in Marine Communities: an Approach to Statistical Analysis and Interpretation.’ 2nd edn. (PRIMER-E: Plymouth, UK.)

DeNiro, M. J., and Epstein, S. (1978). Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42, 495–506.
Influence of diet on the distribution of carbon isotopes in animals.CrossRef | 1:CAS:528:DyaE1cXls1WrsbY%3D&md5=e847066f1990d2371d9319db95a11071CAS | open url image1

Etcheber, H., Relaxans, J. C., Beliard, M., Weber, O., Buscail, R., and Heussner, S. (1999). Distribution and quality of sedimentary organic matter on the Aquitanian margin (Bay of Biscay). Deep-sea Research. Part II, Topical Studies in Oceanography 46, 2249–2288.
Distribution and quality of sedimentary organic matter on the Aquitanian margin (Bay of Biscay).CrossRef | 1:CAS:528:DyaK1MXmtVSls7k%3D&md5=30c6cd83f36d652ee672bde23f50a8baCAS | open url image1

Fanelli, E., and Cartes, J. E. (2008). Spatio-temporal variability in the diet of two pandalid shrimps in the western Mediterranean: evidence from gut-contents and stable isotope analysis. Marine Ecology Progress Series 355, 219–233.
Spatio-temporal variability in the diet of two pandalid shrimps in the western Mediterranean: evidence from gut-contents and stable isotope analysis.CrossRef | open url image1

Fanelli, E., and Cartes, J. E. (2010). Temporal variations in the feeding habits and trophic levels of deep-sea demersal fish from the Western Mediterranean Sea based on stomach contents and stable isotope analyses. Marine Ecology Progress Series 402, 213–232.
Temporal variations in the feeding habits and trophic levels of deep-sea demersal fish from the Western Mediterranean Sea based on stomach contents and stable isotope analyses.CrossRef | open url image1

Fanelli, E., Cartes, J. E., Rumolo, P., and Sprovieri, M. (2009). Food web structure and trophodynamics of mesopelagic-suprabenthic deep sea macrofauna of the Algerian basin (Western Mediterranean) based on stable isotopes of carbon and nitrogen. Deep-sea Research. Part I, Oceanographic Research Papers 56, 1504–1520.
Food web structure and trophodynamics of mesopelagic-suprabenthic deep sea macrofauna of the Algerian basin (Western Mediterranean) based on stable isotopes of carbon and nitrogen.CrossRef | 1:CAS:528:DC%2BD1MXosVajsLg%3D&md5=047221f1d3b11efef9bbda01524d61feCAS | open url image1

Fanelli, E., Papiol, V., Cartes, J. E., Rumolo, P., Brunet, C., and Sprovieri, M. (2011). Food web structure of the megabenthic, invertebrate epifauna on the Catalan slope (NW Mediterranean): evidence from δ13C and δ15N analysis. Deep-sea Research. Part I, Oceanographic Research Papers 58, 98–109.
Food web structure of the megabenthic, invertebrate epifauna on the Catalan slope (NW Mediterranean): evidence from δ13C and δ15N analysis.CrossRef | 1:CAS:528:DC%2BC3MXhsVeqtbs%3D&md5=f1c923544f2434fb2cae838f3acc6203CAS | open url image1

Fanelli, E., Cartes, J. E., and Papiol, V. (2011). Trophodynamics of zooplankton fauna on the Catalan slope (NW Mediterranean): insight from δ13C and δ15N analysis. Journal of Marine Systems 87, 79–89.
Trophodynamics of zooplankton fauna on the Catalan slope (NW Mediterranean): insight from δ13C and δ15N analysis.CrossRef | open url image1

González, M., and Sánchez, P. (2002). Cephalopod assemblages caught by trawling along the Iberian Peninsula Mediterranean coast. Scientia Marina 66, 199–208. open url image1

Haedrich, R. L., Rowe, G. T., and Polloni, P. T. (1980). The megabenthic fauna in the deep sea south of New England, USA. Marine Biology 57, 165–179.
The megabenthic fauna in the deep sea south of New England, USA.CrossRef | open url image1

Hecker, B. (1990). Variation in megafaunal assemblages on the continental margin south of New England. Deep-sea Research. Part I, Oceanographic Research Papers 37, 37–57.
Variation in megafaunal assemblages on the continental margin south of New England.CrossRef | open url image1

Hyslop, E. J. (1980). Stomach content analysis: a review of methods and their application. Journal of Fish Biology 17, 411–429.
Stomach content analysis: a review of methods and their application.CrossRef | open url image1

Iken, K., Brey, T., Wand, U., Voigt, J., and Junghans, P. (2001). Trophic relationships in the benthic community at Porcupine Abyssal Plain (NE Atlantic): a stable isotope analysis. Progress in Oceanography 50, 383–405.
Trophic relationships in the benthic community at Porcupine Abyssal Plain (NE Atlantic): a stable isotope analysis.CrossRef | open url image1

Jackson, G. D., and Domeier, M. L. (2003). The effects of an extraordinary El niño/La niña event on the size and growth of the squid Loligo opalescens off Southern California. Marine Biology 142, 925–935. open url image1

Lampitt, R. S., Billett, D. S. M., and Rice, A. L. (1986). Biomass of the invertebrate megabenthos from 500–4100 m in the Northeast Atlantic Ocean. Marine Biology 93, 69–81.
Biomass of the invertebrate megabenthos from 500–4100 m in the Northeast Atlantic Ocean.CrossRef | open url image1

Layman, C. A., Winemiller, K. O. D., Arrington, A., and Epson, D. B. (2005). Body size and trophic position in a diverse food web. Ecology 86, 2530–2535.
Body size and trophic position in a diverse food web.CrossRef | open url image1

Lefkaditou, E., Mytilineou, C., Maiorano, P., and D’Onghia, G. (2003). Cephalopod species captured by deep-water exploratory trawling in the northeastern Ionian Sea. Fisheries Science 31, 431–440. open url image1

McArdle, B. H., and Anderson, M. J. (2001). Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82, 290–297.
Fitting multivariate models to community data: a comment on distance-based redundancy analysis.CrossRef | open url image1

Merrett, N. G., and Marshall, N. B. (1981). Observations on the ecology of deep-sea bottom-living fishes collected off northwest Africa (08°–27°N). Progress in Oceanography 9, 185–244.
Observations on the ecology of deep-sea bottom-living fishes collected off northwest Africa (08°–27°N).CrossRef | open url image1

Moiseev, S. I. (1991). Observation of the vertical distribution and behaviour of nektonic squids using manned submersibles. Bulletin of Marine Science 49, 446–456. open url image1

Molinero, J. C., Casini, M., and Buecher, E. (2008). The influence of the Atlantic and regional climate variability on the long-term changes in gelatinous carnivore populations in the northwestern Mediterranean. Limnology and Oceanography 53, 1456–1467.
The influence of the Atlantic and regional climate variability on the long-term changes in gelatinous carnivore populations in the northwestern Mediterranean.CrossRef | open url image1

Moranta, J., Stefanescu, C., Massutí, E., Morales-Nin, B., and Lloris, D. (1998). Fish community structure and depth-related trends on the continental slope of the Balearic Islands (Algerian basin, western Mediterranean). Marine Ecology Progress Series 171, 247–259.
Fish community structure and depth-related trends on the continental slope of the Balearic Islands (Algerian basin, western Mediterranean).CrossRef | open url image1

Owens, N. J. P. (1988). Natural variations in 15N in the marine environment. Advances in Marine Biology 24, 389–451.
Natural variations in 15N in the marine environment.CrossRef | open url image1

Phillips, D. L., and Gregg, J. W. (2003). Source partitioning using stable isotopes: coping with too many sources. Oecologia 136, 261–269.
Source partitioning using stable isotopes: coping with too many sources.CrossRef | open url image1

Piatkowski, U., Pierce, G. J., and Morais da Cunha, M. (2001). Impact of cephalopods in the food chain and their interaction with the environment and fisheries: an overview. Fisheries Research 52, 5–10.
Impact of cephalopods in the food chain and their interaction with the environment and fisheries: an overview.CrossRef | open url image1

Pierce, G. J., Boyle, P. R., Hastie, L. C., and Santos, M. B. (1994). Diets of squid Loligo forbesi and Loligo vulgaris in the northeast Atlantic. Fisheries Research 21, 149–163.
Diets of squid Loligo forbesi and Loligo vulgaris in the northeast Atlantic.CrossRef | open url image1

Pinkas, L., Oliphant, M. S., and Iverson, L. R. (1971). Food habits of albacore, bluefin tuna, and bonito in California waters. Fishery Bulletin 152, 1–105. open url image1

Polunin, N. V. C., Morales-Nin, B., Herod, W., Cartes, J. E., Pinnegar, J. K., and Moranta, J. (2001). Feeding relationships in Mediterranean bathyal assemblages elucidated by carbon and nitrogen stable-isotope data. Marine Ecology Progress Series 220, 13–23.
Feeding relationships in Mediterranean bathyal assemblages elucidated by carbon and nitrogen stable-isotope data.CrossRef | 1:CAS:528:DC%2BD3MXpt1Gqu7w%3D&md5=7fcc55add8a6ac83d2deed2ae47caf6eCAS | open url image1

Quetglas, A., Alemany, F., Carbonell, A., Merella, P., and Sánchez, P. (1999). Diet of the European flying squid Todarodes sagittatus (Cephalopoda: Ommastrephidae) in the Balearic Sea (western Mediterranean). Journal of the Marine Biological Association of the United Kingdom 79, 479–486.
Diet of the European flying squid Todarodes sagittatus (Cephalopoda: Ommastrephidae) in the Balearic Sea (western Mediterranean).CrossRef | open url image1

Quetglas, A., Carbonell, A., and Sánchez, P. (2000). Demersal continental shelf and upper slope cephalopod assemblages from the Balearic Sea (north-western Mediterranean). Biological aspects of some deep-sea species. Estuarine, Coastal and Shelf Science 50, 739–749.
Demersal continental shelf and upper slope cephalopod assemblages from the Balearic Sea (north-western Mediterranean). Biological aspects of some deep-sea species.CrossRef | open url image1

Quetglas, A., González, M., Carbonell, A., and Sánchez, P. (2001). Biology of the deep-sea octopus Bathypolypus sponsalis (Cephalopoda: Octopodidae) from the western Mediterranean Sea. Marine Biology 138, 785–792.
Biology of the deep-sea octopus Bathypolypus sponsalis (Cephalopoda: Octopodidae) from the western Mediterranean Sea.CrossRef | open url image1

Quetglas, A., González, M., and Franco, I. (2005). Biology of the upper-slope cephalopod Octopus salutii from the western Mediterranean Sea. Marine Biology 146, 1131–1138.
Biology of the upper-slope cephalopod Octopus salutii from the western Mediterranean Sea.CrossRef | open url image1

Quetglas, A., Ordines, F., González, M., and Franco, I. (2009). Life history of the bathyal octopus Pteroctopus tetracirrhus (Mollusca, Cephalopoda) in the Mediterranean Sea. Deep-sea Research. Part I, Oceanographic Research Papers 56, 1379–1390.
Life history of the bathyal octopus Pteroctopus tetracirrhus (Mollusca, Cephalopoda) in the Mediterranean Sea.CrossRef | open url image1

Rasero, M., Gonzalez, A. F., Castro, B. G., and Guerra, A. (1996). Predatory relationships of two sympatric squid, Todaropsis eblanae and Illex coindetii (Cephalopoda: Ommastrephidae) in Galician waters. Journal of the Marine Biological Association of the United Kingdom 76, 73–87.
Predatory relationships of two sympatric squid, Todaropsis eblanae and Illex coindetii (Cephalopoda: Ommastrephidae) in Galician waters.CrossRef | open url image1

Rex, M. A. (1977). Zonation in deep-sea gastropods: the importance of biological interactions to rates of zonation. In ‘Biology of Benthic Organisms’. (Eds B. F. Keegan, P. O. Ceidigh and P. J. S. Boaden.) pp. 521–530. (Pergamon Press: New York.)

Rodhouse, P. G., and Nigmatullin, C. M. (1996). Role as consumers. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 351, 1003–1022.
Role as consumers.CrossRef | open url image1

Roper, C. F. E., and Young, R. E. (1975). Vertical distribution of pelagic cephalopods. Smithsonian Contributions to Zoology 209, 1–51.
Vertical distribution of pelagic cephalopods.CrossRef | open url image1

Rowe, G. T. (1983). Biomass and production of the deep-sea macrobenthos. In ‘The Sea’. Vol. 8. (Ed. G. T. Rowe.) pp. 97–121. (Wiley Interscience: New York.)

Ruby, G., and Knudsen, J. (1972). Cephalopoda from the Eastern Mediterranean. Israel Journal of Zoology 21, 83–97. open url image1

Salman, A., Katagan, T., and Benli, H. A. (2002). Cephalopod fauna of the eastern Mediterranean. Turkish Journal of Zoology 26, 47–52. open url image1

Sánchez, P., Belcari, P., and Sartor, P. (1998). Composition and spatial distribution of cephalopods in two north-western Mediterranean areas. South African Journal of Marine Science 20, 17–24.
Composition and spatial distribution of cephalopods in two north-western Mediterranean areas.CrossRef | open url image1

Sartor, P., Belcari, P., Carbonell, A., González, M., Quetglas, A., and Sánchez, P. (1998). The importance of cephalopods to trawl fisheries in the western Mediterranean. South African Journal of Marine Science 20, 67–72.
The importance of cephalopods to trawl fisheries in the western Mediterranean.CrossRef | open url image1

Stefanescu, C., Lloris, D., and Rucabado, J. (1993). Deep-sea fish assemblages in the Catalan Sea (western Mediterranean) below a depth of 1000 m. Deep-sea Research. Part I, Oceanographic Research Papers 40, 695–707.
Deep-sea fish assemblages in the Catalan Sea (western Mediterranean) below a depth of 1000 m.CrossRef | open url image1

Underwood, A. J. (1997). ‘Experiments in Ecology: their Logical Design and Interpretation using Analysis of Variance.’ (Cambridge University Press: Cambridge, UK.)

Vanderklift, M. A., and Ponsard, S. (2003). Sources of variation in consumer-diet delta 15N enrichment: a meta-analysis. Oecologia 136, 169–182.
Sources of variation in consumer-diet delta 15N enrichment: a meta-analysis.CrossRef | open url image1

Vecchione, M., Young, R. E., and Piatkowski, U. (2010). Cephalopods of the northern Mid-Atlantic Ridge. Marine Biology Research 6, 25–52.
Cephalopods of the northern Mid-Atlantic Ridge.CrossRef | open url image1

Villanueva, R. (1992). Deep-sea cephalopods of the north-western Mediterranean: indications of up-slope ontogenic migration in two bathybenthic species. Journal of Zoology 227, 267–276.
Deep-sea cephalopods of the north-western Mediterranean: indications of up-slope ontogenic migration in two bathybenthic species.CrossRef | open url image1

Voight, J. R. (2000). A deep-sea octopus (Graneledone cf. boreopacifica) as a shell-crushing hydrothermal vent predator. Journal of Zoology 252, 335–341.
A deep-sea octopus (Graneledone cf. boreopacifica) as a shell-crushing hydrothermal vent predator.CrossRef | open url image1

Williams, N. (1998). The Mediterranean beckons to Europe’s oceanographers. Science 279, 483–484.
The Mediterranean beckons to Europe’s oceanographers.CrossRef | 1:CAS:528:DyaK1cXotVCqug%3D%3D&md5=0cf34e5ac227cfffd90a78013b6617ccCAS | open url image1

Wood, J. B. (2000). The natural history of Bathypolypus arcticus (Prosch), a deep-sea octopus. PhD Thesis, Dalhousie University, Halifax, Nova Scotia, Canada.

Würtz, M., Poggi, R., and Clarke, M. R. (1992). Cephalopods from the stomachs of a Risso’s dolphin (Grampus griseus) from the Mediterranean. Journal of the Marine Biological Association of the United Kingdom 72, 861–867.
Cephalopods from the stomachs of a Risso’s dolphin (Grampus griseus) from the Mediterranean.CrossRef | open url image1



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