North-East Atlantic; DNA molecular analysis; Diet composition; Benthic invertebrates; Crustacean decapods; Trophic ecology; Gut content DNA metabarcoding
Abstract :
[en] While many studies have analyzed the diet of marine consumers using traditional morphology-based methods, the integral diet of many species of functionally important groups such as benthic invertebrates remains poorly resolved. This hinders our ability to precisely establish trophic links among species, which is necessary to understand food webs and ecosystem dynamics. Here, we applied DNA metabarcoding to obtain a high resolution picture of the animal fraction of the diet of six species of crustaceans in the Bay of Biscay; the edible crab Cancer pagurus, the velvet crab Necora puber, the circular crab Atelecyclus undecimdentatus, the spider crab Maja brachydactyla, the shrimp Crangon crangon, and the hermit crab Pagurus bernhardus. We used two pairs of primers targeting the 18S rDNA (generalist) and 12S rDNA (fish-specific) regions to identify prey that makes up the animal fraction of the diet. Based on occurrence data, 54 prey taxa belonging to 5 different phylum mostly represented by teleost fishes and malacostracans were identified. Through a high-level of prey detection, results indicate a scavenging strategy across all consumers mostly based on the consumption of preys likely originating from fishing discards. This study also reveals patterns of niche overlaps among consumers differentiating C. crangon from others and suggesting high overlap in animal resource use between N. puber and M. brachydactyla as well as C. pagurus. High resolution diet description revealed the complexity of trophic interactions on a local scale.
Lejeune, Benjamin ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Laboratoire d'Écologie et de Conservation des Amphibiens (LECA)
Language :
English
Title :
Gut content metabarcoding of six crustaceans provides detailed diet description and insights into their roles as predators and scavengers
Amaral, V., Paula, J., Hawkins, S., Jenkins, S., Cannibalistic interactions in two co-occurring decapod species: effects of density, food, alternative prey and habitat. J. Exp. Mar. Biol. Ecol. 368 (2009), 88–93, 10.1016/j.jembe.2008.10.025.
Anderson, M.J., Ellingsen, K.E., McArdle, B.H., Multivariate dispersion as a measure of beta diversity. Ecol. Lett. 9 (2006), 683–693, 10.1111/j.1461-0248.2006.00926.x.
Ansell, A.D., Comely, C.A., Robb, L., Distribution, movements and diet of macrocrustaceans on a Scottish sandy beach with particular reference to predation on juvenile fishes. Mar. Ecol. Prog. Ser. 176 (1999), 115–130, 10.3354/meps176115.
Asahida, T., Yamashita, Y., Kobayashi, T., Identification of consumed stone flounder, Kareius bicoloratus (Basilewsky), from the stomach contents of sand shrimp, Crangon affinis (De Haan) using mitochondrial DNA analysis. J. Exp. Mar. Biol. Ecol. 217 (1997), 153–163, 10.1016/S0022-0981(97)00039-7.
Bailey, K.M., Predation on juvenile flatfish and recruitment variability. Neth. J. Sea Res. 32 (1994), 175–189, 10.1016/0077-7579(94)90039-6.
Baker, R., Buckland, A., Sheaves, M., Fish gut content analysis: robust measures of diet composition. Fish Fish. 15 (2014), 170–177, 10.1111/faf.12026.
Beasley, J.C., Olson, Z.H., Devault, T.L., Carrion cycling in food webs: comparisons among terrestrial and marine ecosystems. Oikos 121 (2012), 1021–1026, 10.1111/j.1600-0706.2012.20353.x.
Beauchesne, D., Cazelles, K., Archambault, P., Dee, L.E., Gravel, D., On the sensitivity of food webs to multiple stressors. Ecol. Lett. 24 (2021), 2219–2237, 10.1111/ele.13841.
Bergmann, M., Wieczorek, S.K., Moore, P.G., Atkinson, R.J.A., Utilisation of invertebrates discarded from the Nephrops fishery by variously selective benthic scavengers in the west of Scotland. Mar. Ecol. Prog. Ser. 233 (2002), 185–198, 10.3354/meps233185.
Bernárdez, C., Freire, J., González-Gurriarán, E., Feeding of the spider crab Maja squinado in rocky subtidal areas of the Ría de Arousa (north-West Spain). J. Mar. Biol. Assoc. U. K. 80 (2000), 95–102, 10.1017/S0025315499001605.
Berry, O., Bulman, C., Bunce, M., Coghlan, M., Murray, D.C., Ward, R.D., Comparison of morphological and DNA metabarcoding analyses of diets in exploited marine fishes. Mar. Ecol. Prog. Ser. 540 (2015), 167–181, 10.3354/meps11524.
Boudreau, S.A., Worm, B., Ecological role of large benthic decapods in marine ecosystems: a review. Mar. Ecol. Prog. Ser. 469 (2012), 195–213, 10.3354/meps09862.
Boussarie, G., Kopp, D., Méhault, S., Morfin, M., High survivability of discarded invertebrates from bottom trawling fisheries. Reg. Stud. Mar. Sci., 40, 2020, 101543, 10.1016/j.rsma.2020.101543.
Boyer, F., Mercier, C., Bonin, A., Le Bras, Y., Taberlet, P., Coissac, E., Obitools: a unix-inspired software package for DNA metabarcoding. Mol. Ecol. Resour. 16 (2016), 176–182, 10.1111/1755-0998.12428.
Buckland, A., Baker, R., Loneragan, N., Sheaves, M., Standardising fish stomach content analysis: the importance of prey condition. Fish. Res. 196 (2017), 126–140, 10.1016/j.fishres.2017.08.003.
Calderón-Sanou, I., Münkemüller, T., Boyer, F., Zinger, L., Thuiller, W., From environmental DNA sequences to ecological conclusions: how strong is the influence of methodological choices?. J. Biogeogr., 47, 2019, 10.1111/jbi.13681.
Casey, J.M., Meyer, C.P., Morat, F., Brandl, S.J., Planes, S., Parravicini, V., Reconstructing hyperdiverse food webs: gut content metabarcoding as a tool to disentangle trophic interactions on coral reefs. Methods Ecol. Evol. 10 (2019), 1157–1170, 10.1111/2041-210X.13206.
Catchpole, T., Frid, C., Gray, T.S., Discards in North Sea fisheries: causes, consequences and solutions. Mar. Policy 29 (2005), 421–430, 10.1016/j.marpol.2004.07.001.
Chaalali, A., Brind'Amour, A., Dubois, S.F., Le Bris, H., Functional roles of an engineer species for coastal benthic invertebrates and demersal fish. Ecol. Evol. 7 (2017), 5542–5559, 10.1002/ece3.2857.
Chartosia, N., Kitsos, M.-S., Tzomos, Th., Mavromati, E., Koukouras, A., Diet composition of five species of crabs (decapoda, Brachyura) that show a gradual transition from marine to terrestrial life. Crustaceana 83 (2010), 1181–1197, 10.2307/41038629.
Choy, S., Natural diet and feeding habits of the crabs Liocarcinus puber and Liocarcinus holsatus (Decapoda, Brachyura, Portunidae). Mar. Ecol. Prog. Ser. 31 (1986), 87–99, 10.3354/meps031087.
Clarke, K.R., Somerfield, P.J., Chapman, M.G., On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray–Curtis coefficient for denuded assemblages. J. Exp. Mar. Biol. Ecol. 330 (2006), 55–80, 10.1016/j.jembe.2005.12.017.
Coissac, E., OligoTag: a program for designing sets of tags for next-generation sequencing of multiplexed samples. Methods Mol. Biol. 888 (2012), 13–31, 10.1007/978-1-61779-870-2_2.
Colwell, R.K., Futuyma, D.J., On the measurement of niche breadth and overlap. Ecology 52 (1971), 567–576, 10.2307/1934144.
Cornou, A.S., Scavinner, M., Sagan, J., Cloatre, T., Dubroca, L., Billet, N., Catches and Discards of the French Fishing Trades (in French). Results of Observations on Board Professional Fishing Vessels in 2019. Obsmer Report. 2021.
Côté, I., Darling, E., Brown, C., Interactions among ecosystem stressors and their importance in conservation. Proc. R. Soc. B Biol. Sci., 283, 2016, 20152592, 10.1098/rspb.2015.2592.
Crain, C.M., Kroeker, K., Halpern, B.S., Interactive and cumulative effects of multiple human stressors in marine systems. Ecol. Lett. 11 (2008), 1304–1315, 10.1111/j.1461-0248.2008.01253.x.
da Silva, L.P., Mata, V.A., Lopes, P.B., Pereira, P., Jarman, S.N., Lopes, R.J., Beja, P., Advancing the integration of multi-marker metabarcoding data in dietary analysis of trophic generalists. Mol. Ecol. Resour. 19 (2019), 1420–1432, 10.1111/1755-0998.13060.
Davenport, J., McCullough, S., Thomas, R.W., Harman, L., McAllen, R., Behavioural responses of shallow-water benthic marine scavengers to fish carrion: a preliminary study. Mar. Freshw. Behav. Physiol. 49 (2016), 301–315, 10.1080/10236244.2016.1205793.
de Jonge, D.S.W., Merten, V., Bayer, T., Puebla, O., Reusch, T.B.H., Hoving, H.-J.T., A novel metabarcoding primer pair for environmental DNA analysis of Cephalopoda (Mollusca) targeting the nuclear 18S rRNA region. R. Soc. Open Sci., 8, 2021, 201388, 10.1098/rsos.201388.
de Sousa, L.L., Silva, S.M., Xavier, R., DNA metabarcoding in diet studies: unveiling ecological aspects in aquatic and terrestrial ecosystems. Environ. DNA 1 (2019), 199–214, 10.1002/edn3.27.
Deagle, B.E., Thomas, A.C., McInnes, J.C., Clarke, L.J., Vesterinen, E.J., Clare, E.L., Kartzinel, T.R., Eveson, J.P., Counting with DNA in metabarcoding studies: how should we convert sequence reads to dietary data?. Mol. Ecol. 28 (2019), 391–406, 10.1111/mec.14734.
Depestele, J., Feekings, J., Reid, D.G., Cook, R., Gascuel, D., Girardin, R., Heath, M., Hernvann, P.-Y., Morato, T., Soszynski, A., Savina-Rolland, M., The impact of fisheries discards on scavengers in the sea. Uhlmann, S.S., Ulrich, C., Kennelly, S.J., (eds.) The European Landing Obligation: Reducing Discards in Complex, Multi-Species and Multi-Jurisdictional Fisheries, 2019, Springer International Publishing, Cham, 129–162.
Duffy, J.E., Biodiversity and ecosystem function: the consumer connection. Oikos 99 (2002), 201–219, 10.1034/j.1600-0706.2002.990201.x.
Elbrecht, V., Leese, F., Can DNA-based ecosystem assessments quantify species abundance? Testing primer Bias and biomass—sequence relationships with an innovative Metabarcoding protocol. PLoS ONE, 10, 2015, e0130324, 10.1371/journal.pone.0130324.
European Union, Regulation (EU) no 1380/2013 of the European parliament and of the council of 11 December 2013 on the common fisheries policy, amending council regulations (EC) no 1954/2003 and (EC) no 1224/2009 and repealing council regulations (EC) no 2371/2002 and (EC) no 639/2004 and council decision 2004/585/EC. Off. J. Eur. Union L354 (2013), 22–61.
Ficetola, G.F., Coissac, E., Zundel, S., Riaz, T., Shehzad, W., Bessière, J., Taberlet, P., Pompanon, F., An in silico approach for the evaluation of DNA barcodes. BMC Genomics, 11, 2010, 434, 10.1186/1471-2164-11-434.
Fondo, E.N., Chaloupka, M., Heymans, J.J., Skilleter, G.A., Banning fisheries discards abruptly has a negative impact on the population dynamics of charismatic marine megafauna. PLoS ONE, 10(12), 2015, e0144543, 10.1371/journal.pone.0144543.
Froese, R., Pauly, D., FishBase. 2023, World Wide Web Electronic Publication www.fishbase.org (12/2023).
Gerlach, S.A., Ekstrøm, D.K., Eckardt, P.B., Filter feeding in the hermit crab. Oecologia 24 (1976), 257–264, 10.1007/BF00345477.
Gibson, R.N., Yin, M.C., Robb, L., The Behavioural basis of predator-prey size relationships between shrimp (Crangon crangon) and juvenile plaice (Pleuronectes platessa). J. Mar. Biol. Assoc. U. K. 75 (1995), 337–349, 10.1017/S002531540001821X.
Groenewold, S., Effects on benthic scavengers of discards and damaged benthos produced by the beam-trawl fishery in the southern North Sea. ICES J. Mar. Sci. 57 (2000), 1395–1406, 10.1006/jmsc.2000.0914.
Guardiola, M., Uriz, M.J., Taberlet, P., Coissac, E., Wangensteen, O.S., Turon, X., Deep-Sea, deep-sequencing: metabarcoding extracellular DNA from sediments of marine canyons. PLoS ONE, 11(4), 2016, e0153836, 10.1371/journal.pone.0153836.
Gusmão, L.C., Daly, M., Evolution of sea anemones (Cnidaria, Actiniaria, Hormathiidae) symbiotic with hermit crabs. Mol. Phylogenet. Evol. 56 (2010), 868–877, 10.1016/j.ympev.2010.05.001.
Jenkins, S.R., Mullen, C., Brand, A.R., Predator and scavenger aggregation to discarded by-catch from dredge fisheries: importance of damage level. J. Sea Res. 51 (2004), 69–76, 10.1016/j.seares.2003.05.002.
Jennings, S., Kaiser, M.J., The effects of fishing on marine ecosystems. Adv. Mar. Biol. 34 (1998), 201–212, 10.1016/S0065-2881(08)60212-6.
Kaiser, M.J., Ramsay, K., Hughes, R.N., Can fisheries influence interspecific competition in sympatric populations of hermit crabs?. J. Nat. Hist. 32 (1998), 521–531, 10.1080/00222939800770281.
Kopp, D., Marianne, R., Tiphaine, C., Sonia, M., Some expected impacts of the common fishery policy on marine food webs. Mar. Policy 66 (2016), 8–14, 10.1016/j.marpol.2016.01.002.
Lamb, P.D., Randall, P., Weltersbach, M.S., Andrews, B., Hyder, K., Estimating discard survival of European sea bass (Dicentrarchus labrax) in the UK commercial hook-and-line fishery. Fish. Manag. Ecol. 29 (2022), 105–114, 10.1111/fme.12518.
Lancaster, I., Pagurus bernhardus (L.) – an introduction to the natural history of hermit crabs. Field Stud. 7 (1988), 198–238.
Lejeune, B., Mouchet, M.A., Méhault, S., Kopp, D., Gut content metabarcoding reveals potential importance of fisheries discards consumption in marine fauna. Can. J. Fish. Aquat. Sci. 79 (2022), 1064–1073, 10.1139/cjfas-2021-0267.
Lejeune, B., Marcout, A., Kopp, D., Morandeau, F., Méhault, S., Mouchet, M.A., Assessing discard consumption dynamic in shallow coastal environment using underwater video. Fish. Res., 260, 2023, 106587, 10.1016/j.fishres.2022.106587.
Machovsky-Capuska, G.E., Raubenheimer, D., The nutritional ecology of marine apex predators. Annu. Rev. Mar. Sci. 12 (2020), 361–387, 10.1146/annurev-marine-010318-095411.
Macia, A., Abrantes, K.G.S., Paula, J., Thorn fish Terapon jarbua (Forskål) predation on juvenile white shrimp Penaeus indicus H. Milne Edwards and brown shrimp Metapenaeus monoceros (Fabricius): the effect of turbidity, prey density, substrate type and pneumatophore density. J. Exp. Mar. Biol. Ecol. 291 (2003), 29–56, 10.1016/S0022-0981(03)00097-2.
Martinetto, P., Iribarne, O., Palomo, G., Effect of fish predation on intertidal benthic fauna is modified by crab bioturbation. J. Exp. Mar. Biol. Ecol. 318 (2005), 71–84, 10.1016/j.jembe.2004.12.009.
Martinez Arbizu, P., pairwiseAdonis: Pairwise Multilevel Comparison Using Adonis. R Package Version 0.4. https://github.com/pmartinezarbizu/pairwiseAdonis, 2020.
Mascaró, M., Seed, R., Foraging behavior of juvenile Carcinus maenas (L.) and Cancer pagurus L. Mar. Biol. 139 (2001), 1135–1145, 10.1007/s002270100677.
McGaw, I.J., Curtis, D.L., A review of gastric processing in decapod crustaceans. J. Comp. Physiol. B. 183 (2013), 443–465, 10.1007/s00360-012-0730-3.
Méléder, V., Rincé, Y., Barillé, L., Gaudin, P., Rosa, P., Spatiotemporal changes in microphytobenthos assemblages in a macrotidal flat (Bourgneuf Bay, France). J. Phycol. 43 (2007), 1177–1190, 10.1111/j.1529-8817.2007.00423.x.
Mercier, C., Boyer, F., Kopylova, E., Taberlet, P., Bonin, A., Coissac, E., SUMATRA and SUMACLUST: fast and exact comparison and clustering of sequences. Programs and Abstracts of the SeqBio 2013 Workshop, 2013, 27–29.
Montoya, J.M., Pimm, S.L., Solé, R.V., Ecological networks and their fragility. Nature 442 (2006), 259–264, 10.1038/nature04927.
Morfin, M., Méhault, S., Benoît, H.P., Kopp, D., Narrowing down the number of species requiring detailed study as candidates for the EU common fisheries policy discard ban. Mar. Policy 77 (2017), 23–29, 10.1016/j.marpol.2016.12.003.
Norman, C.P., Jones, M.B., Influence of depth, season and moult stage on the diet of the velvet swimming crab Necora puber (brachyura, portunidae). Estuar. Coast. Shelf Sci. 34 (1992), 71–83, 10.1016/S0272-7714(05)80127-1.
Oh, C.-W., Hartnoll, R.G., Nash, R.D.M., Feeding ecology of the common shrimp Crangon crangon in port Erin Bay, Isle of Man, Irish Sea. Mar. Ecol. Prog. Ser. 214 (2001), 211–223, 10.3354/meps214211.
Oksanen, J., Simpson, G.L., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O'Hara, R.B., Solymos, P., Stevens, M.H.H., Szoecs, E., Wagner, H., Barbour, M., Bedward, M., Bolker, B., Borcard, D., Carvalho, G., Chirico, M., Caceres, M.D., Durand, S., Evangelista, H.B.A., FitzJohn, R., Friendly, M., Furneaux, B., Hannigan, G., Hill, M.O., Lahti, L., McGlinn, D., Ouellette, M.-H., Cunha, E.R., Smith, T., Stier, A., Braak, C.J.F.T., Weedon, J., Vegan: Community Ecology Package. R Package Version. 2.6-4. https://github.com/vegandevs/vegan, 2022.
Oro, D., Genovart, M., Tavecchia, G., Fowler, M.S., Martínez-Abraín, A., Ecological and evolutionary implications of food subsidies from humans. Ecol. Lett. 16 (2013), 1501–1514, 10.1111/ele.12187.
Orton, J.H., On the mode of feeding of the hermit-crab, Eupagurus Bernhardus, and some other Decapoda. J. Mar. Biol. Assoc. U. K. 14 (1927), 909–921, 10.1017/S0025315400051146.
Palomares, M., Pauly, D., SeaLifeBase. 2023, World Wide Web Electronic Publication www.sealifebase.org version (12/2023).
Quaggiotto, M.M., Burke, L., McCafferty, D., Bailey, D., First investigations of the consumption of seal carcasses by terrestrial and marine scavengers. Glasgow Nat. 26 (2016), 33–52.
R Core Team, R: A Language and Environment for Statistical Computing. 2020, R Foundation for Statistical Computing, Vienna, Austria https://www.R-project.org/.
R Core Team, R: A Language and Environment for Statistical Computing. 2023, R Foundation for Statistical Computing, Vienna, Austria https://www.R-project.org/.
Raffaelli, D., Conacher, A., McLachlan, H., Emes, C., The role of epibenthic crustacean predators in an estuarine food web. Estuar. Coast. Shelf Sci. 28 (1989), 149–160, 10.1016/0272-7714(89)90062-0.
Ramsay, K., Kaiser, M., Hughes, R., Changes in hermit crab feeding patterns in response to trawling disturbance. Mar. Ecol. Prog. Ser. 144 (1996), 63–72, 10.3354/meps144063.
Ramsay, K., Kaiser, M.J., Moore, P.G., Hughes, R.N., Consumption of fisheries discards by benthic scavengers: utilization of energy subsidies in different marine habitats. J. Anim. Ecol. 66 (1997), 884–896, 10.2307/6004.
Reis, K., Moderate predation on meiofauna by the macrobenthos of the Wadden Sea. Helgoländer Meeresun. 32 (1979), 453–465, 10.1007/BF02277989.
Romano, N., Zeng, C., Cannibalism of decapod crustaceans and implications for their aquaculture: a review of its prevalence, influencing factors, and mitigating methods. Rev. Fish. Sci. Aquac. 25 (2017), 42–69, 10.1080/23308249.2016.1221379.
Rooney, N., McCann, K., Gellner, G., Moore, J.C., Structural asymmetry and the stability of diverse food webs. Nature 442 (2006), 265–269, 10.1038/nature04887.
Schmitz, O.J., Predator and prey functional traits: understanding the adaptive machinery driving predator–prey interactions. F1000Research, 6, 2017, 1767, 10.12688/f1000research.11813.1.
Schnell, I.B., Bohmann, K., Gilbert, M.T.P., Tag jumps illuminated – reducing sequence-to-sample misidentifications in metabarcoding studies. Mol. Ecol. Resour. 15 (2015), 1289–1303, 10.1111/1755-0998.12402.
Shannon, C.E., A mathematical theory of communication. Bell Syst. Tech. J. 27 (1948), 379–423, 10.1002/j.1538-7305.1948.tb01338.x.
Shelton, R.G.G., Kinnear, J., Livingstone, K., A preliminary account of the feeding habits of the edible crab (Cancer pagurus) off north West Scotland. Int. Counc. Explor. Sea Comm. Meet., K: 35, 1979.
Shum, P., Wäge-Recchioni, J., Sellers, G.S., Johnson, M.L., Joyce, D.A., DNA metabarcoding reveals the dietary profiles of a benthic marine crustacean, Nephrops norvegicus. PLoS ONE, 18, 2023, e0289221, 10.1371/journal.pone.0289221.
Siegenthaler, A., Mastin, A., Dufaut, C., Mondal, D., Benvenuto, C., Background matching in the brown shrimp Crangon crangon: adaptive camouflage and behavioural-plasticity. Sci. Rep., 8, 2018, 3292, 10.1038/s41598-018-21412-y.
Siegenthaler, A., Wangensteen, O.S., Benvenuto, C., Campos, J., Mariani, S., DNA metabarcoding unveils multiscale trophic variation in a widespread coastal opportunist. Mol. Ecol. 28 (2019), 232–249, 10.1111/mec.14886.
Siegenthaler, A., Wangensteen, O.S., Soto, A.Z., Benvenuto, C., Corrigan, L., Mariani, S., Metabarcoding of shrimp stomach content: harnessing a natural sampler for fish biodiversity monitoring. Mol. Ecol. Resour. 19 (2019), 206–220, 10.1111/1755-0998.12956.
Števčić, Z., The feeding complex of the spider crab Maja squinado (in German with French abstract). Helgoländer Meeresun. 15 (1967), 630–636, 10.1007/BF01618656.
Symondson, W.O.C., Molecular identification of prey in predator diets. Mol. Ecol. 11 (2002), 627–641, 10.1046/j.1365-294X.2002.01471.x.
Szaniawska, A., Function and importance of crustaceans. Baltic Crustaceans, 2018, 185–188, 10.1007/978-3-319-56354-1_11.
Taberlet, P., Bonin, A., Zinger, L., Coissac, E., Environmental DNA: For Biodiversity Research and Monitoring. 2018, Oxford University Press, Oxford, UK, 10.1093/oso/9780198767220.001.0001.
Tam, J.C., Link, J.S., Rossberg, A.G., Rogers, S.I., Levin, P.S., Rochet, M.-J., Bundy, A., Belgrano, A., Libralato, S., Tomczak, M., van de Wolfshaar, K., Pranovi, F., Gorokhova, E., Large, S.I., Niquil, N., Greenstreet, S.P.R., Druon, J.-N., Lesutiene, J., Johansen, M., Preciado, I., Patricio, J., Palialexis, A., Tett, P., Johansen, G.O., Houle, J., Rindorf, A., Towards ecosystem-based management: identifying operational food-web indicators for marine ecosystems. ICES J. Mar. Sci. 74 (2017), 2040–2052, 10.1093/icesjms/fsw230.
Tamara, L., Fosso, B., Bachir, B., Giuseppe, C., Michele, G., Marinella, M., Graziano, P., Monica, S., Pierri, C., Hippocampus guttulatus diet based on DNA metabarcoding. Front. Mar. Sci., 10, 2023, 10.3389/fmars.2023.1138279.
Tsagarakis, K., Nikolioudakis, N., Papandroulakis, N., Vassilopoulou, V., Machias, A., Preliminary assessment of discards survival in a multi-species Mediterranean bottom trawl fishery. J. Appl. Ichthyol. 34 (2018), 842–849, 10.1111/jai.13691.
van der Reis, A.L., Jeffs, A.G., Lavery, S.D., From feeding habits to food webs: exploring the diet of an opportunistic benthic generalist. Mar. Ecol. Prog. Ser. 655 (2020), 107–121, 10.3354/meps13511.
van der Veer, H., Bergman, M.J.N., Predation by crustaceans on a newly settled 0-group plaice Pleuronectes platessa population in the western Wadden Sea. Mar. Ecol. Prog. Ser. 35 (1987), 203–215, 10.3354/meps035203.
Williams, M.J., Methods for analysis of natural diet in portunid crabs (Crustacea, Decapoda, Portunidae). J. Exp. Mar. Biol. Ecol. 52 (1981), 103–113, 10.1016/0022-0981(81)90174-X.
Wilson, E.E., Wolkovich, E.M., Scavenging: how carnivores and carrion structure communities. Trends Ecol. Evol. 26 (2011), 129–135, 10.1016/j.tree.2010.12.011.
Worm, B., Duffy, J.E., Biodiversity, productivity and stability in real food webs. Trends Ecol. Evol. 18 (2003), 628–632, 10.1016/j.tree.2003.09.003.
WoRMS Editorial Board, World Register of Marine Species. Available from https://www.marinespecies.org at VLIZ. Accessed 2023-02-12, 2023, 10.14284/170.
Zinger, L., Lionnet, C., Benoiston, A.-S., Donald, J., Mercier, C., Boyer, F., metabaR: an r package for the evaluation and improvement of DNA metabarcoding data quality. Methods Ecol. Evol. 12 (2021), 586–592, 10.1111/2041-210X.13552.
Zipser, E., Vermeij, G.J., Crushing behavior of tropical and temperate crabs. J. Exp. Mar. Biol. Ecol. 31 (1978), 155–172, 10.1016/0022-0981(78)90127-2.