Different feeding strategies in Antarctic scavenging amphipods and their implications for colonisation success in times of retreating glaciers
Tóm tắt
Scavenger guilds are composed of a variety of species, co-existing in the same habitat and sharing the same niche in the food web. Niche partitioning among them can manifest in different feeding strategies, e.g. during carcass feeding. In the bentho-pelagic realm of the Southern Ocean, scavenging amphipods (Lysianassoidea) are ubiquitous and occupy a central role in decomposition processes. Here we address the question whether scavenging lysianassoid amphipods employ different feeding strategies during carcass feeding, and whether synergistic feeding activities may influence carcass decomposition. To this end, we compared the relatively large species Waldeckia obesa with the small species Cheirimedon femoratus, Hippomedon kergueleni, and Orchomenella rotundifrons during fish carcass feeding (Notothenia spp.). The experimental approach combined ex situ feeding experiments, behavioural observations, and scanning electron microscopic analyses of mandibles. Furthermore, we aimed to detect ecological drivers for distribution patterns of scavenging amphipods in the Antarctic coastal ecosystems of Potter Cove. In Potter Cove, the climate-driven rapid retreat of the Fourcade Glacier is causing various environmental changes including the provision of new marine habitats to colonise. While in the newly ice-free areas fish are rare, macroalgae have already colonised hard substrates. Assuming that a temporal dietary switch may increase the colonisation success of the most abundant lysianassoids C. femoratus and H. kergueleni, we aimed to determine their consumption rates (g food x g amphipods−1 x day−1) and preferences of macroalgae and fish. We detected two functional groups with different feeding strategies among scavenging amphipods during carcass feeding: carcass ‘opener’ and ‘squeezer’. Synergistic effects between these groups were not statistically verified under the conditions tested. C. femoratus switched its diet when fish was not available by consuming macroalgae (about 0.2 day−1) but preferred fish by feeding up to 80% of its own mass daily. Contrary, H. kergueleni rejected macroalgae entirely and consumed fish with a maximal rate of 0.8 day−1. This study reveals functional groups in scavenging shallow-water amphipods and provides new information on coastal intraguild niche partitioning. We conclude that the dietary flexibility of C. femoratus is a potential ecological driver and central to its success in the colonisation of newly available ice-free Antarctic coastal habitats.
Tài liệu tham khảo
Getz WM. Biomass transformation webs provide a unified approach to consumer-resource modelling. Ecol Lett. 2011;14:113–24.
Stokland JN, Siitonen J, Jonsson BG. Biodiversity in dead wood. 1st ed: Cambridge University Press; 2012.
Duponnois R, Paugy M, Thioulouse J, Masse D, Lepage M. Functional diversity of soil microbial community, rock phosphate dissolution and growth of Acacia Seyal as influenced by grass-, litter- and soil-feeding termite nest structure amendments. Geoderma. 2005;124:349–61.
Kendall CJ. The early bird gets the carcass: temporal segregation and its effects on foraging success in avian scavengers. Auk. 2014;131:12–9.
Hunter J, Durant S, Caro T. Patterns of scavenger arrival at cheetah kills in Serengeti National Park Tanzania. Afr J Ecol. 2007;45:275–81.
Kruuk H. Competition for food between vultures in East Africa. Ardea. 1967;55:171–93.
Mallon JM, Swing K, Mosquera D. Neotropical vulture scavenging succession at a capybara carcass in eastern Ecuador. Ornitol Neotrop. 2013;24:475–80.
Sauer EF. Notes on the behaviour of lappet-faced vultures and cape vultures in the Namib desert of south West Africa. Modoqua. 1973;2:43–62.
Anderson GS, Bell LS. Impact of marine submergence and season on faunal colonization and decomposition of pig carcasses in the Salish Sea. PLoS One. 2016; doi:10.1371/journal.pone.0149107.
Jones EG, Collins MA, Bagley PM, Addison S, Priede IG. The fate of cetacean carcasses in the deep sea: observations on consumption rates and succession of scavenging species in the abyssal north-east Atlantic Ocean. Proc R Soc Lond B. 1998;265:1119–27.
Premke K, Klages M, Arntz WE. Aggregations of Arctic deep-sea scavengers at large food falls: temporal distribution, consumption rates and population structure. Mar Ecol Prog Ser. 2006;325:121–35.
De Broyer C, Nyssen F, Dauby P. The crustacean scavenger guild in Antarctic shelf, bathyal and abyssal communities. Deep Sea Res (II Top Stud Oceanogr). 2004;51:1733–52.
De Broyer C, Jażdżewska A. Biogeographic patterns of Southern Ocean benthic amphipods. In: KP DBC, Griffiths H, Raymond B, d'Udekem d'Acoz C, Van de Putte A, Danis B, David B, Grant S, Gutt J, Held C, Hosie G, Huettmann F, Post A, Ropert-Coudert Y, editors. Biogeographic atlas of the Southern Ocean. Cambridge: Scientific Committee on Antarctic Research; 2014. p. 155–65.
Dauby P, Scailteur Y, De Broyer C. Trophic diversity within the eastern Weddell Sea amphipod community. Hydrobiologia. 2001;443:69–86.
Dahl E. Deep-sea carrion feeding amphipods: evolutionary patterns in niche adaptation. Oikos. 1979:167–75.
Sainte-Marie B. Foraging of scavenging deep-sea lysianassoid amphipods. In: Rowe GTPV, editor. Deep-sea food chains and the global carbon cycle. Berlin Heidelberg New York: Springer; 1992. p. 105–24.
Watling L. Functional morphology of the amphipod mandible. J Nat Hist. 1993;27:837–49.
De Broyer C, Thurston MH. New Atlantic material and redescription of the type specimens of the giant abyssal amphipod Alicella Gigantea Chevreux (Crustacea). Zool Scr. 1987;16:335–50.
Quartino ML, Deregibus D, Campana GL, Latorre GEJ, Momo FR. Evidence of macroalgal colonization on newly ice-free areas following glacial retreat in potter cove (south Shetland Islands), Antarctica. PLoS One. 2013; doi:10.1371/journal.pone.0058223.
Pasotti F, Saravia LA, De Troch M, Tarantelli MS, Sahade R, Vanreusel A. Benthic trophic interactions in an Antarctic shallow water ecosystem affected by recent glacier retreat. PLoS One. 2015; doi:10.1371/journal.pone.0141742.
Sahade R, Lagger C, Torre L, Momo F, Monien P, Schloss I, Barnes DK, Servetto N, Tarantelli S, Tatian M, et al. Climate change and glacier retreat drive shifts in an Antarctic benthic ecosystem. Sci Adv. 2015; doi:10.1126/sciadv.1500050.
Lagger C, Nime M, Torre L, Servetto N, Tatián M, Sahade R. Climate change, glacier retreat and a new ice-Free Island offer new insights on Antarctic benthic responses. Ecography. 2017; doi:10.1111/ecog.03018.
Havermans C. DNA Barcoding, Phylogeography and Phylogeny of the Lysianassoidea (Crustacea: Amphipoda) from the Southern Ocean and the World’s Deep Seas. PhD Dissertation. Belgium: Université Catholique de Louvain; 2012. p. 1–423.
Seefeldt MA, Weigand AM, Havermans C, Moreira E, Held C. Fishing for scavengers: an integrated study to amphipod (Crustacea: Lysianassoidea) diversity of potter cove (south Shetland Islands, Antarctica). Mar Biodivers. 2017; doi:10.1007/s12526-017-0737-9.
Wölfl A-C, Wittenberg N, Feldens P, Hass HC, Betzler C, Kuhn G. Submarine landforms related to glacier retreat in a shallow Antarctic fjord. Antarct Sci. 2016;28:475–86.
Rückamp M, Braun M, Suckro S, Blindow N. Observed glacial changes on the king George Island ice cap, Antarctica, in the last decade. Glob Planet Chang. 2011;79:99–109.
Klöser H, Ferreyra G, Schloss I, Mercuri G, Laturnus F, Curtosi A. Hydrography of potter cove, a small fjord-like inlet on king George island (south Shetlands). Estuar Coast Shelf Sci. 1994;38:523–37.
Schloss IR, Abele D, Moreau S, Demers S, Bers AV, González O, Ferreyra GA. Response of phytoplankton dynamics to 19-year (1991–2009) climate trends in potter cove (Antarctica). J Mar Syst. 2012;92:53–66.
Klöser H, Quartino ML, Wiencke C. Distribution of macroalgae and macroalgal communities in gradients of physical conditions in potter cove, king George Island, Antarctica. Hydrobiologia. 1996;333:1–17.
IMCONet Interdisciplinary Modelling of Climate Change in Coastal Western Antarctica - Network for Staff Exchange and Training. http://www.imconet.eu/publications/ (2017). Accessed 04 Sept 2017.
Schneider CA, Rasband WS, Eliceiri KWNIH. Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9:671–5.
Huang YM, McClintock JB, Amsler CD, Peters KJ, Baker BJ. Feeding rates of common Antarctic gammarid amphipods on ecologically important sympatric macroalgae. J Exp Mar Biol Ecol. 2006;329:55–65.
Lastra M, Rodil IF, Sánchez-Mata A, García-Gallego M, Mora J. Fate and processing of macroalgal wrack subsidies in beaches of Deception Island, Antarctic peninsula. J Sea Res. 2014;88:1–10.
StatSoft I. Statistica version 12 (data analysis software system). 2013.
Mayer G, Maas A, Waloszek D. Mouthpart morphology of Synurella Ambulans (F. Müller, 1846). Spixiana. 2015;38:219–29.
Sainte-Marie B. Morphological adaptations for carrion feeding in four species of littoral or circalittoral lysianassid amphipods. Can J Zool. 1984;62:1668–74.
Morritt D. The crab carrion-scavenging amphipod, Orchomene Nanus in lough Hyne, co. Cork, Ireland. J Mar Biol Assoc UK. 2001;81:1059–60.
d’Udekem d’Acoz C, Havermans C. Two new Pseudorchomene species from the Southern Ocean, with phylogenetic remarks on the genus and related species (Crustacea: Amphipoda: Lysianassoidea: Lysianassidae: Tryphosinae). Zootaxa. 2012;3310:1–50.
Kaiser M, Moore POPINION. Obligate marine scavengers: do they exist? J Nat Hist. 1999;33:475–81.
Moore P, Wong Y. Orchomene nanus (Krøyer) (Amphipoda: Lysianassoidea), a selective scavenger of dead crabs: feeding preferences in the field. J Exp Mar Biol Ecol. 1995;192:35–45.
Moore P, Wong Y. Observations on the life history of Orchomene nanus (Krøyer) (Amphipoda: Lysianassoidea) at Millport, Scotland as deduced from baited trapping. J Exp Mar Biol Ecol. 1996;195:53–70.
Ramsay K, Kaiser MJ, Moore PG, Hughes RN. Consumption of fisheries discards by benthic scavengers: utilization of energy subsidies in different marine habitats. J Anim Ecol. 1997:884–96.
Campbell MON. Vultures: their evolution, ecology and conservation. 1st ed. Boca Raton: CRC Press; 2015.
Dabbs GR, Martin DC. Geographic variation in the taphonomic effect of vulture scavenging: the case for southern Illinois. J Forensic Sci. 2013;58(Suppl 1):20–5.
Pavés H, Schlatter R, Espinoza C. Scavenging and predation by black vultures Coragyps Atratus at a south American sea lion breeding colony. Vulture News. 2008;58:4–15.
Bornemissza G. An analysis of arthropod succession in carrion and the effect of its decomposiion on the soil fauna. Aust J Zool. 1957;5:1–12.
Goff M, Flynn M. Determination of postmortem interval by arthropod succession: a case study from the Hawaiian islands. J Forensic Sci. 1991;36:607–14.
Benecke MA. Brief history of forensic entomology. Forensic Sci Int. 2001;120:2–14.
Centeno N, Maldonado M, Oliva A. Seasonal patterns of arthropods occurring on sheltered and unsheltered pig carcasses in Buenos Aires Province (Argentina). Forensic Sci Int. 2002;126:63–70.
McIntosh CS, Dadour IR, Voss SCA. Comparison of carcass decomposition and associated insect succession onto burnt and unburnt pig carcasses. Int J Legal Med. 2017;131:835–45.
Wang Y, Ma M-y, Jiang X-y, Wang J-f, Li L-l, Yin X-j, Wang M, Lai Y, Tao L-y. Insect succession on remains of human and animals in Shenzhen, China. Forensic Sci Int. 2017;271:75–86.
Anderson GS, Bell LS. Comparison of faunal scavenging of submerged carrion in two seasons at a depth of 170 m, in the strait of Georgia, British Columbia. Insects. 2017;8:33.
Griffiths HJW, Rowan J, Roberts SJ, Belchier M, Linse K, Thatje S. Decapoda: crabs and lobsters. In: KP DBC, Griffiths H, Raymond B, d'Udekem d'Acoz C, Van de Putte A, Danis B, David B, Grant S, Gutt J, Held C, Hosie G, Huettmann F, Post A, Ropert-Coudert Y, editors. Biogeographic Atlas of the Southern Ocean. Cambridge: Scientific Committee on Antarctic Research; 2014. p. 185–9.
Basher Z, Costello M. Shrimps (Crustacea: Decapoda). In: KP DBC, Griffiths H, Raymond B, d'Udekem d'Acoz C, Van de Putte A, Danis B, David B, Grant S, Gutt J, Held C, Hosie G, Huettmann F, Post A, Ropert-Coudert Y, editors. Biogeographic Atlas of the Southern Ocean. Cambridge: Scientific Committee on Antarctic Research; 2014. p. 190–4.
Gorny M. Untersuchungen zur Ökologie antarktischer Garnelen (Decapoda, Natantia). In: PhD Dissertation. Germany: University of Bremen; 1992. p. 129.
Storch V, Bluhm BA, Arntz WE. Microscopic anatomy and ultrastructure of the digestive system of three Antarctic shrimps (Crustacea: Decapoda: Caridea). In: Arntz WECA, editor. Ecological studies in the Antarctic Sea ice zone. Heidelberg: Springer; 2002. p. 66–76.
d’Udekem d’Acoz C, Havermans C. Contribution to the systematics of the genus Eurythenes SI smith in scudder, 1882: an integrative study (Crustacea: Amphipoda: Lysianassoidea: Eurytheneidae). Zootaxa. 2015;3971:1–80.
Coleman CO. Comparative fore-gut morphology of Antarctic Amphipoda (Crustacea) adapted to different food sources. Hydrobiologia. 1991;223:1–9.
Chapelle G, Peck LS, Clarke A. Effects of feeding and starvation on the metabolic rate of the necrophagous Antarctic amphipod Waldeckia obesa (Chevreux, 1905). J Exp Mar Biol Ecol. 1994;183:63–76.
Rakusa-Suszczewski S, Lach A. Respiration of Orchomene plebs (Hurley, 1965) and Waldeckia obesa (Chevreux, 1905) from Admiralty Bay (south Shetlands Islands, Antarctic). Hydrobiologia. 1991;223:177–80.
Sainte-Marie B, Percy J, Shea J. A comparison of meal size and feeding rate of the lysianassid amphipods Anonyx nugax, Onisimus (= Pseudalibrotus) litoralis and Orchomenella pinguis. Mar Biol. 1989;102:361–8.
Wilson EE, Wolkovich EM. Scavenging: how carnivores and carrion structure communities. Trends Ecol Evol. 2011;26:129–35.
Tanabe K, Namba T. Omnivory creates chaos in simple food web models. Ecology. 2005;86:3411–4.
Amsler CD, Iken K, McClintock JB, Amsler MO, Peters KJ, Hubbard JM, Furrow FB, Baker BJ. Comprehensive evaluation of the palatability and chemical defenses of subtidal macroalgae from the Antarctic peninsula. Mar Ecol Prog Ser. 2005;294:141–59.
Koubbi P, De Broyer C, Clarke A, Pakhomov E, Scott F, Van den Berghe W, Danis Be The SCAR-MarBIN Register of Antarctic Marine Species (RAMS): Pisces. http://www.marinespecies.org/rams (2017). 2017–07-27.
Figuerola B, Núñez-Pons L, Moles J, Avila C. Feeding repellence in Antarctic bryozoans. Naturwissenschaften. 2013;100:1069–81.
Núñez-Pons L, Rodríguez-Arias M, Gómez-Garreta A, Ribera-Siguán A, Avila C. Feeding deterrency in Antarctic marine organisms: bioassays with the omnivore amphipod Cheirimedon Femoratus. Mar Ecol Prog Ser. 2012;462:163–74.
Poulin E, Palma AT, Féral J-P. Evolutionary versus ecological success in Antarctic benthic invertebrates. Trends Ecol Evol. 2002;17:218–22.
Barnes DKA, Sands CJ, Hogg OT, Robinson BJO, Downey RV, Smith JA. Biodiversity signature of the last glacial maximum at South Georgia, Southern Ocean. J Biogeogr. 2016;43:2391–9.
Bregazzi P. Life cycles and seasonal movements of Cheirimedon femoratus (Pfeffer) and Tryphosella kergueleni (Miers) (Crustacea: Amphipoda). Br Antarct Surv Bull. 1972;310:1–34.
Bluhm BA, Brey T, Klages M. The autofluorescent age pigment lipofuscin: key to age, growth and productivity of the Antarctic amphipod Waldeckia obesa (Chevreux, 1905). J Exp Mar Biol Ecol. 2001;258:215–35.
Thurston MH. The Crustacea Amphipoda of Signy Island. British Antarctic Survey: South Orkney Islands; 1972.
Bregazzi P. Habitat selection by Cheirimedon femoratus (Pfeffer) and Tryphosella kergueleni (Miers) (Crustacea: Amphipoda). Br Antarct Surv Bull. 1972;31:21–31.
Nyssen F, Brey T, Lepoint G, Bouquegneau J-M, De Broyer C, Dauby PA. Stable isotope approach to the eastern Weddell Sea trophic web: focus on benthic amphipods. Polar Biol. 2002;25:280–7.
Graeve M, Dauby P, Scailteur Y. Combined lipid, fatty acid and digestive tract content analyses: a penetrating approach to estimate feeding modes of Antarctic amphipods. Polar Biol. 2001;24:853–62.
Nyssen F, Brey T, Dauby P, Graeve M. Trophic position of Antarctic amphipods—enhanced analysis by a 2-dimensional biomarker assay. Mar Ecol Prog Ser. 2005;300:135–45.
Scambos TA, Bohlander J, Shuman C, Skvarca P. Glacier acceleration and thinning after ice shelf collapse in the Larsen B embayment, Antarctica. Geophys Res Lett. 2004;31
Gutt J, Barratt I, Domack E, CdU d’A, Dimmler W, Grémare A, Heilmayer O, Isla E, Janussen D, Jorgensen E. Biodiversity change after climate-induced ice-shelf collapse in the Antarctic. Deep-Sea Res II Top Stud Oceanogr. 2011;58:74–83.
Olson Z, Beasley J, DeVault TL, Rhodes O. Scavenger community response to the removal of a dominant scavenger. Oikos. 2012;121:77–84.