Diet and life history reduce interspecific and intraspecific competition among three sympatric Arctic cephalopods
1.
Gause, G. F. The Struggle for Existence (Williams & Wilkins, Baltimore, 1934).
Google Scholar
2.
Hutchinson, G. E. Concluding remarks. Cold Spring Harb. Symp. Quant. Biol. 22, 415–427 (1957).
Article Google Scholar
3.
Volterra, V. Variations and fluctuations of the number of individuals in marine intertidal species living together. J. Conseil. 3, 3–51 (1928).
Article Google Scholar
4.
Darwin, C. On the Origin of Species by Natural Selection, or the Preservation of Favoured Races in the Struggle for Life (John Murray, London, 1859).
Google Scholar
5.
Hardin, G. The competitive exclusion principle. Science 131, 1292–1297 (1960).
ADS CAS Article Google Scholar
6.
Alley, T. R. Competition theory, evolution, and the concept of an ecological niche. Acta Biotheor. 31, 165–179 (1982).
CAS PubMed Article Google Scholar
7.
Chase, J. M. & Leibold, M. A. Ecological Niches: Linking Classical and Contemporary Approaches (University of Chicago Press, Chicago, 2003).
Google Scholar
8.
Pianka, E. R. Competition and niche theory. In Theoretical Ecology: Principles and Applications (ed. May, R. M.) 114–141 (W.B. Saunders, Philadelphia, 1976).
Google Scholar
9.
Gerking, S. D. The Feeding Ecology of Fish (Academic, San Diego, 1994).
Google Scholar
10.
Ross, S. T. Resource partitioning in fish assemblages: a review of field studies. Copeia 2, 352–388 (1986).
Article Google Scholar
11.
Persson, L. Asymmetrical competition: are larger animals competitively superior?. Am. Nat. 126, 261–266 (1985).
Article Google Scholar
12.
Boecklen, W. J., Yarnes, C. T., Cook, B. A. & James, A. C. On the use of stable isotopes in trophic ecology. Annu. Rev. Ecol. Evol. Syst. 42, 411–440 (2011).
Article Google Scholar
13.
Layman, C. A. et al. Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biol. Rev. Camb. Philos. 87, 545–562 (2012).
Article Google Scholar
14.
Bearhop, S., Adams, C. E., Waldron, S., Fuller, R. A. & MacLeod, H. Determining trophic niche width: a novel approach using stable isotope analysis. J. Anim. Ecol. 73, 1007–1012 (2004).
Article Google Scholar
15.
Jackson, A. L., Inger, R., Parnell, A. C. & Bearhop, S. Comparing isotopic niche widths among and within communities: SIBER-stable isotope Bayesian ellipses in R. J. Anim. Ecol. 80, 595–602 (2011).
PubMed Article Google Scholar
16.
Layman, C. A., Arrington, D. A., Montaña, C. G. & Post, D. M. Can stable isotope ratios provide for community-wide measures of trophic structure?. Ecology 88, 42–48 (2007).
PubMed Article Google Scholar
17.
Newsome, S. D., del Rio, C. M., Bearhop, S. & Phillips, D. L. A niche for isotopic ecology. Front. Ecol. Environ. 5, 429–436 (2007).
Article Google Scholar
18.
Hette-Tronquart, N. Isotopic niche is not equal to trophic niche. Ecol. Lett. 22, 1987–1989 (2019).
PubMed Article Google Scholar
19.
Parnell, C. A. et al. Bayesian stable isotope mixing models. Environmetrics 24, 387–399 (2013).
MathSciNet Google Scholar
20.
Phillips, D. L. et al. Best practices for use of stable isotope mixing models in food-web studies. Can. J. Zool. 92, 823–835 (2014).
Article Google Scholar
21.
Knickle, D. C. & Rose, G. A. Dietary niche partitioning in sympatric gadid species in coastal Newfoundland: evidence from stomachs and C-N isotopes. Environ. Biol. Fish. 97, 343–355 (2014).
Article Google Scholar
22.
Simpson, S. J., Sims, D. W. & Trueman, C. M. Ontogenetic trends in resource partitioning and trophic geography of sympatric skates (Rajidae) inferred from stable isotope composition across eye lenses. Mar. Ecol. Prog. Ser. 624, 103–116 (2019).
ADS CAS Article Google Scholar
23.
Bearhop, S. et al. Stable isotopes indicate sex-specific and long-term individual foraging specialisation in diving seabirds. Mar. Ecol. Prog. Ser. 311, 157–164 (2006).
ADS Article Google Scholar
24.
Young, H. S., McCauley, D. J., Dirzo, R., Dunbar, R. B. & Shaffer, S. A. Niche partitioning among and within sympatric tropical seabirds revealed by stable isotope analysis. Mar. Ecol. Prog. Ser. 416, 285–294 (2010).
ADS CAS Article Google Scholar
25.
Botta, S. et al. Isotopic niche overlap and partition among three Antarctic seals from the Western Antarctic Peninsula. Deep-Sea Res. II(149), 240–249 (2018).
Google Scholar
26.
Kiszka, J. et al. Ecological niche segregation within a community of sympatric dolphins around a tropical island. Mar. Ecol. Prog. Ser. 433, 273–288 (2011).
ADS Article Google Scholar
27.
Ogloff, W. R., Yurkowski, D. J., Davoren, G. K. & Ferguson, S. H. Diet and isotopic niche overlap elucidate competition potential between seasonally sympatric phocids in the Canadian Arctic. Mar. Biol. 166, 103 (2019).
Article CAS Google Scholar
28.
Dubois, S., Orvain, F., Marin-Léal, J. C., Ropert, M. & Lefebvre, S. Small-scale spatial variability of food partitioning between cultivated oysters and associated suspension feeding species, as revealed by stable isotopes. Mar. Ecol. Prog. Ser. 336, 151–160 (2007).
ADS CAS Article Google Scholar
29.
Karlson, A. M. L., Gorokhova, E. & Elmgren, R. Do deposit-feeders compete? Isotopic niche analysis of an invasion in a species-poor system. Sci. Rep. 5, 9715 (2015).
ADS CAS PubMed PubMed Central Article Google Scholar
30.
Taupp, T., Hellmann, C., Gergs, R., Winkelmann, C. & Wetzel, M. A. Life under exceptional conditions—isotopic niches of benthic invertebrates in the estuarine maximum turbidity zone. Estuar. Coast. 40, 502–512 (2017).
CAS Article Google Scholar
31.
Bennice, C. O., Rayburn, A. R., Brooks, W. R. & Hanlon, R. T. Fine-scale habitat partitioning facilitates sympatry between two octopus species in a shallow Florida lagoon. Mar. Ecol. Prog. Ser. 609, 151–161 (2019).
Article Google Scholar
32.
Matias, R. S. et al. Show your beaks and we tell you what you eat: different ecology in sympatric Antarctic benthic octopods under a climate change context. Mar. Environ. Res. 150, 104757 (2019).
CAS PubMed Article Google Scholar
33.
Rosas-Luis, R., Navarro, J., Sánchez, P. & del Río, J. L. Assessing the trophic ecology of three sympatric squid in the marine ecosystem off the Patagonian Shelf by combining stomach content and stable isotopic analyses. Mar. Biol. Res. 12, 402–411 (2016).
Article Google Scholar
34.
Boyle, P. R. & Rodhouse, P. G. Cephalopods: Ecology and Fisheries (Wiley-Blackwell, Oxford, 2005).
Google Scholar
35.
Rodhouse, P. G. & Nigmatullin, Ch. M. Role as consumers. Philos. Trans. R. Soc. B 351, 1003–1022 (1996).
ADS Article Google Scholar
36.
Jereb, P. & Roper, C.F.E. Cephalopods of the world. An annotated and illustrated catalogue of cephalopod species known to date. Volume 1. Chambered nautiluses and sepioids (Nautilidae, Sepiidae, Sepiolidae, Sepiadariidae, Idiosepiidae and Spirulidae). FAO Species Catalogue for Fishery Purposes, No. 4. Rome: FAO (2005).
37.
Golikov, A. V., Sabirov, R. M., Lubin, P. A. & Jørgensen, L. L. Changes in distribution and range structure of Arctic cephalopods due to climatic changes of the last decades. Biodiversity 14, 28–35 (2013).
Article Google Scholar
38.
Nesis, K. N. Cephalopod mollusks of the Arctic Ocean and its seas. In Fauna and Distribution of Molluscs: North Pacific and Arctic Basin (ed. Kafanov, A. I.) 115–136 (USSR Academy of Sciences, Vladivostok, 1987) (in Russian).
Google Scholar
39.
Xavier, J. C. et al. A review on the biodiversity, distribution and trophic role of cephalopods in the Arctic and Antarctic marine ecosystems under a changing ocean. Mar. Biol. 165, 93 (2018).
Article Google Scholar
40.
Golikov, A. V. et al. Reproductive biology and ecology of the boreoatlantic armhook squid Gonatus fabricii (Cephalopoda: Gonatidae). J. Mollus. Stud. 85, 287–299 (2019).
Article Google Scholar
41.
Golikov, A. V. et al. Food spectrum and trophic position of an Arctic cephalopod, Rossia palpebrosa (Sepiolida), inferred by stomach contents and stable isotope (δ13C and δ15N) analyses. Mar. Ecol. Prog. Ser. 632, 131–144 (2019).
ADS Article Google Scholar
42.
Golikov, A. V. et al. Ontogenetic changes in stable isotope (δ13C and δ15N) values in squid Gonatus fabricii (Cephalopoda) reveal its important ecological role in the Arctic. Mar. Ecol. Prog. Ser. 606, 65–78 (2018).
ADS CAS Article Google Scholar
43.
Golikov, A. V., Sabirov, R. M. & Lubin, P. A. First assessment of biomass and abundance of cephalopods Rossia palpebrosa and Gonatus fabricii in the Barents Sea. J. Mar. Biol. Assoc. UK 97, 1605–1616 (2017).
Article Google Scholar
44.
Nesis, K. N. Oceanic Cephalopods: Distribution, Life Forms, Evolution (Nauka, Moscow, 1985) (in Russian).
Google Scholar
45.
Overland, J. E., Wang, M., Walsh, J. E. & Stroeve, J. C. Future Arctic climate changes: adaptation and mitigation time scales. Earth’s Future 2, 68–74 (2014).
ADS Article Google Scholar
46.
Dalpadado, P. et al. Climate effects on temporal and spatial dynamics of phytoplankton and zooplankton in the Barents Sea. Prog. Oceanogr. 185, 102320 (2020).
Article Google Scholar
47.
Laidre, K. L. et al. Arctic marine mammal population status, sea ice habitat loss, and conservation recommendations for the 21st century. Conserv. Biol. 29, 724–737 (2015).
PubMed PubMed Central Article Google Scholar
48.
Mercer, M.C. Systematics of the Sepiolid Squid Rossia Owen 1835 in Canadian Waters with a Preliminary Review of the Genus and Notes on Biology (MSc thesis). St. Johns: Memorial University of Newfoundland (1968).
49.
Golikov, A.V. Distribution and reproductive biology of ten-armed cephalopods (Sepiolida, Teuthida) in the Barents Sea and adjacent areas (PhD thesis). Moscow: Moscow State University (2015) (in Russian).
50.
Golikov, A.V., Sabirov, R.M., Gudmundsson, G. Cephalopoda (Smokkdýr), Rossia megaptera Verrill, 1881. (2018). http://www.ni.is/biota/animalia/mollusca/cephalopoda/rossia-megaptera. Accessed 04 June 2020.
51.
Golikov, A. V., Morov, A. R., Sabirov, R. M., Lubin, P. A. & Jørgensen, L. L. Functional morphology of reproductive system of Rossia palpebrosa (Cephalopoda, Sepiolida) in Barents Sea. Proc. Kazan Univ. Nat. Sci. Ser. 155, 116–129 (2013) (in Russian with English abstract).
Google Scholar
52.
Cherel, Y., Ducatez, S., Fontaine, C., Richard, P. & Guinet, C. Stable isotopes reveal the trophic position and mesopelagic fish diet of female southern elephant seals breeding on the Kerguelen Islands. Mar. Ecol. Prog. Ser. 370, 239–247 (2008).
ADS Article Google Scholar
53.
Cherel, Y. & Hobson, K. A. Stable isotopes, beaks and predators: a new tool to study the trophic ecology of cephalopods, including giant and colossal squids. Proc. R. Soc. B. 272, 1601–1607 (2005).
PubMed Article Google Scholar
54.
Golikov, A. V. et al. The first global deep-sea stable isotope assessment reveals the unique trophic ecology of Vampire Squid Vampyroteuthis infernalis (Cephalopoda). Sci. Rep. 9, 19099 (2019).
ADS CAS PubMed PubMed Central Article Google Scholar
55.
Cherel, Y., Fontaine, C., Jackson, G. D., Jackson, C. H. & Richard, P. Tissue, ontogenic and sex-related differences in δ13C and δ15N values of the oceanic squid Todarodes filippovae (Cephalopoda: Ommastrephidae). Mar. Biol. 156, 699–708 (2009).
Article Google Scholar
56.
Zar, J. H. Biostatistical Analysis 5th edn. (Prentice Hall, Upper Saddle River, 2010).
Google Scholar
57.
Ruiz-Cooley, R. I., Garcia, K. Y. & Hetherington, E. D. Effects of lipid removal and preservatives on carbon and nitrogen stable isotope ratios of squid tissues: implications for ecological studies. J. Exp. Mar. Biol. Ecol. 407, 101–107 (2011).
CAS Article Google Scholar
58.
Hobson, K. A. & Cherel, Y. Isotopic reconstruction of marine food webs using cephalopod beaks: new insight from captively raised Sepia officinalis. Can. J. Zool. 84, 766–770 (2006).
Article Google Scholar
59.
Post, D. M. Using stable isotopes to estimate trophic position: models, methods and assumptions. Ecology 83, 703–718 (2002).
Article Google Scholar
60.
Hobson, K. A. et al. A stable isotope (δ13C, δ15N) model for the North Water food web: implications for evaluating trophodynamics and the flow of energy and contaminants. Deep-Sea Res. II 49, 5131–5150 (2002).
ADS CAS Article Google Scholar
61.
Van der Zanden, M. J., Cabana, G. & Rasmussen, J. B. Comparing trophic position of freshwater fish calculated using stable nitrogen isotope ratios (δ15N) and literature dietary data. Can. J. Fish. Aquat. Sci. 54, 1142–1158 (1997).
Article Google Scholar
62.
Hussey, N. E. et al. Rescaling the trophic structure of marine food webs. Ecol. Lett. 17, 239–250 (2014).
PubMed Article Google Scholar
63.
Hussey, N. E. et al. Corrigendum to Hussey et al. (2014). Ecol. Lett. 17, 768 (2014).
PubMed Central Article PubMed Google Scholar
64.
Linnebjerg, J. F. et al. Deciphering the structure of the West Greenland marine food web using stable isotopes (δ13C, δ15N). Mar. Biol. 163, 230 (2016).
Article Google Scholar
65.
Søreide, J. E. et al. Sympagic-pelagic-benthic coupling in Arctic and Atlantic waters around Svalbard revealed by stable isotopic and fatty acid tracers. Mar. Biol. Res. 9, 831–850 (2013).
Article Google Scholar
66.
Sokolowski, A. et al. Trophic structure of the macrobenthic community of Hornsund, Spitsbergen, based on the determination of stable carbon and nitrogen isotopic signatures. Polar Biol. 37, 1247–1260 (2014).
Article Google Scholar
67.
Tamelander, T. et al. Trophic relationships and pelagic-benthic coupling during summer in the Barents Sea marginal ice zone, revealed by stable carbon and nitrogen isotope measurements. Mar. Ecol. Prog. Ser. 310, 33–46 (2006).
ADS CAS Article Google Scholar
68.
R Development Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. (2019). http://www.r-project.org/. Accessed 04 June 2020.
69.
Syväranta, J., Lensu, A., Marjomaki, T. J., Oksanen, S. & Jones, R. I. An empirical evaluation of the utility of convex hull and standard ellipse areas for assessing population niche widths from stable isotope data. PLoS ONE 8, e56094 (2013).
ADS PubMed PubMed Central Article CAS Google Scholar
70.
Langton, R. W. Diet overlap between Atlantic cod, Gadus morphua, silver hake, Merluccius bilinearis, and fifteen other northwest Atlantic finfish. Fish. B NOAA 80, 745–759 (1982).
Google Scholar
71.
Parnell, C.A. simmr: A Stable Isotope Mixing Model. Version 0.4.1. (2019). https://cran.r-project.org/web/packages/simmr/. Accessed 04 June 2020.
72.
Smith, J. A., Mazumder, D., Suthers, I. M. & Taylor, M. D. To fit or not to fit: evaluating stable isotope mixing models using simulated mixing polygons. Methods Ecol. Evol. 4, 612–618 (2013).
Article Google Scholar
73.
Hammer, Ø., Harper, D. A. T. & Ryan, P. D. PAST: paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4, 1–9 (2001).
Google Scholar
74.
Gruber, N. et al. Spatiotemporal patterns of carbon-13 in the global surface oceans and the oceanic Suess effect. Glob. Biogeochem. Cycl. 13, 307–335 (1999).
ADS CAS Article Google Scholar
75.
Yurkowski, D. J., Hussey, N. E., Ferguson, S. H. & Fisk, A. T. A temporal shift in trophic diversity among a predator assemblage in a warming Arctic. R. Soc. Open. Sci. 5, 180259 (2018).
ADS CAS PubMed PubMed Central Article Google Scholar
76.
Guerra, A. et al. Life-history traits of the giant squid Architeuthis dux revealed from stable isotope signatures recorded in beaks. ICES J. Mar. Sci. 67, 1425–1431 (2010).
Article Google Scholar
77.
Queirós, J. P. et al. Ontogenic changes in habitat and trophic ecology in the Antarctic squid Kondakovia longimana derived from isotopic analysis on beaks. Polar Biol. 41, 2409–2421 (2018).
Article Google Scholar
78.
Queirós, J. P. et al. Ontogenetic changes in habitat and trophic ecology of the giant Antarctic octopus Megaleledone setebos inferred from stable isotope analyses in beaks. Mar. Biol. 167, 56 (2020).
Article CAS Google Scholar
79.
Hansen, H. J., Hedeholm, R. B., Sünksen, K., Christensen, J. T. & Grønkjær, P. Spatial variability of carbon (δ13C) and nitrogen (δ15N) stable isotope ratios in an Arctic marine food web. Mar. Ecol. Prog. Ser. 467, 47–59 (2012).
ADS CAS Article Google Scholar
80.
Cherel, Y., Ridoux, V., Spitz, J. & Richard, P. Stable isotopes document the trophic structure of a deep-sea cephalopod assemblage including giant octopod and giant squid. Biol. Lett. 5, 364–367 (2009).
CAS PubMed PubMed Central Article Google Scholar
81.
Chouvelon, T. et al. Revisiting the use of δ15N in meso-scale studies of marine food webs by considering spatio-temporal variations in stable isotopic signatures—the case of an open ecosystem: the Bay of Biscay (North-East Atlantic). Prog. Oceanogr. 101, 92–105 (2012).
ADS Article Google Scholar
82.
Das, K., Lepoint, G., Leroy, Y. & Bouquegneau, J. M. Marine mammals from the southern North Sea: feeding ecology data from δ13C and δ15N measurements. Mar. Ecol. Prog. Ser. 263, 287–298 (2003).
ADS Article Google Scholar
83.
Gong, Y., Ruiz-Cooley, R. I., Hunsicker, M. E., Li, Y. & Chen, X. Sexual dimorphism in feeding apparatus and niche partitioning in juvenile jumbo squid Dosidicus gigas. Mar. Ecol. Prog. Ser. 607, 99–112 (2018).
ADS CAS Article Google Scholar
84.
Trasviña-Carrillo, L. D. et al. Spatial and trophic preferences of jumbo squid Dosidicus gigas (D’Orbigny, 1835) in the central Gulf of California: ecological inferences using stable isotopes. Rapid Commun. Mass. Spectrom. 32, 1225–1236 (2018).
ADS PubMed Article CAS Google Scholar
85.
Guerreiro, M. et al. Habitat and trophic ecology of Southern Ocean cephalopods from stable isotope analyses. Mar. Ecol. Prog. Ser. 530, 119–134 (2015).
ADS CAS Article Google Scholar
86.
Kato, Y. et al. Stable isotope analysis of the gladius to investigate migration and trophic patterns of the neon flying squid (Ommastrephes bartramii). Fish. Res. 173, 169–174 (2016).
Article Google Scholar More