Skip to main content
Log in

Intraspecific dietary variation in niche partitioning within a community of ecologically similar snakes

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

Niche partitioning is an important mechanism for allowing ecologically similar species to coexist, contributing to biodiversity and the functioning of ecological communities. Species partition niches by taking advantage of environmental heterogeneity. However, niche partitioning and species coexistence investigations often do not include intraspecific variation or individual differences like sex and body size even though these factors can have important ecological consequences. Such intrapopulation factors can reduce the number of individuals among species that overlap in resource use and potentially facilitate coexistence. Using stable isotopes (δ13C and δ15N), we quantified dietary differences among three ecologically similar, sympatric watersnake species: Nerodia erythrogaster, N. rhombifer and N. sipedon. Additionally for each species, we determined intraspecific dietary patterns and determined how those within-species patterns may contribute to dietary niche partitioning among species. Nerodia erythrogaster fed more on terrestrial prey, while N. rhombifer fed at higher trophic levels. Females across species fed at higher trophic levels than did males, and isotopic variance differed between the sexes in N. sipedon. Larger watersnakes foraged at higher trophic levels and fed more on terrestrial prey. Each watersnake species had a distinct diet that overlapped to some degree with the other species’ diets, but these diets varied both between sexes and among size groups within species. This inter- and intraspecific dietary variation can facilitate species coexistence by reducing the number of individuals from all species that use the same resources. Intraspecific variation can add important and nuanced layers to the evolution of species coexistence, and research on interspecific niche relationships needs to increasingly consider the effects of these intraspecific variations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

Data from this study are available at Dyrad Digital Depository: https://doi.org/10.5061/dryad.2ngf1vhm0

References

  • Alfaro ME, Arnold SJ (2001) Molecular systematics and evolution of Regina and the thamnophiine snakes. Mol Phylogenet Evol 21:408–423

    CAS  PubMed  Google Scholar 

  • Altig R, Whiles MR, Taylor CL (2007) What do tadpoles really eat? Assessing the trophic status of an understudied and imperiled group of consumers in freshwater habitats. Freshw Biol 52:386–395

    Google Scholar 

  • Arim M, Abades SR, Laufer G et al (2010) Food web structure and body size: trophic position and resource acquisition. Oikos 119:147–153

    Google Scholar 

  • Arnold SJ (1993) Foraging theory and prey-size-predator-size relations in snakes. In: Seigel RA, Collins JT (eds) Snakes: ecology and behavior. The Blackburn Press, Caldwell, pp 87–115

    Google Scholar 

  • Bearhop S, Adams CE, Waldron S et al (2004) Determining trophic niche width: a novel approach using stable isotope analysis. J Anim Ecol 73:1007–1012

    Google Scholar 

  • Bearhop S, Phillips RA, McGill R et al (2006) Stable isotopes indicate sex-specific and long-term individual foraging specialisation in diving seabirds. Mar Ecol Prog Ser 311:157–164

    Google Scholar 

  • Beaulieu M, Sockman KW (2012) One meadow for two sparrows: resource partitioning in a high elevation habitat. Oecologia 170:529–540

    PubMed  Google Scholar 

  • Beck CA, Iverson SJ, Bowen WD, Blanchard W (2007) Sex differences in grey seal diet reflect seasonal variation in foraging behaviour and reproductive expenditure: evidence from quantitative fatty acid signature analysis. J Anim Ecol 76:490–502

    PubMed  Google Scholar 

  • Bilcke J, Herrel A, Van Damme R (2006) Correlated evolution of aquatic prey-capture strategies in European and American natricine snakes. Biol J Linn Soc 88:73–83

    Google Scholar 

  • Bolnick DI, Svanbäck R, Fordyce JA et al (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28

    PubMed  Google Scholar 

  • Bolnick DI, Svanbäck R, Araújo MS, Persson L (2007) Comparative support for the niche variation hypothesis that more generalized populations also are more heterogeneous. Proc Natl Acad Sci 104:10075–10079

    CAS  PubMed  Google Scholar 

  • Bowen KD (2004) Geographic and size-related variation in the diet of insular populations of the northern watersnake. Am Midl Nat 152:418–424

    Google Scholar 

  • Broekhuis F, Thuo D, Hayward MW (2018) Feeding ecology of cheetahs in the Massai Mara, Kenya and the potential for intra- and interspecific competition. J Zool 304:65–72

    Google Scholar 

  • Brown GP, Weatherhead PJ (2000) Thermal ecology and sexual size dimorphism in northern watersnakes, Nerodia sipedon. Ecol Monogr 70:311–330

    Google Scholar 

  • Burbrink FT, Phillips CA, Heske EJ (1998) A riparian zone in southern Illinois as a potential dispersal corridor for reptiles and amphibians. Biol Conserv 86:107–115

    Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Canavero A, Hernández D, Zarucki M, Arim M (2014) Patterns of co-occurrences in a killifish metacommunity are more related with body size than with species identity. Austral Ecol 39:455–461

    Google Scholar 

  • Cherel Y, Fontaine C, Richard P, Labat J-P (2010) Isotopic niches and trophic levels of myctophid fishes and their predators in the Southern Ocean. Limnol Oceanogr 55:324–332

    CAS  Google Scholar 

  • Cloyed CS, Eason PK (2016) Different ecological conditions support individual specialization in closely related, ecologically similar species. Evol Ecol 30:379–400

    Google Scholar 

  • Cloyed CS, Eason PK (2017) Niche partitioning and the role of intraspecific niche variation in structuring a guild of generalist anurans. R Soc Open Sci 4:170060

    PubMed  PubMed Central  Google Scholar 

  • Costa GC, Vitt LJ, Pianka ER et al (2008) Optimal foraging constrains macroecological patterns: body size and dietary niche breadth in lizards. Glob Ecol Biogeogr 17:670–677

    Google Scholar 

  • Costa-Pereira R, Araújo MS, Souza FL, Ingram T (2019) Competition and resource breadth shape niche variation and overlap in multiple trophic dimensions. Proc R Soc B 286:20190369

    PubMed  Google Scholar 

  • Dalponti G, Guariento RD, Caliman A (2018) Hunting high or low: body size drives trophic position among and within marine predators. Mar Ecol Prog Ser 597:39–46

    Google Scholar 

  • Dayan T, Simberloff D (2005) Ecological and community-wide character displacement: the next generation. Ecol Lett 8:875–894

    Google Scholar 

  • Durso AM, Willson JD, Winne CT (2013) Habitat influences diet overlap in aquatic snake assemblages. J Zool 291:185–193

    Google Scholar 

  • Egan JP, Gibbs S, Simons AM (2018) Trophic niches through ontogeny in 12 species of Indo-Pacific marine Clupeoidei (herrings, sardines, and anchovies). Mar Biol 165:153

    Google Scholar 

  • Ernst CH, Ernst EM (2003) Snakes of the United States and Canada. Smithsonian Institution Press, Washington

    Google Scholar 

  • Falke LP, Henderson JS, Novak M, Preston DL (2020) Temporal shifts in intraspecific and interspecific diet variation among 3 stream predators. Freshw Sci 39:115–125

    Google Scholar 

  • Fink P, Reichwaldt ES, Harrod C, Rossberg AG (2012) Determining trophic niche width: an experimental test of the stable isotope approach. Oikos 121:1985–1994

    Google Scholar 

  • Fitzgerald LA (2012) Finding and capturing reptiles. In: McDiarmid RW, Foster MS, Guyer C et al (eds) Reptile biodiversity: standard methods for inventory and monitoring. University of California Press, Berkeley, pp 77–88

    Google Scholar 

  • Fletcher DE, Lindell AH, Stillings GK et al (2015) Trophic variation in coastal plain stream predatory fishes. Southeast Nat 14:373–396

    Google Scholar 

  • Forero MG, González-Solís J, Hobson KA et al (2005) Stable isotopes reveal trophic segregation by sex and age in the southern giant petrel in two different food webs. Mar Ecol Prog Ser 296:107–113

    Google Scholar 

  • Fry B, Mumford PL, Tam F et al (1999) Trophic position and individual feeding histories of fish from Lake Okeechobee, Florida. Can J Fish Aquat Sci 56:590–600

    Google Scholar 

  • Gause GF (1934) Experimental analysis of Vito Volterra’s mathematical theory of the struggle for existence. Science 79:16–17

    CAS  PubMed  Google Scholar 

  • Gibbons JW, Andrews KM (2004) PIT tagging: simple technology at its best. BioScience 54:447–454

    Google Scholar 

  • Gibbons JW, Dorcas ME (2004) North American watersnakes: a natural history. University of Oklahoma Press, Norman

    Google Scholar 

  • Gittleman JL, Van Valkenburgh BV (1997) Sexual dimorphism in the canines and skulls of carnivores: effects of size, phylogeny, and behavioural ecology. J Zool 242:97–117

    Google Scholar 

  • Hadi S, Ziegler T, Waltert M et al (2012) Habitat use of trophic niche overlap of two sympatric Colobines, Presbytis potenziani and Simias concolor, on Siberut Island, Indonesia. Int J Primatol 33:218–232

    Google Scholar 

  • Hardin G (1960) The competitive exclusion principle. Science 131:1292–1297

    CAS  PubMed  Google Scholar 

  • Hendry CR, Guiher TJ, Pyron RA (2014) Ecological divergence and sexual selection drive sexual size dimorphism in new world pitvipers (Serpentes: Viperidae). J Evol Biol 27:760–771

    CAS  PubMed  Google Scholar 

  • Himes JG (2003) Intra- and interspecific competition among the water snakes, Nerodia sipedon and Nerodia rhombifer. J Herpetol 37:126–131

    Google Scholar 

  • Hollows JW, Townsend CR, Collier KJ (2002) Diet of the crayfish Paranephrops zealandicus in bush and pasture streams: insights from stable isotopes and stomach analysis. N Z J Mar Freshw Res 36:129–142

    Google Scholar 

  • Hubert WA, Pope KL, Dettmers JM (2012) Passive capture techniques. In: Zale AV, Parrish DL, Sutton TM (eds) Fisheries techniques, 3rd edn. American Fisheries Society, Bethesda, pp 223–265

    Google Scholar 

  • Hutchinson GE (1959) Homage to Santa Rosalia or why are there so many kinds of animals? Am Nat 93:145–159

    Google Scholar 

  • Hutchinson GE (1961) The paradox of the plankton. Am Nat 95:137–145

    Google Scholar 

  • Hutinec BJ, Mebert K (2011) Ecological partitioning between dice Snakes (Natrix tessallata) and grass snakes (Natrix natrix) in Southern Croatia. Mertensiella 18:225–233

    Google Scholar 

  • Jennings S, Pinnegar JK, Polunin NVC, Boon TW (2001) Weak cross-species relationships between body size and trophic level belie powerful size-based trophic structuring in fish communities. J Anim Ecol 70:934–944

    Google Scholar 

  • King RB (1993) Microgeographic, historical, and size-correlated variation in water snake diet composition. J Herpetol 27:90–94

    Google Scholar 

  • King RB, Ray JM, Stanford KM (2006) Gorging on gobies: beneficial effects of alien prey on a threatened vertebrate. Can J Zool 84:108–115

    Google Scholar 

  • Kliemann BCK, Baldasso MC, Pini SFR et al (2019) Assessing the diet and trophic niche breadth of an omnivorous fish (Glanidium ribeiroi) in subtropical lotic environments: intraspecific and ontogenic responses to spatial variations. Mar Freshw Res 70:1116–1128

    Google Scholar 

  • Kofron CP (1978) Food and habitats of aquatic snakes (Reptilia, Serpentes) in a Louisiana swamp. J Herpetol 12:543–554

    Google Scholar 

  • Lacy GB (1995) Food habits of the midland water snake, Nerodia sipedon pleuralis in a Piedmont creek, with comments on its population structure. Master thesis, Georgia College

  • Langeland A, L’Abée-Lund JH, Jonsson B, Jonsson N (1991) Resource partitioning and niche shift in Arctic charr Salvelinus alpinus and brown trout Salmo trutta. J Anim Ecol 60:895–912

    Google Scholar 

  • Lasky JR, Yang J, Zhang G et al (2014) The role of functional traits and individual variation in the co-occurrence of Ficus species. Ecology 95:978–990

    PubMed  Google Scholar 

  • Laurent EJ, Kingsbury BA (2003) Habitat separation among three species of water snakes in northwestern Kentucky. J Herpetol 37:229–235

    Google Scholar 

  • Lichstein JW, Dushoff J, Levin SA, Pacala SW (2007) Intraspecific variation and species coexistence. Am Nat 170:807–818

    PubMed  Google Scholar 

  • Lürig MD, Best RJ, Stachowicz JJ (2016) Microhabitat partitioning in seagrass mesograzers is driven by consistent species choices across multiple predator and competitor contexts. Oikos 125:1324–1333

    Google Scholar 

  • MacArthur RH (1958) Population ecology of some warblers of northeastern coniferous forests. Ecology 39:599–619

    Google Scholar 

  • MacArthur R, Levins R (1967) The limiting similarity, convergence, and divergence of coexisting species. Am Nat 101:377–385

    Google Scholar 

  • Marshall JC Jr (2008) Population genetics and landscape modeling in water snakes. Dissertation. Purdue University

  • Mata VA, Amorim F, Corley MFV et al (2016) Female dietary bias towards large migratory moths in the European free-tailed bat (Tadarida teniotis). Biol Lett 12:20150988

    PubMed  PubMed Central  Google Scholar 

  • McDiarmid RW, Altig R (1999) Tadpoles: the biology of anuran larvae. The University of Chicago Press, Chicago

    Google Scholar 

  • McVay JD, Flores-Villela O, Carstens B (2015) Diversification of North American natricine snakes. Biol J Linn Soc 116:1–12

    Google Scholar 

  • Milanovich JR, Maerz JC (2012) Assessing the use of non-lethal tail clips for measuring stable isotopes of plethodontid salamanders. Herpetol Conserv Biol 7:67–74

    Google Scholar 

  • Mushinsky HR, Hebrard JJ (1977) Food partitioning by five species of water snakes in Louisiana. Herpetologica 33:162–166

    Google Scholar 

  • Mushinsky HR, Lotz KH (1980) Chemoreceptive responses of two sympatric water snakes to to extracts of commonly ingested prey species. J Chem Ecol 6:523–535

    Google Scholar 

  • Mushinsky HR, Hebrard JJ, Vodopich DS (1982) Ontogeny of water snake foraging ecology. Ecology 63:1624–1629

    Google Scholar 

  • Nakazawa T (2015) Ontogenetic niche shifts matter in community ecology: a review and future perspectives. Popul Ecol 57:347–354

    Google Scholar 

  • Neuman-Lee LA, Durso AM, Kiriazis NM et al (2013) Differential habitat use by common watersnakes (Nerodia sipedon). IRCF Reptil Amphib 20:166–171

    Google Scholar 

  • Olson MH (1996) Ontogenetic niche shifts in largemouth bass: variability and consequences for first-year growth. Ecology 77:179–190

    Google Scholar 

  • Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5:e9672

    PubMed  PubMed Central  Google Scholar 

  • Pattishall A, Cundall D (2009) Habitat use by synurbic watersnakes (Nerodia sipedon). Herpetologica 65:183–198

    Google Scholar 

  • Pekár S, Martišová M, Bilde T (2011) Intersexual trophic niche partitioning in an ant-eating spider (Araneae: Zodariidae). PLoS ONE 6:e14603

    PubMed  PubMed Central  Google Scholar 

  • Perkins MW, Eason PK (2019) The relationship of head morphology and diet among three sympatric watersnake species. Amphibia-Reptilia 40:65–77

    Google Scholar 

  • Pianka ER (1973) The structure of lizard communities. Annu Rev Ecol Syst 4:53–74

    Google Scholar 

  • Pianka ER (1975) Niche relations of desert lizards. In: Cody ML, Diamond JM (eds) Ecology and evolution of communities. The Belknap Press of Harvard University, Cambridge, pp 292–314

    Google Scholar 

  • Plummer MV, Ferner JW (2012) Marking reptiles. In: McDiarmid W, Foster MS, Guyer C et al (eds) Reptile biodiversity: standard methods for inventory and monitoring. University of California Press, Berkeley, pp 143–150

    Google Scholar 

  • Plummer MV, Goy JM (1984) Ontogenetic dietary shift of water snakes (Nerodia rhombifera) in a fish hatchery. Copeia 2:550–552

    Google Scholar 

  • Preston WB (1970) The comparative ecology of two water snakes, Natrix rhombifera and Natrix erythrogaster in Oklahoma. Dissertation, University of Oklahoma

  • Rasmussen JB (2010) Estimating terrestrial contribution to stream invertebrates and periphyton using a gradient-based mixing model for δ13C. J Anim Ecol 79:393–402

    PubMed  Google Scholar 

  • Roe JH, Kingsbury BA, Herbert NR (2004) Comparative water snake ecology: conservation of mobile animals that use temporally dynamic resources. Biol Conserv 118:79–89

    Google Scholar 

  • Roughgarden J (1976) Resource partitioning among competing species—a coevolutionary approach. Theor Popul Biol 9:388–424

    CAS  PubMed  Google Scholar 

  • Rudolf VHW, Rasmussen NL (2013) Ontogenetic functional diversity: size structure of a keystone predator drives functioning of a complex ecosystem. Ecology 94:1046–1056

    PubMed  Google Scholar 

  • Sabatés A, Saiz E (2000) Intra- and interspecific variability in prey size and niche breadth of myctophiform fish larvae. Mar Ecol Prog Ser 201:261–271

    Google Scholar 

  • Samplonius JM, Kappers EF, Brands S, Both C (2016) Phenological mismatch and ontogenetic diet shifts interactively affect offspring condition in a passerine. J Anim Ecol 85:1255–1264

    PubMed  Google Scholar 

  • Sanderson BL, Tran CD, Coe HJ et al (2009) Nonlethal sampling of fish caudal fins yields valuable stable isotope data for threatened and endangered fishes. Trans Am Fish Soc 138:1166–1177

    Google Scholar 

  • SAS Institute (2000) SAS. Version 9.0. SAS Institute, Cary

    Google Scholar 

  • Savitsky BAC (1989) Aquatic foraging in two independently evolved species of snake: Nerodia rhombifera (Colubridae) and Agkistrodon piscivorus (Viperidae). Dissertation, The University of Tennessee

  • Schoener TW (1968) The Anolis lizards of Bimini: resource partitioning in a complex fauna. Ecology 49:704–726

    Google Scholar 

  • Schoener TW (1974) Resource partitioning in ecological communities. Science 185:27–39

    CAS  PubMed  Google Scholar 

  • Seminoff JA, Jones TT, Eguchi T et al (2006) Stable isotope discrimination (δ13C and δ15N) between soft tissues of the green sea turtle Chelonia mydas and its diet. Mar Ecol Prog Ser 308:271–278

    CAS  Google Scholar 

  • Sheppard CE, Inger R, McDonald RA et al (2018) Intragroup competition predicts individual foraging specialisation in a group-living mammal. Ecol Lett 21:665–673

    PubMed  PubMed Central  Google Scholar 

  • Shine R, Wall M (2007) Why is intraspecific niche partitioning more common in snakes than in lizards. In: Reilly SM, McBayer LD, Miles DB (eds) Lizard ecology: the evolutionary consequences of foraging mode. Cambridge University Press, New York, pp 173–208

    Google Scholar 

  • Steen DA, McClure CJW, Brock JC et al (2014) Snake co-occurrence patterns are best explained by habitat and hypothesized effects of interspecific interactions. J Anim Ecol 83:286–295

    PubMed  Google Scholar 

  • Stephens PR, Wiens JJ (2009) Evolution of sexual size dimorphisms in emydid turtles: ecological dimorphism, Rensch’s rule, and sympatric divergence. Evolution 63:910–925

    PubMed  Google Scholar 

  • Svanbäck R, Bolnick DI (2005) Intraspecific competition affects the strength of individual specialization: an optimal diet theory method. Evol Ecol Res 7:993–1012

    Google Scholar 

  • Trakimas G, Jardine TD, Barisevičiūtė R et al (2011) Ontogenetic dietary shifts in European common frog (Rana temporaria) revealed by stable isotopes. Hydrobiologia 675:87–95

    Google Scholar 

  • Tronquart NH, Mazeas L, Reuilly-Manenti L et al (2012) Fish fins as non-lethal surrogates for muscle tissues in freshwater food web studies using stable isotopes. Rapid Commun Mass Spectrom 26:1603–1608

    CAS  Google Scholar 

  • Tucker JK (1995) Notes on road-killed snakes and their implications on habitat modification due to summer flooding on the Mississippi River in west central Illinois. Trans IL State Acad Sci 88:61–71

    Google Scholar 

  • van Beest FM, McLoughlin PD, Vander Wal E, Brook RK (2014) Density-dependent habitat selection and partitioning between two sympatric ungulates. Oecologia 175:1155–1165

    PubMed  Google Scholar 

  • Vassilieva AB, Sinev AY, Tiunov AV (2017) Trophic segregation of anuran larvae in two temporary tropical ponds in southern Vietnam. Herpetol J 27:217–229

    Google Scholar 

  • Voigt CC, Krofel M, Menges V et al (2018) Sex-specific dietary specialization in a terrestrial apex predator, the leopard, revealed by stable isotope analysis. J Zool 306:1–7

    Google Scholar 

  • Willson JD, Winne CT, Pilgrim MA et al (2010) Seasonal variation in terrestrial resource subsidies influences trophic niche width and overlap in two aquatic snake species: a stable isotope approach. Oikos 119:1161–1171

    Google Scholar 

  • Woo KJ, Elliott KH, Davidson M et al (2008) Individual specialization in diet by a generalist marine predator reflects specialization in foraging behaviour. J Anim Ecol 77:1082–1091

    PubMed  Google Scholar 

  • Zalewski A (2007) Does size dimorphism reduce competition between sexes? The diet of male male and female pine martens at local and wider geographical scales. Acta Theriol 52:237–250

    Google Scholar 

  • Zeug SC, Winemiller KO (2008) Evidence supporting the importance of terrestrial carbon in a large-river food web. Ecol 89:1733–1743

    Google Scholar 

Download references

Acknowledgements

We thank Jenny Perkins for comments on an earlier version of this manuscript. We thank L. Beard, J. Martin, B. Newton, J. Guinto, E. Clark, M. Alschbach, D. Perkins, I. Perkins, R. Perkins, J. Perkins and Z. Humphrey for assistance in field data collection. We thank Kentucky Department of Fish and Wildlife Resources for research site access. This research was funded by University of Louisville, Watershed Studies Institute (Murray State University), Greater Cincinnati Herpetological Society, Chicago Herpetological Society, Kentucky Society of Natural History and The Kentucky Chapter of The Wildlife Society. This work conforms to the legal requirements in the U.S.A., and we obtained all necessary permits. We followed all University of Louisville Institutional Animal Care Use Committee guidelines (Protocol: #13037).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Micah W. Perkins.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 61 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Perkins, M.W., Cloyed, C.S. & Eason, P.K. Intraspecific dietary variation in niche partitioning within a community of ecologically similar snakes. Evol Ecol 34, 1017–1035 (2020). https://doi.org/10.1007/s10682-020-10078-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-020-10078-6

Keywords

Navigation