Specialization directs habitat selection responses to a top predator in semiaquatic but not aquatic taxa
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
34556794
PubMed Central
PMC8460784
DOI
10.1038/s41598-021-98632-2
PII: 10.1038/s41598-021-98632-2
Knihovny.cz E-zdroje
- MeSH
- brouci MeSH
- býložravci fyziologie MeSH
- potravní řetězec * MeSH
- predátorské chování fyziologie MeSH
- ropuchy MeSH
- rozšíření zvířat fyziologie MeSH
- ryby MeSH
- sladká voda MeSH
- vážky MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Habitat selectivity has become an increasingly acknowledged mechanism shaping the structure of freshwater communities; however, most studies have focused on the effect of predators and competitors, neglecting habitat complexity and specialization. In this study, we examined the habitat selection of semiaquatic (amphibians: Bufonidae; odonates: Libellulidae) and aquatic organisms (true bugs: Notonectidae; diving beetles: Dytiscidae). From each family, we selected one habitat generalist species able to coexist with fish (Bufo bufo, Sympetrum sanguineum, Notonecta glauca, Dytiscus marginalis) and one species specialized in fishless habitats (Bufotes viridis, Sympetrum danae, Notonecta obliqua, Acilius sulcatus). In a mesocosm experiment, we quantified habitat selection decisions in response to the non-consumptive presence of fish (Carassius auratus) and vegetation structure mimicking different successional stages of aquatic habitats (no macrophytes; submerged and floating macrophytes; submerged, floating, and littoral-emergent macrophytes). No congruence between habitat specialists and generalists was observed, but a similar response to fish and vegetation structure defined both semiaquatic and aquatic organisms. While semiaquatic generalists did not distinguish between fish and fishless pools, specialists avoided fish-occupied pools and had a preferred vegetation structure. In aquatic taxa, predator presence affected habitat selection only in combination with vegetation structure, and all species preferred fishless pools with floating and submerged macrophytes. Fish presence triggered avoidance only in the generalist bug N. glauca. Our results highlight the significance of habitat selectivity for structuring freshwater ecosystems and illustrate how habitat selection responses to a top predator are dictated by specialization and life history.
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Binckley CA, Resetarits WJ. Habitat selection determines abundance, richness and species composition of beetles in aquatic communities. Biol. Lett. 2005;1:370–374. doi: 10.1098/rsbl.2005.0310. PubMed DOI PMC
Foltz SJ, Dodson SI. Aquatic Hemiptera community structure in stormwater retention ponds: A watershed land cover approach. Hydrobiologia. 2009;621:49–62. doi: 10.1007/s10750-008-9631-6. DOI
Goldberg FJ, Quinzio S, Vaira M. Oviposition-site selection by the toad Melanophryniscus rubriventris in an unpredictable environment in Argentina. Can. J. Zool. 2006;84:699–705. doi: 10.1139/z06-038. DOI
Blaustein, L. Oviposition site selection in response to risk of predation: Evidence from aquatic habitats and consequences for population dynamics and community. In Evolutionary Theory and Processes: Modern Perspectives (ed. Wasser, S. P.) 441–456 (Kluwer, 1999).
Resetarits WJ, Binckley CA. Spatial contagion of predation risk affects colonization dynamics in experimental aquatic landscapes. Ecology. 2009;90:869–876. doi: 10.1890/08-0613.1. PubMed DOI
Kraus JM, Vonesh JR. Feedbacks between community assembly and habitat selection shape variation in local colonization. J. Anim. Ecol. 2010;79:795–802. PubMed
Resetarits WJ. Oviposition site choice and life history evolution. Am. Zool. 1996;36:205–215. doi: 10.1093/icb/36.2.205. DOI
Morris DW. Toward an ecological synthesis: A case for habitat selection. Oecologia. 2003;136:1–13. doi: 10.1007/s00442-003-1241-4. PubMed DOI
Resetarits WJ, Wilbur HM. Choice of oviposition site by Hyla chrysoscelis: Role of predators and competitors. Ecology. 1989;70:220–228. doi: 10.2307/1938428. DOI
Resetarits, W. J., Binckley, C. A. & Chalcraft, D. R. Habitat selection, species interactions, and processes of community assembly in complex landscapes: A metacommunity perspective. In Metacommunities: Spatial Dynamics and Ecological Communities (eds. Holyoak, M., Leybold, A. & Holt, R. D.) 374–398 (University of Chicago Press, Chicago, 2005).
Lima SL, Dill LM. Behavioral decisions made under the risk of predation: A review and prospectus. Can. J. Zool. 1990;68:619–640. doi: 10.1139/z90-092. DOI
Langellotto GA, Denno RF. Responses of invertebrate natural enemies to complex-structured habitats: A meta-analytical synthesis. Oecologia. 2004;139:1–10. doi: 10.1007/s00442-004-1497-3. PubMed DOI
Åbjörnsson K, Brönmark C, Hansson L-A. The relative importance of lethal and non-lethal effects of fish on insect colonisation of ponds: Influence of fish on insect colonisation. Freshw. Biol. 2002;47:1489–1495. doi: 10.1046/j.1365-2427.2002.00883.x. DOI
Pintar MR, Resetarits WJ., Jr Out with the old, in with the new: Oviposition preference matches larval success in cope’s gray treefrog, Hyla chrysoscelis. J. Herpetol. 2017;51:186–189. doi: 10.1670/16-019. DOI
Wellborn GA, Skelly DK, Werner EE. Mechanisms creating community structure across a freshwater habitat gradient. Annu. Rev. Ecol. Evol. Syst. 1996;27:337–363. doi: 10.1146/annurev.ecolsys.27.1.337. DOI
Caudill CC, Peckarsky BL. Lack of appropriate behavioral or developmental responses by mayfly larvae to trout predators. Ecology. 2003;84:2133–2144. doi: 10.1890/0012-9658(2003)084[2133:LOABOD]2.0.CO;2. DOI
Binckley CA, Resetarits WJ. Functional equivalence of non-lethal effects: Generalized fish avoidance determines distribution of gray treefrog, Hyla chrysoscelis, larvae. Oikos. 2003;102:623–629. doi: 10.1034/j.1600-0706.2003.12483.x. DOI
Pollard CJ, et al. Removal of an exotic fish influences amphibian breeding site selection: Exotic fish removal. J. Wildl. Manag. 2017;81:720–727. doi: 10.1002/jwmg.21232. DOI
Petranka JW, Fakhoury K. Evidence of a chemically-mediated avoidance response of ovipositing insects to bluegills and green frog tadpoles. Copeia. 1991;1991:234–239. doi: 10.2307/1446271. DOI
McPeek MA. Differential dispersal tendencies among Enallagma damselflies (Odonata) inhabiting different habitats. Oikos. 1989;56:187–195. doi: 10.2307/3565335. DOI
Šigutová H, Šigut M, Dolný A. Intensive fish ponds as ecological traps for dragonflies: An imminent threat to the endangered species Sympetrum depressiusculum (Odonata: Libellulidae) J. Insect Conserv. 2015;19:961–974. doi: 10.1007/s10841-015-9813-2. DOI
Potts, K. M. Survival and development of larval odonates (Anisoptera) and female oviposition site choice in response to predatory fish. https://egrove.olemiss.edu/etd/1854 (2020).
Blaustein L, Kiflawi M, Eitam A, Mangel M, Cohen JE. Oviposition habitat selection in response to risk of predation in temporary pools: Mode of detection and consistency across experimental venue. Oecologia. 2004;138:300–305. doi: 10.1007/s00442-003-1398-x. PubMed DOI
Wildermuth, H. Habitat selection and oviposition site recognition by the dragonfly Aeshna juncea (L.): An experimental approach in natural habitats (Anisoptera: Aeshnidae). Odonatologica22, 27–44 (1993).
Wildermuth H. Habitatselektion bei Libellen. Adv. Odonatol. 1994;6:223–257.
Laurila A. Breeding habitat selection and larval performance of two anurans in freshwater rock-pools. Ecography. 1998;21:484–494. doi: 10.1111/j.1600-0587.1998.tb00440.x. DOI
Schwind R. Spectral regions in which aquatic insects see reflected polarized light. J. Comp. Physiol. A. 1995;177:439–448. doi: 10.1007/BF00187480. DOI
Horváth, G. & Kriska, G. Polarization vision in aquatic insects and ecological traps for polarotactic insects in Aquatic Insects: Challenges to Populations (eds. Lancaster, J. & Briers, R. A.) 204–229 (CAB International Publishing, 2008).
Schulte LM, et al. The smell of success: Choice of larval rearing sites by means of chemical cues in a Peruvian poison frog. Anim. Behav. 2011;81:1147–1154. doi: 10.1016/j.anbehav.2011.02.019. DOI
Corbet, P. S. Dragonflies: Behavior and ecology of Odonata. (Harley Books, 1999).
Nicolet P, et al. The wetland plant and macroinvertebrate assemblages of temporary ponds in England and Wales. Biol. Conserv. 2004;120:261–278. doi: 10.1016/j.biocon.2004.03.010. DOI
Henrikson B-I. Sphagnum mosses as a microhabitat for invertebrates in acidified lakes and the colour adaptation and substrate preference in Leucorrhinia dubia (Odonata, Anisoptera) Ecography. 1993;16:143–153. doi: 10.1111/j.1600-0587.1993.tb00066.x. DOI
Kokko H, Sutherland WJ. Ecological traps in changing environments: Ecological and evolutionary consequences of a behaviourally mediated Allee effect. Evol. Ecol. Res. 2001;3:537–551.
Gilroy JJ, Sutherland WJ. Beyond ecological traps: Perceptual errors and undervalued resources. Trends Ecol. Evol. 2007;22:351–356. doi: 10.1016/j.tree.2007.03.014. PubMed DOI
Abrams PA, Cressman R, Křivan V. The role of behavioral dynamics in determining the patch distributions of interacting species. Am. Nat. 2007;169:505–518. doi: 10.1086/511963. PubMed DOI
Denton J, Beebee TJC. Palatability of anuran eggs and embryos. Amphib. Reptil. 1991;12:111–112. doi: 10.1163/156853891X00374. DOI
Larson DJ. The predaceous water beetles (Coleoptera: Dytiscidae) of Alberta: Systematics, natural history and distribution. Quaest. Entomol. 1985;11:245–498.
Mikolajewski DJ, Rolff J. Benefits of morphological defence demonstrated by direct manipulation in larval dragonflies. Evol. Ecol. Res. 2004;6:619–626.
Relyea RA. Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology. 2001;82:523–540. doi: 10.1890/0012-9658(2001)082[0523:MABPOL]2.0.CO;2. DOI
Benard MF. Predator-induced phenotypic plasticity in organisms with complex life histories. Annu. Rev. Ecol. Evol. Syst. 2004;35:651–673. doi: 10.1146/annurev.ecolsys.35.021004.112426. DOI
McCauley SJ, Davis CJ, Werner EE. Predator induction of spine length in larval Leucorrhinia intacta (Odonata) Evol. Ecol. Res. 2008;10:435–447.
Nöllert, A. & Nöllert, C. Die Amphibien Europas. (Franckh-Kosmos Verlags-GmbH and Company, 1992).
Maštera, J., Zavadil, V. & Dvořák, J. Vajíčka a larvy obojživelníků České republiky. (Academia, 2015).
Speybroeck, J., Beukema, W., Bok, B. & Van der Voort, J. Field Guide to the Amphibians and Reptiles of Britain and Europe. (Bloomsbury Natural History, 2016).
Sternberg, K. & Buchwald, R. Die Libellen Baden-Württembergs. Band 2: Großlibellen (Anisoptera). (Verlag Eugen Ulmer Gmbh & Co., 2000).
Mikolajewski DJ, Johansson F. Morphological and behavioral defenses in dragonfly larvae: Trait compensation and cospecialization. Behav. Ecol. 2004;15:614–620. doi: 10.1093/beheco/arh061. DOI
Kjærstad G, Dolmen D, Olsvik HA, Tilseth E. The backswimmer Notonecta glauca L. (Hemiptera, Notonectidae) in Central Norway. Nor. J. Entomol. 2009;56:44–49.
Svensson BG, Tallmark B, Petersson E. Habitat heterogeneity, coexistence and habitat utilization in five backswimmer species (Notonecta spp.; Hemiptera, Notonectidae) Aquat. Insects. 2000;22:81–98. doi: 10.1076/0165-0424(200004)22:2;1-P;FT081. DOI
Macan TT. A twenty-one-year study of the water-bugs in a Moorland Fishpond. J. Anim. Ecol. 1976;45:913–922. doi: 10.2307/3589. DOI
Lock K, Adriaens T, Meutter FVD, Goethals P. Effect of water quality on waterbugs (Hemiptera: Gerromorpha & Nepomorpha) in Flanders (Belgium): Results from a large-scale field survey. Ann. Limnol. Int. J. Limnol. 2013;49:121–128. doi: 10.1051/limn/2013047. DOI
Cook WL, Streams FA. Fish predation on Notonecta (Hemiptera): Relationship between prey risk and habitat utilization. Oecologia. 1984;64:177–183. doi: 10.1007/BF00376868. PubMed DOI
Swevers L, Lambert JGD, De Loof A. Synthesis and metabolism of vertebrate-type steroids by tissues of insects: A critical evaluation. Experientia. 1991;47:687–698. doi: 10.1007/BF01958817. PubMed DOI
Bergsten J, Miller KB. Taxonomic revision of the Holarctic diving beetle genus Acilius Leach (Coleoptera: Dytiscidae): Acilius taxonomic revision. Syst. Entomol. 2005;31:145–197. doi: 10.1111/j.1365-3113.2005.00309.x. DOI
Åbjörnsson K, Wagner BMA, Axelsson A, Bjerselius R, Olsén KH. Responses of Acilius sulcatus (Coleoptera: Dytiscidae) to chemical cues from perch (Perca fluviatilis) Oecologia. 1997;111:166–171. doi: 10.1007/s004420050221. PubMed DOI
Boukal DS, et al. Catalogue of water beetles of the Czech Republic. Klapalekiana. 2007;43(Suppl.):1–289.
Gioria M, Schaffers A, Bacaro G, Feehan J. The conservation value of farmland ponds: Predicting water beetle assemblages using vascular plants as a surrogate group. Biol. Conserv. 2010;143:1125–1133. doi: 10.1016/j.biocon.2010.02.007. DOI
Everard, M. Britain’s Freshwater Fishes. (Princeton University Press, 2013).
Briers RA, Warren PH. Competition between the nymphs of two regionally co-occurring species of Notonecta (Hemiptera: Notonectidae) Freshw. Biol. 1999;42:11–20. doi: 10.1046/j.1365-2427.1999.00448.x. DOI
Wiggins GB, Mackay RJ, Smith IM. Evolutionary and ecological strategies of animals on annual temporary pools. Arch. Für Hydrobiol. Suppl. 1980;58:197–206.
Culler, L. E., Ohba, S. & Crumrine, P. Predator-Prey Interactions of Dytiscids. In Ecology, Systematics, and the Natural History of Predaceous Diving Beetles (Coleoptera: Dytiscidae) (ed. Yee, D. A.) 363–379 (Springer, 2014).
Schuh RT, Slater JA. True Bugs of the World (Hemiptera:Heteroptera): Classification and Natural History. Cornell: Cornell University Press; 1995.
Streams FA. Intrageneric predation by Notonecta (Hemiptera: Notonectidae) in the laboratory and in nature. Ann. Entomol. Soc. Am. 1992;85:265–273. doi: 10.1093/aesa/85.3.265. DOI
Giacoma C, Zugolaro C, Beani L. The advertisement calls of the green toad (Bufo viridis): Variability and role in mate choice. Herpetologica. 1997;53:454–464.
Pekár S, Brabec M. Generalized estimating equations: A pragmatic and flexible approach to the marginal GLM modelling of correlated data in the behavioural sciences. Ethology. 2018;124:86–93. doi: 10.1111/eth.12713. DOI
Halekoh U, Højsgaard S, Yan J. The R Package geepack for generalized estimating equations. J. Stat. Softw. 2006;15:1–11. doi: 10.18637/jss.v015.i02. DOI
R Core Team. R: A Language and Environment for Statistical Computing (The R Foundation for Statistical Computing, Vienna, Austria). https://www.r-project.org/ (2020).
Wells, K. D. The Ecology and Behavior of Amphibians. (University of Chicago Press, 2007).
Purrenhage JL, Boone MD. Amphibian community response to variation in habitat structure and competitor density. Herpetologica. 2009;65:14–30. doi: 10.1655/08-017R1.1. DOI
Formanowicz DR, Bobka MS. Predation risk and microhabitat preference: An experimental study of the behavioral responses of prey and predator. Am. Midl. Nat. 1989;121:379–386. doi: 10.2307/2426042. DOI
Egan RS, Paton PWC. Within-pond parameters affecting oviposition by wood frogs and spotted salamanders. Wetlands. 2004;24:1–13. doi: 10.1672/0277-5212(2004)024[0001:WPAOBW]2.0.CO;2. DOI
Ward SA. Optimal habitat selection in time-limited dispersers. Am. Nat. 1987;129:568–579. doi: 10.1086/284658. DOI
Fretwell SD, Lucas HL. On territorial behavior and other factors influencing habitat distribution in birds. I. Theoretical development. Biotheoretica. 1970;19:16–36. doi: 10.1007/BF01601953. DOI
Austad SN. A classification of alternative reproductive behaviors and methods for field-testing ESS models. Am. Zool. 1984;24:309–319. doi: 10.1093/icb/24.2.309. DOI
Crespo JG. A review of chemosensation and related behavior in aquatic insects. J. Insect Sci. 2011;11:1–39. doi: 10.1673/031.011.6201. PubMed DOI PMC
Wildermuth H. Dragonflies recognize the water of rendezvous and oviposition sites by horizontally polarized light: A behavioural field test. Naturwissenschaften. 1998;85:297–302. doi: 10.1007/s001140050504. DOI
Chislock MF, Doster E, Zitomer RA, Wilson AE. Eutrophication: Causes, consequences, and controls in aquatic ecosystems. Nat. Educ. Knowl. 2013;4:10.
Dolný A, Mižičová H, Harabiš F. Natal philopatry in four European species of dragonflies (Odonata: Sympetrinae) and possible implications for conservation management. J. Insect Conserv. 2013;17:821–829. doi: 10.1007/s10841-013-9564-x. DOI
Refsnider JM, Janzen FJ. Putting eggs in one basket: Ecological and evolutionary hypotheses for variation in oviposition-site choice. Annu. Rev. Ecol. Evol. Syst. 2010;41:39–57. doi: 10.1146/annurev-ecolsys-102209-144712. DOI
Brodin T, Mikolajewski DJ, Johansson F. Behavioural and life history effects of predator diet cues during ontogeny in damselfly larvae. Oecologia. 2006;148:162–169. doi: 10.1007/s00442-005-0334-7. PubMed DOI
Kershenbaum A, Spencer M, Blaustein L, Cohen JE. Modelling evolutionarily stable strategies in oviposition site selection, with varying risks of predation and intraspecific competition. Evol. Ecol. 2012;26:955–974. doi: 10.1007/s10682-011-9548-9. DOI
Hopper KR. Risk-spreading and bet-hedging in insect population biology. Annu. Rev. Entomol. 1999;44:535–560. doi: 10.1146/annurev.ento.44.1.535. PubMed DOI
Gioria M. Habitats. In: Yee DA, editor. Ecology, Systematics, and the Natural History of predaceous diving beetles (Coleoptera: Dytiscidae) Netherlands: Springer; 2014. pp. 307–362.
Diehl S. Fish predation and benthic community structure: The role of omnivory and habitat complexity. Ecology. 1992;73:1646–1661. doi: 10.2307/1940017. DOI
Giller PS, McNeill S. Predation strategies, resource partitioning and habitat selection in Notonecta (Hemiptera/Heteroptera) J. Anim. Ecol. 1981;50:789–808. doi: 10.2307/4137. DOI
Ribera I, Nilsson AN. Morphometric patterns among diving beetles (Coleoptera: Noteridae, Hygrobiidae, and Dytiscidae) Can. J. Zool. 2011;73:2343–2360. doi: 10.1139/z95-275. DOI
Roberts G. Why individual vigilance declines as group size increases. Anim. Behav. 1996;51:1077–1086. doi: 10.1006/anbe.1996.0109. DOI
Schoeppner NM, Relyea RA. Damage, digestion, and defence: The roles of alarm cues and kairomones for inducing prey defences. Ecol. Lett. 2005;8:505–512. doi: 10.1111/j.1461-0248.2005.00744.x. PubMed DOI
Schoeppner NM, Relyea RA. Interpreting the smells of predation: How alarm cues and kairomones induce different prey defences. Funct. Ecol. 2009;23:1114–1121. doi: 10.1111/j.1365-2435.2009.01578.x. DOI
McCauley SJ, Rowe L. Notonecta exhibit threat-sensitive, predator-induced dispersal. Biol. Lett. 2010;6:449–452. doi: 10.1098/rsbl.2009.1082. PubMed DOI PMC
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