Abstract
Almost all organisms on Earth exhibit ontogenetic niche shifts, which causes great phenotypic variation among individuals and is thus considered to critically mediate community structure and dynamics. In contrast, community ecology has traditionally assumed that species are composed of identical individuals with invariant traits and ignored the potentially important ecological roles of ontogenetic niche shifts. To bridge the gap, here I briefly review ecologically relevant examples which show that basic insights of species-based community theories can be revised by including the ontogenetic perspective. Specifically, I focus on the most representative animals in the study of ontogenetic niche shifts, i.e., fish, insects, and amphibians. Notably, their ontogenetic niche shifts create novel views of community structure: (1) ontogenetic diet shifts of predatory fish couple pelagic and benthic food webs in aquatic systems, (2) ontogenetic shifts in interaction types of pollinating insects couple herbivory and pollination networks in terrestrial systems, and (3) ontogenetic habitat shifts of amphibians and aquatic insects couple aquatic and terrestrial metacommunities at interface areas. Dynamic models of such stage-structured communities suggest that their ontogenetic niche shifts may affect the community resilience and disturbance responses. Exploring more complex systems (e.g., where many species undergo ontogenetic niche shifts several times or continuously) is a future direction, for which describing body size relationships between interacting organisms would be a promising approach. I conclude that both theoretical and empirical advances are needed to facilitate the ontogenetic perspective for better understanding mechanisms underlying biodiversity and ecosystem functioning which are increasingly threatened by anthropogenic disturbance.
Similar content being viewed by others
References
Altermatt F, Pearse IS (2011) Similarity and specialization of the larval versus adult diet of European butterflies and moths. Am Nat 178:372–382
Armsworth PR, Roughgarden JE (2005) The impact of directed versus random movement on population dynamics and biodiversity patterns. Am Nat 165:449–465
Attayde JL, Ripa J (2008) The coupling between grazing and detritus food chains and the strength of trophic cascades across a gradient of nutrient enrichment. Ecosystems 11:980–990
Baxter CV, Fausch KD, Saunders WC (2005) Tangled webs: reciprocal flows of invertebrate prey link streams and riparian zones. Freshwat Biol 50:201–220
Begon M, Townsend CR, Harper JL (2006) Ecology: from individuals to ecosystems, 4th edn. Blackwell, Oxford
Blanchard JL, Jennings S, Law R, Castle MD, McCloghrie P, Rochet M-J, Benoît E (2009) How does abundance scale with body size in coupled size-structured food webs? J Anim Ecol 78:270–280
Boege K, Barton KE, Dirzo R (2011) Influence of tree ontogeny on plant-herbivore interactions. In: Meinzer FC, Lachenbruch B, Dawson TE (eds) Size- and age-related changes in tree structure and function. Springer, Netherlands, Dordrecht, pp 132–214
Bohonak AJ, Jenkins DG (2003) Ecological and evolutionary significance of dispersal by freshwater invertebrates. Ecol Lett 6:783–796
Briones JC, Tsai CH, Nakazawa T, Sakai Y, Papa RD, Hsieh CH, Okuda N (2012) Long-term changes in the diet of Gymnogobius isaza from Lake Biwa, Japan: effects of body size and environmental prey availability. PLoS One 7:e53167
Bronstein JL, Huxman T, Horvath B, Farabee M, Davidowitz G (2009) Reproductive biology of Datura Wrightii: the benefits of a herbivorous pollinator. Ann Bot 103:1435–1443
Brose U (2010) Body-mass constraints on foraging behaviour determine population and food-web dynamics. Funct Ecol 24:28–34
Brose U, Jonsson T, Berlow EL, Warren P, Banasek-Richter C, Bersier LF, Blanchard JL, Brey T, Carpenter SR, Blandenier MF, Cushing L, Dawah HA, Dell T, Edwards F, Harper-Smith S, Jacob U, Ledger ME, Martinez ND, Memmott J, Mintenbeck K, Pinnegar JK, Rall BC, Rayner TS, Reuman DC, Ruess L, Ulrich W, Williams RJ, Woodward G, Cohen JE (2006) Consumer-resource body-size relationships in natural food webs. Ecology 87:2411–2417
Cohen JE, Jonsson T, Müller CB, Godfray HC, Savage VM (2005) Body sizes of hosts and parasitoids in individual feeding relationships. Proc Natl Acad Sci USA 102:684–689
de Roos AM, Persson L (2013) Population and community ecology of ontogenetic development. Princeton University Press, Princeton
de Roos AM, Leonardsson K, Persson L, Mittelbach GG (2002) Ontogenetic niche shifts and flexible behaviour in size-structured populations. Ecol Mon 72:271–292
Dudgeon D, Arthington AH, Gessner MO, Kawabata Z-I, Knowler DJ, Lévêque C, Naiman RJ, Prieur-Richard A-H, Soto D, Stiassny MLJ, Sullivan CA (2006) Freshwater biodiversity: importance, threats, status and conservation challenges. Biol Rev 81:163–182
Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Annu Rev Ecol Evol Syst 35:375–403
Fontaine C, Guimarães PR, Kéfi S, Loeuille N, Memmott J, van der Putten WH, van Veen FJF, Thébault E (2011) The ecological and evolutionary implications of merging different types of networks. Ecol Lett 14:1170–1181
Fretwell SD (1987) Food chain dynamics: the central theory of ecology? Oikos 50:291–301
Futuyma DJ, Agrawal AA (2009) Macroevolution and the biological diversity of plants and herbivores. Proc Natl Acad Sci USA 106:18054–18061
Gaston KJ, Blackburn TM (2000) Pattern and process in macroecology. Blackwell, Oxford
Gende SM, Edwards RT, Willson MF, Wipfli MS (2002) Pacific salmon in aquatic and terrestrial ecosystems. Bioscience 52:917–928
Guill C (2009) Alternative dynamical states in stage-structured consumer populations. Theor Popul Biol 76:168–178
Hansson LA (1988) Effects of competitive interactions on the biomass development of planktonic and periphytic algae in lakes. Limnol Oceanogr 33:121–128
Hartvig M, Andersen KH, Beyer JE (2011) Food web framework for size-structured populations. J Theor Biol 272:113–122
Hauzy C, Gauduchon M, Hulot FD, Loreau M (2010) Density-dependent dispersal and relative dispersal affect the stability of predator-prey metacommunities. J Theor Biol 266:458–469
Hildrew AG, Raffaelli DR, Edmonds-Brown R (2007) Body size: the structure and function of aquatic ecosystems. Cambridge University Press, Cambridge
Holyoak M, Leibold MA, Holt RD (2005) Metacommunities: spatial dynamics and ecological communities. University of Chicago Press, Chicago
Jeppesen E, Jensen JP, Jensen C, Faafeng B, Hessen DO, Søndergaard M, Lauridsen T, Brettum P, Christoffersen K (2003) The impact of nutrient state and lake depth on top-down control in the pelagic zone of lakes: a study of 466 lakes from the temperate zone to the arctic. Ecosystems 6:313–325
Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant-pollinator interactions. Annu Rev Ecol Syst 29:83–112
Knight TM, McCoy MW, Chase JM, McCoy KA, Holt RD (2005) Trophic cascades across ecosystems. Nature 437:880–883
Kondoh M (2003) Foraging adaptation and the relationship between food-web complexity and stability. Science 299:1388–1391
Lannoo MJ (2005) Amphibian declines: the conservation status of United States species. University of California Press, Berkeley
Lin W-T, C-h Hsieh, Miki T (2013) Difference in adaptive dispersal ability can promote species coexistence in fluctuating environments. PLoS One 8:e55218
Lurgi M, López BC, Montoya JM (2012) Climate change impacts on body size and food web structure on mountain ecosystems. Philos Trans R Soc B-Biol Sci 367:3050–3057
Marsh DM, Trenham PC (2001) Metapopulation dynamics and amphibian conservation. Conserv Biol 15:40–49
May RM (1973) Stability and complexity in model ecosystems. Princeton University Press, Princeton
McCann KS (2011) Food webs. Princeton University Press, Princeton
McCann K, Hastings AG, Huxel R (1998) Weak trophic interactions and the balance of nature. Nature 395:794–798
McCoy MW, Barfield M, Holt RD (2009) Predator shadows: complex life histories as generators of spatially patterned indirect interactions across ecosystems. Oikos 118:87–100
Melián CJ, Bascompte J, Jordano P, Krivan V (2009) Diversity in a complex ecological network with two interaction types. Oikos 118:122–130
Miller TEX, Rudolf VHW (2011) Thinking inside the box: community-level consequences of stage structured populations. Trend Ecol Evol 26:457–466
Mougi A, Kondoh M (2012) Diversity of interaction types and ecological community stability. Science 337:349–351
Nakano S, Murakami M (2001) Reciprocal subsidies: dynamic interdependence between terrestrial and aquatic food webs. Proc Natl Acad Sci USA 98:166–170
Nakazawa T (2011a) Ontogenetic niche shift, food-web coupling, and alternative stable states. Theor Ecol 4:479–492
Nakazawa T (2011b) Alternative stable states generated by ontogenetic habitat coupling in the presence of multiple resource use. PLoS One 6:e14667
Nakazawa T (2014) A dynamics resilience perspective toward integrated ecosystem management: biodiversity, landscape, and climate. In: Okuda N (ed) Biodiversity in aquatic systems and environments: Lake Biwa. Springer Japan, Tokyo, pp 69–91
Nakazawa T, Doi H (2012) A perspective on match/mismatch of phenology in community contexts. Oikos 121:489–495
Nakazawa T, Yamamura N (2007) Breeding migration and population stability. Popul Ecol 49:101–113
Nakazawa T, Sakai Y, Hsieh CH, Koitabashi T, Tayasu I, Yamamura N, Okuda N (2010) Is the relationship between body size and trophic niche position time-invariant in a predatory fish? First stable isotope evidence. PLoS One 5:e9120
Nakazawa T, Ushio M, Kondoh M (2011) Scale dependence of predator-prey mass ratio: determinants and applications. Adv Ecol Res 45:269–302
Nakazawa T, Yamanaka T, Urano S (2012) Model analysis for plant disease dynamics co-mediated by herbivory and herbivore-borne phytopathogens. Biol Lett 8:685–688
Nakazawa T, Ohba S, Ushio M (2013) Predator-prey body size relationships when predators can consume prey larger than themselves. Biol Lett 9:20121193
Namba T (1980) Density-dependent dispersal and spatial distribution of a population. J Theor Biol 86:351–363
Owen-Smith N, Mills MGL (2008) Predator–prey size relationships in an African large-mammal food web. J Anim Ecol 77:173–183
Parris KM (2006) Urban amphibian assemblages as metacommunities. J Anim Ecol 75:757–764
Post DM, Conners ME, Goldberg DS (2000) Prey preference by a top predator and the stability of linked food chains. Ecology 81:8–14
Rooney N, McCann K, Gellner G, Moore JC (2006) Structural asymmetry and the stability of diverse food webs. Nature 442:265–269
Rudolf VHW, Lafferty KD (2011) Stage Structure alters how complexity affects stability. Ecol Lett 14:75–79
Rudolf VHW, Rasmussen NL (2013a) Population structure determines functional differences among species and ecosystems processes. Nature Commun 4:2318
Rudolf VHW, Rasmussen NL (2013b) Ontogenetic functional diversity: size-structure of a keystone predator alters functioning of a complex ecosystem. Ecology 94:1046–1056
Rudolf VHW, Rasmussen NL, Dibble CJ, Van Allen BG (2014) Resolving the roles of body size and species identity in driving functional differences among consumers. Proc Soc B-Biol Sci 281:20133203
Schindler DE, Scheuerell MD (2002) Habitat coupling in lake ecosystems. Oikos 98:177–189
Schreiber S, Rudolf VHW (2008) Crossing habitat boundaries: coupling dynamics of ecosystems through complex life cycles. Ecol Lett 11:576–587
Schtickzelle N, Quinn TP (2007) A metapopulation perspective for salmon and other anadromous fish. Fish 8:297–314
Vadeboncoeur Y, McCann KS, Vander Zanden MJ, Rasmussen JB (2005) Effects of multi-chain omnivory on the strength of trophic control in lakes. Ecosystems 9:682–693
Vadeboncoeur Y, Peterson G, Vander Zanden MJ, Kalff J (2008) Benthic algal production across lake size gradients: interactions among morphometry, nutrients, and light. Ecology 89:2542–2552
van Leeuwen A, Huss M, Gårdmark A, Casini M, Vitale F, Hjelm J, Persson L, de Roos AM (2013) Predators with multiple ontogenetic niche shifts have limited potential for population growth and top-down control of their prey. Am Nat 182:53–66
Vander Zanden MJ, Vadeboncoeur Y (2002) Fishes as integrators of benthic and pelagic food webs in lakes. Ecology 83:2152–2161
Vander Zanden MJ, Vadeboncoeur Y, Chandra S (2011) Fish reliance on littoral-benthic resources and the distribution of primary production in lakes. Ecosystems 14:894–903
Verhoef HA, Morin PJ (2010) Community ecology: processes, models and applications. Oxford University Press, Oxford
Wäckers FL, van Rijn PCJ, Bruin J (2005) Plant-provided food for carnivorous insects: a protective mutualism and its applications. Cambridge University Press, Cambridge
Wäckers FL, Romeis J, van Rijn P (2007) Nectar and pollen feeding by insect herbivores and implications for multitrophic interactions. Annu Rev Entomol 52:301–323
Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size-structured populations. Annu Rev Ecol Syst 15:393–425
Wilbur HM (1980) Complex life cycles. Annu Rev Ecol Syst 11:67–93
Wollrab S, de Roos AM, Diehl S (2013) Ontogenetic diet shifts promote predator-mediated coexistence. Ecology 94:2886–2897
Woodward G, Warren PH (2007) Body size and predatory interaction in freshwaters: scaling from individuals to communities. In: Hildrew AG, Raffaelli D, Edmonds-Brown R (eds) Body size the structure and function of aquatic ecosystems. Cambridge University Press, Cambridge, pp 97–117
Acknowledgments
I thank members of Center for Ecological Research, Kyoto University and Institute of Oceanography, National Taiwan University for their active collaboration and fruitful discussions, and two anonymous reviewers for their thoughtful comments on the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Takefumi Nakazawa is the recipient of the 7th Population Ecology Young Scientist Award.
Rights and permissions
About this article
Cite this article
Nakazawa, T. Ontogenetic niche shifts matter in community ecology: a review and future perspectives. Popul Ecol 57, 347–354 (2015). https://doi.org/10.1007/s10144-014-0448-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10144-014-0448-z