Biology:Ontogenetic niche shift

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Short description: Ecological phenomenon
The metamorphosis exhibited in frogs is one of the many examples of the ontogenetic niche shifting.

Ontogenetic niche shift (abbreviated ONS)[1] is an ecological phenomenon where an organism (usually an animal) changes its diet or habitat during its ontogeny (development).[2] During the ontogenetic niche shifting an ecological niche of an individual changes its breadth and position.[3] The best known representatives of taxa that exhibit some kind of the ontogenetic niche shift are fish (e.g. migration of so-called diadromous fish between saltwater and freshwater for purpose of breeding[2]), insects (e.g. metamorphosis between different life stages; such as larva, pupa and imago[2]) and amphibians (e.g. metamorphosis from tadpole to adult frog[2]).[4] A niche shift is thought to be determined genetically, while also being irreversible.[5] Important aspect of the ONS is the fact, that individuals of different stages of a population (e.g. of various age or size) utilize different kind of resources and habitats.[6][7] The term was introduced in a 1984 paper by biologists Earl E. Werner and James F. Gilliam.[1][8]

Characteristics

The ontogenetic niche shift is thought to be determined genetically, while also being irreversible.[5] In complex natural systems the ONS happens multiple times in lifetime of an individual (in some examples the ontogenetic niche shifting can occur continuously).[4] The ontogenetic niche shift varies across species; in some it is hardly visible and gradual (for example a change in diet or in size in mammals and reptiles), while in others it is obvious and abrupt (the metamorphosis of insects, which often results in changing habitat, diet and other ecological conditions).[5][9] One of the studies suggests that differences in the ONS across species could be (at least to some degree) explained by diversity of traits and functional roles of a species. As a consequence differences in ontogenetic niche shifting are thought to follow some general patterns.[10]

Importance

For communities

The ONS, which divides a population of the same species into distinct life-history stages, can affect food web of a community.

It is thought that almost every organism shows some kind of ontogenetic niche shift. The ONS, which is responsible for causing a noticeable phenotypic variation among individuals of the same species, plays important role in structuring communities and influencing their inside dynamics.[4] In some cases individuals undergoing the ONS, in which they change their habitat, become a (mobile) link between two different communities (for example via flow of energy, matter and nutrients).[11] A stage structure of a population can result in various stages interacting with different representatives of a community or even with individuals of other communities,[2][12] thus having a distinct ecological role from other life-history stages of the same population.[13] Theoretical models, where communities are stage-structured, propose the ontogenetic niche shifting of studied organisms is influencing the whole community (especially its resilience and disturbance responses).[4]

For population

The most apparent consequence of the ontogenetic niche shifting is a reduction of competition between different stages of the same population. Because of the ONS individuals of different age or size do not compete for food, materials and other habitat resources.[6] Different stages of the same population also have different trophic effects on food web of a community.[7] A division of a population on distinct life-history stages is useful and evident, when there is a lack of resources for one stage (for example when juveniles do not get enough resources for themselves). In that case a lacking stage will have higher mortality rate.[6]

The ONS is of great importance for survival of populations. Researchers noticed that many species exhibit the ontogenetic niche shifting at different times and in a lot of examples the ONS occurred as a response to various abiotic and biotic environmental factors. It is thought that the ontogenetic niche shift could be an adaptive response to changing conditions in individual's habitat. Authors of the life history theory predicted that organisms can affect the time of their ontogenetic niche shifting. While individuals living in favorable conditions would usually delay their ONS to successive ecological niche, organisms living in a niche with poor conditions typically advance to a further niche.[2]

Understanding the ontogenetic niche shifting in different species and its impact on the whole community is important when studying a biodiversity and ecosystem functioning.[4] It is thought to be useful when dealing with populations threatened by anthropogenic disturbances[4][13] and environmental changes.[10][13]

Representative taxa

The extreme ONS can be seen among insects. On the picture above are shown a pupa and an imago of Rhopalomyia solidaginis.
Pacific salmon (Oncorhynchus) is an anadromous fish species that exhibits a drastic habitat niche shift.
Skull of a juvenile Tyrannosaurus. Juveniles of megatheropods proposedly occupied mesocarnivoran ecological niche.

Even though the occurrence of ontogenetic niche shifting is thought to be widely distributed, the best known representative taxa with extensively studied ONS are insects and a few groups of vertebrates, especially fish and amphibians, where individuals often change their habitat as well as a lot of other aspects of their niche during the development. The less pronounced ontogenetic niche shifting can be seen in many other taxa, where their habitat stays the same. Usually the ONS in those species is evident, when looking at resources being used by organisms of the same species but various ages or size classes (for example a change in their diet).[2]

Invertebrates

The ontogenetic niche shifting, which is connected with extreme habitat changes, can be seen among insects.[2] Individuals of taxon Insecta are known to exhibit one of the various types of metamorphosis, the best studied being hemimetabolism (where an insect passes three life stages; egg, nymph and imago) and holometabolism (characterized with four life stages of an insect; egg, larva, pupa and imago).[14] Nutritional niches and their shifting during a ontogeny can be accurately measured by using a stable isotopic signature of animals.[15][16] Such method has been used in studying the ONS in gastropods, such as field slugs.[15]

Vertebrates

The ONS similar to that among insects happens in amphibian taxa,[2] the best known being frogs, which start as an egg and then hatch into a larval stage called the tadpole.[17] Tadpoles exhibit many differences that distinguish them from an adult stage of a frog; most species' tadpoles are aquatic, they usually possess external gills and primarily feed with plant material (even though there are some exceptions that consume dead animal flesh or mixed diet).[18] Another well studied example of the ONS occurs in fish, that exhibit diadromous behaviour. Diadromous fish species drastically change their habitat, when they set out on a journey from sea (saltwater) to rivers (freshwater) and vice versa.[2] A lot of freshwater fish species show the ONS in their diet, when they switch from preying on plankton to performing benthivory.[5]

The ONS may not be so visible in reptiles, even though these vertebrates do utilize it. The ontogenetic niche shifting was studied in American alligator (Alligator mississippiensis), which is ideal for studying ecological aspects of ONS because of many distinct size stages in a population. Alligators were switching their habitat niche between hydrologically isolated, seasonal wetlands and riverine systems. The study has shown that riverine systems were populated primarily with adults and subadults of both sexes, that used the area as a non-nesting habitat. On the other hand, juveniles and adult females were found on seasonal wetlands, which served as a nursery and nesting sites respectively.[11]

Good example of the ONS in birds are big seabirds, such as albatrosses, which spend some of their time as fully oceanic birds and when sexually mature begin to visit breeding grounds. Immature juveniles usually stay in subtropical water, where they occupy high trophic levels. Researchers noticed that young birds progressively direct towards lower trophic positions when they are coming closer to sexual maturity. After time they take on an isotopic niche of an adult bird.[19]

The ontogenetic niche shifting is a concept widely studied in paleontology and paleozoology. Large non-avian dinosaurs are known to have had exhibited one of the most intensive ontogenetic niche shifting, as they were hatched from an egg and had to experience big size shifts during their ontogeny.[20] One of the problems, connected with understanding Mesozoic dinosaur fauna was lack of so-called mesocarnivores. It is predicted the ontogenetic niche shift is an answer, because carnivorous dinosaurs started out as small hatchlings and progressed towards adult size, while occupying different successive niches and limiting trophic species diversity. Juvenile individuals of megatheropods are thought to occupy mesocarnivore niche.[21]

Plants

The ontogenetic niche shifting is primarily studied in animals, but there are some studies that deal with the ONS in plants.[3][22][23] One of the ONSs studied in plants is changing of a regeneration niche. Authors of the paper noticed that during the ontogeny the regeneration niche of Acer opalus, the Italian maple, had shrinked. It is thought such ontogenetic niche shift was mainly a consequence of herbivory, the depth of the litter layer and presence of other plants (especially adult trees and shrubs).[23]

See also

References

  1. ↑ 1.0 1.1 Fokkema, Wimke; van der Jeugd, Henk P.; Lameris, Thomas K.; Dokter, Adriaan M.; Ebbinge, Barwolt S.; de Roos, André M.; Nolet, Bart A.; Piersma, Theunis et al. (2020-06-01). "Ontogenetic niche shifts as a driver of seasonal migration" (in en). Oecologia 193 (2): 285–297. doi:10.1007/s00442-020-04682-0. ISSN 1432-1939. PMID 32529317. PMC 7320946. Bibcode: 2020Oecol.193..285F. https://doi.org/10.1007/s00442-020-04682-0. 
  2. ↑ 2.0 2.1 2.2 2.3 2.4 2.5 2.6 2.7 2.8 2.9 Takimoto, Gaku (2003). "Adaptive Plasticity in Ontogenetic Niche Shifts Stabilizes Consumer‐Resource Dynamics". The American Naturalist 162 (1): 93–109. doi:10.1086/375540. ISSN 0003-0147. PMID 12856239. http://dx.doi.org/10.1086/375540. 
  3. ↑ 3.0 3.1 Eriksson, Ove (2011-02-02). "Ontogenetic niche shifts and their implications for recruitment in three clonal Vaccinium shrubs: Vaccinium myrtillus, Vaccinium vitis-idaea, and Vaccinium oxycoccos" (in en). Canadian Journal of Botany 80 (6): 635–641. doi:10.1139/b02-044. https://cdnsciencepub.com/doi/abs/10.1139/b02-044. 
  4. ↑ 4.0 4.1 4.2 4.3 4.4 4.5 Nakazawa, Takefumi (2015). "Ontogenetic niche shifts matter in community ecology: a review and future perspectives" (in en). Population Ecology 57 (2): 347–354. doi:10.1007/s10144-014-0448-z. ISSN 1438-390X. https://esj-journals.onlinelibrary.wiley.com/doi/abs/10.1007/s10144-014-0448-z. 
  5. ↑ 5.0 5.1 5.2 5.3 Claessen, D.; Dieckmann, U. (2001). "Ontogenetic Niche Shifts and Evolutionary Branching in Size-Structured Populations" (in en). http://pure.iiasa.ac.at/id/eprint/6468/. 
  6. ↑ 6.0 6.1 6.2 Lindmark, Elin (2021). Habitat availability and ontogenetic niche shifts : The effects on adult size of lake-living brown trout (Salmo trutta). http://urn.kb.se/resolve?urn=urn:nbn:se:umu:diva-178788. 
  7. ↑ 7.0 7.1 Nakazawa, Takefumi (2011-02-08). "Alternative Stable States Generated by Ontogenetic Niche Shift in the Presence of Multiple Resource Use" (in en). PLOS ONE 6 (2): e14667. doi:10.1371/journal.pone.0014667. ISSN 1932-6203. PMID 21346805. Bibcode: 2011PLoSO...614667N. 
  8. ↑ Werner, E E; Gilliam, J F (1984-11-01). "The Ontogenetic Niche and Species Interactions in Size-Structured Populations". Annual Review of Ecology and Systematics 15 (1): 393–425. doi:10.1146/annurev.es.15.110184.002141. ISSN 0066-4162. https://www.annualreviews.org/doi/10.1146/annurev.es.15.110184.002141. 
  9. ↑ Bassar, Ronald D.; Travis, Joseph; Coulson, Tim (2017-03-22). "Predicting Coexistence in Species with Continuous Ontogenetic Niche Shifts and Competitive Asymmetry" (in en). bioRxiv 98 (11): 2823–2836. doi:10.1101/119446. PMID 28766700. https://www.biorxiv.org/content/10.1101/119446v1. 
  10. ↑ 10.0 10.1 Rudolf, Volker H. W. (2020). "A multivariate approach reveals diversity of ontogenetic niche shifts across taxonomic and functional groups" (in en). Freshwater Biology 65 (4): 745–756. doi:10.1111/fwb.13463. ISSN 1365-2427. 
  11. ↑ 11.0 11.1 Subalusky, Amanda L.; Fitzgerald, Lee A.; Smith, Lora L. (2009-07-01). "Ontogenetic niche shifts in the American Alligator establish functional connectivity between aquatic systems" (in en). Biological Conservation 142 (7): 1507–1514. doi:10.1016/j.biocon.2009.02.019. ISSN 0006-3207. https://www.sciencedirect.com/science/article/abs/pii/S0006320709000950. 
  12. ↑ "Events: Ecological and evolutionary consequences of ontogenetic niche and habitat shifts | Santa Fe Institute" (in en). https://www.santafe.edu//events/ecological-and-evolutionary-consequences-ontogenet. 
  13. ↑ 13.0 13.1 13.2 "NSF Award Search: Award # 1256860 - Linking ontogenetic niche shifts and functional diversity: Consequences for community dynamics and biodiversity loss" (in en). https://www.nsf.gov/awardsearch/showAward?AWD_ID=1256860&HistoricalAwards=false. 
  14. ↑ "Comparative transcriptomics of hemimetabolan and holometabolan metamorphosis" (in en). https://www.researchgate.net/publication/322698687. 
  15. ↑ 15.0 15.1 Bonkowski, Michael; Kappes, Heike (2018-02-01). "Niche partitioning and indication of ontogenetic niche shifts in forest slugs according to stable isotopes". Journal of Molluscan Studies 84 (1): 111–112. doi:10.1093/mollus/eyx042. ISSN 0260-1230. 
  16. ↑ Hammerschlag-Peyer, Caroline M.; Yeager, Lauren A.; Araújo, Márcio S.; Layman, Craig A. (2011-11-03). "A Hypothesis-Testing Framework for Studies Investigating Ontogenetic Niche Shifts Using Stable Isotope Ratios". PLOS ONE 6 (11): e27104. doi:10.1371/journal.pone.0027104. ISSN 1932-6203. PMID 22073265. Bibcode: 2011PLoSO...627104H. 
  17. ↑ "Tadpole to frog: development stages & metamorphosis - Saga". https://www.saga.co.uk/magazine/home-garden/gardening/wildlife/amphibians/the-tadpole. 
  18. ↑ Mylniczenko, Natalie (2009-01-01). "AMPHIBIANS" (in en). Manual of Exotic Pet Practice: 73–111. doi:10.1016/B978-141600119-5.50008-1. ISBN 9781416001195. https://www.sciencedirect.com/science/article/pii/B9781416001195500081. 
  19. ↑ Carravieri, Alice; Weimerskirch, Henri; Bustamante, Paco; Cherel, Yves (2017). "Progressive ontogenetic niche shift over the prolonged immaturity period of wandering albatrosses". Royal Society Open Science 4 (10): 171039. doi:10.1098/rsos.171039. PMID 29134098. Bibcode: 2017RSOS....471039C. 
  20. ↑ Codron, Daryl; Carbone, C.; Müller, D. W. H.; Clauss, Marcus (2012). "Ontogenetic niche shifts in dinosaurs influenced size, diversity and extinction in terrestrial vertebrates". Biology Letters 8 (4): 620–623. doi:10.1098/rsbl.2012.0240. ISSN 1744-9561. PMID 22513279. PMC 3391484. https://www.zora.uzh.ch/id/eprint/63559/. 
  21. ↑ Schroeder, Katlin; Lyons, S. Kathleen; Smith, Felisa A. (2021-02-26). "The influence of juvenile dinosaurs on community structure and diversity" (in en). Science 371 (6532): 941–944. doi:10.1126/science.abd9220. ISSN 0036-8075. PMID 33632845. Bibcode: 2021Sci...371..941S. https://www.science.org/doi/10.1126/science.abd9220. 
  22. ↑ Cameron, Fiona (2014-08-19). Ontogenetic Niche Shifts Within Floodplain Meadow Species (mphil thesis). The Open University.
  23. ↑ 23.0 23.1 Quero, José L; Gómez-Aparicio, Lorena; Zamora, Regino; Maestre, Fernando T. (2008). "Shifts in the regeneration niche of an endangered tree (Acer opalus ssp. granatense) during ontogeny: Using an ecological concept for application". Basic and Applied Ecology 9 (6): 635–644. doi:10.1016/j.baae.2007.06.012. ISSN 1439-1791. http://dx.doi.org/10.1016/j.baae.2007.06.012. 



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