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Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Intraspecific competition reduces the quantity of excreted nutrients in tadpoles

Noelikanto Ramamonjisoa https://orcid.org/0000-0002-1056-1560 A E , Harisoa Rakotonoely B , TaeOh Kwon C , Kosuke Nakanishi D and Yosihiro Natuhara A
+ Author Affiliations
- Author Affiliations

A Graduate School of Environmental Studies, Nagoya University, Furocho, Chikusa Ward, Nagoya, Aichi 464-8601, Japan.

B Graduate School of Environmental Science, Hokkaido University, Sapporo 060-0808, Japan.

C Field Science Center for Northern Biosphere, Hokkaido University, Kita 8 Nishi 5, Kita Ward, Sapporo, Hokkaido 060-0808, Japan.

D National Institute for Environmental Studies, Onogawa 16-2, Tsukuba, Ibaraki 305-8506, Japan.

E Corresponding author. Email: noelikanto@gmail.com

Marine and Freshwater Research - https://doi.org/10.1071/MF20018
Submitted: 16 January 2020  Accepted: 5 June 2020   Published online: 20 July 2020

Abstract

Anuran larvae can form the largest animal biomass seasonally in freshwater environments, yet, they are still one of the least-studied taxa in terms of nutrient regeneration. The present study tested whether sympatric tadpoles regenerate nutrients at similar rates and ratios, and whether increased intraspecific competition (hereafter ‘competition’) alters patterns of excretion. We quantified rates and ratios of excretion (dissolved nitrogen (N) from ammonia, phosphorus (P) from total dissolved P, and N : P ratio) in three pond-dwelling Japanese tadpoles (Pelophylax nigromaculatus, Rhacophorus schlegelii, Hyla japonica), and tested the effect of competition on excretion in Pelophylax nigromaculatus and Rhacophorus arboreus. The three co-occurring species regenerated nutrients at different rates and ratios; H. japonica excreted nutrients and produced faecal pellets at the lowest rates. Inside field enclosures, increasing tadpole density reduced the quantity but not the quality of excretion by the tadpoles, suggesting higher nutrient sequestration, likely to maintain a stoichiometrically balanced growth under limited resources. Differences in rates and ratios of excretion have previously been shown to have various effects on community structure by affecting primary productivity, highlighting the importance of species identity and interactions on ecosystem function.

Additional keywords: competitor density, functional redundancy, nutrient recycling, paddy fields, pond-dwelling tadpoles.


References

Altig, R., and Johnston, G. F. (1989). Guilds of anuran larvae: relationships among developmental modes, morphologies, and habitats. Herpetological Monograph 3, 81–109.
Guilds of anuran larvae: relationships among developmental modes, morphologies, and habitats.Crossref | GoogleScholarGoogle Scholar |

Altig, R., and McDearman, W. (1975). Percent assimilation and clearance times of five anuran tadpoles. Herpetologica 31, 67–69.

Altig, R., Whiles, M. R., and Taylor, C. L. (2007). What do tadpoles really eat? Assessing the trophic status of an understudied and imperiled group of consumers in freshwater habitats. Freshwater Biology 52, 386–395.
What do tadpoles really eat? Assessing the trophic status of an understudied and imperiled group of consumers in freshwater habitats.Crossref | GoogleScholarGoogle Scholar |

Arribas, R., Díaz-Paniagua, C., Caut, S., and Gomez-Mestre, I. (2015). Stable isotopes reveal trophic partitioning and trophic plasticity of a larval amphibian guild. PLoS One 10, e0130897.
Stable isotopes reveal trophic partitioning and trophic plasticity of a larval amphibian guild.Crossref | GoogleScholarGoogle Scholar | 26091281PubMed |

Atkinson, C. L., Capps, K. A., Rugenski, A. T., and Vanni, M. J. (2017). Consumer‐driven nutrient dynamics in freshwater ecosystems: from individuals to ecosystems. Biological Reviews of the Cambridge Philosophical Society 92, 2003–2023.
Consumer‐driven nutrient dynamics in freshwater ecosystems: from individuals to ecosystems.Crossref | GoogleScholarGoogle Scholar | 28008706PubMed |

Attayde, J. L., and Hansson, L.-A. (1999). Effects of nutrient recycling by zooplankton and fish on phytoplankton communities. Oecologia 121, 47–54.
Effects of nutrient recycling by zooplankton and fish on phytoplankton communities.Crossref | GoogleScholarGoogle Scholar | 28307888PubMed |

Clissold, F. J., Tedder, B. J., Conigrave, A. D., and Simpson, S. J. (2010). The gastrointestinal tract as nutrient-balancing organ. Proceedings of the Royal Society of London B: Biological Sciences 277, 1751–1759.

Costello, D. M., and Michel, M. J. (2013). Predator‐induced defenses in tadpoles confound body stoichiometry predictions of the general stress paradigm. Ecology 94, 2229–2236.
Predator‐induced defenses in tadpoles confound body stoichiometry predictions of the general stress paradigm.Crossref | GoogleScholarGoogle Scholar | 24358709PubMed |

Crawley, M. J. (2013). ‘The R Book,’ 2nd Edn. (John Wiley & Sons: West Sussex, UK.)

Gosner, K. L. (1960). A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16, 183–190.

Greene, R. (2015). The effects of non-native and native anuran tadpoles on aquatic ecosystem processes. M.Sc. Thesis, Arizona State University, Tempe, AZ, USA.

Guariento, R. D., Carneiro, L. S., Jorge, J. S., Borges, A. N., Esteves, F. A., and Caliman, A. (2015). Interactive effects of predation risk and conspecific density on the nutrient stoichiometry of prey. Ecology and Evolution 5, 4747–4756.
Interactive effects of predation risk and conspecific density on the nutrient stoichiometry of prey.Crossref | GoogleScholarGoogle Scholar | 26640656PubMed |

Halekoh, U., and Højsgaard, S. (2014). A Kenward-Roger approximation and parametric bootstrap methods for tests in linear mixed models: the R package pbkrtest. Journal of Statistical Software 59, 1–30.
A Kenward-Roger approximation and parametric bootstrap methods for tests in linear mixed models: the R package pbkrtest.Crossref | GoogleScholarGoogle Scholar |

Halvorson, H. M., and Atkinson, C. L. (2019). Egestion versus excretion: a meta-analysis examining nutrient release rates and ratios across freshwater fauna. Diversity 11, 189.
Egestion versus excretion: a meta-analysis examining nutrient release rates and ratios across freshwater fauna.Crossref | GoogleScholarGoogle Scholar |

Horiuchi, S., and Koshida, Y. (1989). Effects of foodstuffs on intestinal length in larvae of Rhacophorus arboreus (Anura: Rhacophoridae): developmental biology. Zoological Science 6, 321–328.

Janča, M., and Gvoždík, L. (2017). Costly neighbours: heterospecific competitive interactions increase metabolic rates in dominant species. Scientific Reports 7, 5177.
Costly neighbours: heterospecific competitive interactions increase metabolic rates in dominant species.Crossref | GoogleScholarGoogle Scholar | 28701786PubMed |

Jenssen, T. A. (1967). Food habits of the green frog, Rana clamitans, before and during metamorphosis. Copeia 1967, 214–218.
Food habits of the green frog, Rana clamitans, before and during metamorphosis.Crossref | GoogleScholarGoogle Scholar |

Kimura, S. (2019). Influence of different farming methods on the trophic ecology and growth of tadpoles in paddy fields. M.Sc. Thesis, Nagoya University, Nagoya, Japan.

Kuznetsova, A., Brockhoff, P. B., and Christensen, R. H. B. (2017). lmerTest package: tests in linear mixed effects models. Journal of Statistical Software 82, 1–26.
lmerTest package: tests in linear mixed effects models.Crossref | GoogleScholarGoogle Scholar |

Lenth, R. V. (2016). Least-squares means: the R package lsmeans. Journal of Statistical Software 69, 1–33.
Least-squares means: the R package lsmeans.Crossref | GoogleScholarGoogle Scholar |

Liess, A., Guo, J., Lind, M. I., and Rowe, O. (2015). Cool tadpoles from Arctic environments waste fewer nutrients: high gross growth efficiencies lead to low consumer‐mediated nutrient recycling in the north. Journal of Animal Ecology 84, 1744–1756.
Cool tadpoles from Arctic environments waste fewer nutrients: high gross growth efficiencies lead to low consumer‐mediated nutrient recycling in the north.Crossref | GoogleScholarGoogle Scholar | 26239271PubMed |

Matsui, M., and Seki, S. (2008). ‘Handbook of the Larvae of Frogs, Salamanders, and Newts in Japan.’ (Bun-ichi Sougo Shuppan: Tokyo, Japan.) [In Japanese]

McLeay, S. M., Smith, L. L., and Atkinson, C. L. (2019). The stoichiometry of larval anuran development in natural wetlands. Journal of Freshwater Ecology 34, 497–512.

McManamay, R. A., Webster, J. R., Valett, H. M., and Dolloff, C. A. (2011). Does diet influence consumer nutrient cycling? Macroinvertebrate and fish excretion in streams. Journal of the North American Benthological Society 30, 84–102.
Does diet influence consumer nutrient cycling? Macroinvertebrate and fish excretion in streams.Crossref | GoogleScholarGoogle Scholar |

Mitchell, W. A., Abramsky, Z., Kotler, B. P., Pinshow, B., and Brown, J. S. (1990). The effect of competition on foraging activity in desert rodents: theory and experiments. Ecology 71, 844–854.
The effect of competition on foraging activity in desert rodents: theory and experiments.Crossref | GoogleScholarGoogle Scholar |

Natuhara, Y. (2013). Ecosystem services by paddy fields as substitutes of natural wetlands in Japan. Ecological Engineering 56, 97–106.
Ecosystem services by paddy fields as substitutes of natural wetlands in Japan.Crossref | GoogleScholarGoogle Scholar |

Norlin, L., Byström, P., Karlsson, J., Johansson, M., and Liess, A. (2016). Climate change will alter amphibian-mediated nutrient pathways: evidence from Rana temporaria tadpoles in experimental ponds. Freshwater Biology 61, 472–485.
Climate change will alter amphibian-mediated nutrient pathways: evidence from Rana temporaria tadpoles in experimental ponds.Crossref | GoogleScholarGoogle Scholar |

R Core Team (2017). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

Ramamonjisoa, N., and Natuhara, Y. (2017). Hierarchical competitive ability and phenotypic investments in prey: inferior competitors compete and defend. Journal of Zoology 301, 157–164.
Hierarchical competitive ability and phenotypic investments in prey: inferior competitors compete and defend.Crossref | GoogleScholarGoogle Scholar |

Ramamonjisoa, N., and Natuhara, Y. (2018). Contrasting effects of functionally distinct tadpole species on nutrient cycling and litter breakdown in a tropical rainforest stream. Freshwater Biology 63, 202–213.
Contrasting effects of functionally distinct tadpole species on nutrient cycling and litter breakdown in a tropical rainforest stream.Crossref | GoogleScholarGoogle Scholar |

Ramamonjisoa, N., Rakotonoely, H., and Natuhara, Y. (2016). Animal or algal materials: food toughness, food concentration, and competitor density influence food choice in an omnivorous tadpole. Herpetologica 72, 114–119.
Animal or algal materials: food toughness, food concentration, and competitor density influence food choice in an omnivorous tadpole.Crossref | GoogleScholarGoogle Scholar |

Relyea, R. A., and Auld, J. R. (2004). Having the guts to compete: how intestinal plasticity explains costs of inducible defences. Ecology Letters 7, 869–875.
Having the guts to compete: how intestinal plasticity explains costs of inducible defences.Crossref | GoogleScholarGoogle Scholar |

Schmidt, K., Pearson, R. G., Alford, R. A., and Puschendorf, R. (2019). Tadpole species have variable roles in litter breakdown, sediment removal, and nutrient cycling in a tropical stream. Freshwater Science 38, 103–112.
Tadpole species have variable roles in litter breakdown, sediment removal, and nutrient cycling in a tropical stream.Crossref | GoogleScholarGoogle Scholar |

Sterner, R. W., and Elser, J. J. (2002). ‘Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere.’ (Princeton University Press: Princeton, NJ, USA.)

Strauß, A., Reeve, E., Randrianiaina, R., Vences, M., and Glos, J. (2010). The world’s richest tadpole communities show functional redundancy and low functional diversity: ecological data on Madagascar’s stream-dwelling amphibian larvae. BMC Ecology 10, 12.
The world’s richest tadpole communities show functional redundancy and low functional diversity: ecological data on Madagascar’s stream-dwelling amphibian larvae.Crossref | GoogleScholarGoogle Scholar | 20459864PubMed |

Tattersall, G. J., and Wright, P. A. (1996). The effects of ambient pH on nitrogen excretion in early life stages of the American toad (Bufo americanus). Comparative Biochemistry and Physiology. Part A, Physiology 113, 369–374.
The effects of ambient pH on nitrogen excretion in early life stages of the American toad (Bufo americanus).Crossref | GoogleScholarGoogle Scholar | 8689522PubMed |

Vanni, M. J. (2002). Nutrient cycling by animals in freshwater ecosystems. Annual Review of Ecology and Systematics 33, 341–370.
Nutrient cycling by animals in freshwater ecosystems.Crossref | GoogleScholarGoogle Scholar |

Vanni, M. J., and McIntyre, P. B. (2016). Predicting nutrient excretion of aquatic animals with metabolic ecology and ecological stoichiometry: a global synthesis. Ecology 97, 3460–3471.
Predicting nutrient excretion of aquatic animals with metabolic ecology and ecological stoichiometry: a global synthesis.Crossref | GoogleScholarGoogle Scholar | 27912023PubMed |

Vanni, M. J., Flecker, A. S., Hood, J. M., and Headworth, J. L. (2002). Stoichiometry of nutrient recycling by vertebrates in a tropical stream: linking species identity and ecosystem processes. Ecology Letters 5, 285–293.
Stoichiometry of nutrient recycling by vertebrates in a tropical stream: linking species identity and ecosystem processes.Crossref | GoogleScholarGoogle Scholar |

Whiles, M. R., and Altig, R. (2010). Dietary assessments of larval amphibians. In ‘Amphibian Ecology and Conservation: A Handbook of Techniques’. (Ed. C. K. Dodd.) pp. 71–86. (Oxford University Press: New York, USA.)