Abstract
Phenology has an important effect on the life strategies of species that live in temporary waters. Predaceous aquatic insects are key components of communities associated with seasonal ponds. Since the life cycles of these predators and their prey are unusual in that they occur at different moments of the pond hydroperiod, differences in temporal overlap could change the strength of their interactions. This study analyzed the phenology of the giant water bug Belostoma bifoveolatum and its prey. Breeding phenology, nymph population, and prey phenology were studied extensively in three wetlands during the spring season. Experimental trials were carried out to evaluate prey consumption and prey preference. The results showed a strong overlap in phenology between the water bug and the Pleurodema thaul frog. The timing of tadpole and water bug nymph hatching could ensure high survival levels of the early immature stages of this insect. As giant water bugs develop, their prey selectivity experiences a shift—older nymphs and adults having a higher impact on tadpoles. The fluctuating climate of the Patagonian region probably influences the phenology of predator–prey assemblages in seasonal communities, and may have the potential to drive feeding performance and the strength of interspecific interactions.
Similar content being viewed by others
References
Aditya, G., S. Bhattacharyya, N. Kundu, G. K. Saha & S. K. Raut, 2004. Predatory efficiency of the water bug Sphaerodema annulatum on mosquito larvae (Culex quinquefasciatus) and its effect on adult emergence. Bioresearch Technology 95: 169–172.
Aditya, G., S. Bhattacharyya, N. Kundu & G. K. Saha, 2005. Frequency dependent prey selection of predacious water bugs on Armigeres subalbatus immature. Journal of Vector Borne Disease. 42: 9–14.
Alford, R. A., 1989. Variation in predator phenology affects predator performance and prey community composition. Ecology 70: 206–219.
Armúa De Reyes, C. & A. L. Estévez, 2005. Diversidad de Heterópteros acuáticos, conespecial referencia a las Belostoma (Heteróptera: Belostomatidae). INSUGEO Miscelánea 14: 281–292.
Benard, M. F., 2015. Warmer winters reduce frog fecundity and shift breeding phenology, which consequently alters larval development and metamorphic timing. Global Change Biology 21: 1058–1065.
Blaustein, A. R., S. C. Walls, B. A. Bancroft, J. J. Lawler, C. L. Searle & S. S. Gervast, 2010. Direct and indirect effects of climate change on amphibian populations. Diversity 2(2): 281–313.
Calhoun, A. J. K., D. M. Mushet, K. P. Bell, D. Boix, J. A. Fitsimons & F. Isselin-Nondedeu, 2017. Temporary wetlands: challenges and solutions to conserving a “disappearing” ecosystem. Biological Conservation 211: 3–11.
Cayrou, J. & R. Cereghino, 2005. Life-cycle phenology of some aquatic insects: implications for pond conservation. Aquatic Conservation: Marine and Freshwater Ecosystems 15: 559–571.
Chesson, J., 1978. Measuring preference in selective predation. Ecology 59: 211–215.
Cloarec, A., 1990. Variations of predatory tactics of a water bug during development. Ethology 86: 33–46.
Faúndez, E. I. & M. A. Carvajal, 2017. Notas sobre Belostomatidae (Hemiptera: Heteroptera) en Chile. Revista Chilena de Entomología 43: 75–80.
Foltz, S. J. & S. I. Dodson, 2009. Aquatic Hemiptera community structure in storm water retention ponds: a watershed land cover approach. Hydrobiologia 1: 49–62.
Formanowicz, D. R., 1984. Foraging tactics of an aquatic insect: partial consumption of prey. Animal Behavior 32: 774–781.
Formanowicz Jr., D. R., 1986. Anuran tadpole/aquatic insect predator-prey interactions: tadpole size and predator capture success. Herpetologica 42: 367–373.
Gosner, K. L., 1960. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16: 183–190.
Hampton, S. E., 2004. Habitat overlap of enemies: temporal patterns and the role of spatial complexity. Oecologia 138: 475–484.
Heckman, C. W., 2011. Encyclopedia of South American aquatic insects: Hemiptera-Heteroptera. Springer, London: 679.
Hirai, T. & K. Hidaka, 2002. Anuran-dependent predation by the giant water bug, Lethocerus deyrollei (Hemiptera: Belostomatidae), in rice fields of Japan. Ecological Research 17: 655–661.
Jara, F. G., 2008. Tadpole-odonate larvae interactions: influence of body size and diel rhythm. Aquatic Ecology 42: 503–509.
Jara, F. G., 2014. Trophic ontogenetic shifts of the dragonfly Rhionaeschna variegata: the role of larvae as predators and prey in Andean wetland communities. Annales de Limnologie - International Journal of Limnology 50: 173–184.
Jara, F. G., 2016. Predator-prey body size relationship in temporary wetlands: effect of predatory insects on prey size spectra and survival. Annales de Limnologie - International Journal of Limnology 52: 205–216.
Jara, F. G. & M. G. Perotti, 2010. Risk of predation and behavioral response in three anuran species: influence of tadpole size and predator type. Hydrobiologia 644: 313–324. https://doi.org/10.1007/s10750-010-0196-9
Jara, F. G. & M. G. Perotti, 2018. The life cycle of the giant water bug of northwestern Patagonian wetlands: the effect of hydroperiod and temperature regime. Invertebrate Biology 137: 105–115.
Jara, F. G., C. A. Úbeda & M. G. Perotti, 2013. Predatory insects in lentic freshwater habitats from northwest Patagonia: richness and phenology. Journal of Natural History 47: 2749–2768.
Kehr, A. I. & J. A. Schnack, 1991. Predator-prey relationship between giant water bugs (Belostoma oxyurum) and larval anurans (Bufo arenarum). Alytes 9: 61–69.
Kingsolver, J. G., H. A. Woods, L. B. Buckley, K. A. Potter, H. J. MacLean & J. K. Higgins, 2011. Complex life cycles and the responses of insects to climate change. Integrative and Comparative Biology 51: 719–732.
Lawler, S. P. & P. J. Morin, 1993. Temporal overlap, competition, and priority effects in larval anurans. Ecology 74: 174–182.
Lopatina, E. B., D. A. Kutcherov & S. V. Balashov, 2014. The influence of diet on the duration and thermal sensitivity of development in the linden bug Pyrrhocoris apterus L. (Heteroptera: Pyrrhocoridae). Physiological Entomology 39: 208–216.
Manly, B. F. J., 1974. A model for certain types of selection experiments. Biometrics 30: 281–294.
McCauley, S. J., J. I. Hammond, D. N. Frances & K. E. Mabry, 2015. Effects of experimental warming on survival, phenology and morphology of an aquatic insect (Odonata). Ecological Entomology 40: 211–220.
Melo, M. C., 2009. Biodiversity of aquatic and semiaquatic Heteroptera (Hemiptera) from Argentinean Patagonia. Revista de la Sociedad Entomologica Argentina 68: 177–185.
Moncada, C., 2011. Patrones reproductivos y de desarrollo larval de un ensamble de anuros enuna laguna de un mallín de bosque nordpatagónico. Licenciatura Thesis. San Carlos de Bariloche. Universidad Nacional del Comahue.
Nakazawa, T., S.-Y. Ohba & M. Ushio, 2013. Predator-prey body size relationships when predators can consume prey larger than themselves. Biology Letters. https://doi.org/10.1098/rsbl.2012.1193.
National Research Council, 1995. Wetlands: Characteristics and Boundaries. The National Academies Press, Washington, DC. https://doi.org/10.17226/4766.
Oertli, B., D. Auderset-Joye, E. Castella, R. Juge, A. Lehmann & J. B. Lachavanne, 2005. PLOCH: a standardized method for sampling and assessing the biodiversity in ponds. Aquatic Conservation: Marine and Freshwater Research 15: 665–679.
Ohba, S.-Y. & T. Haruki, 2015. Young giant water bug nymphs prefer larger prey: changes in foraging behaviour with nymphal growth in Kirkaldyia deyrolli. Biological Journal of Linnean Society 117: 601–606.
Ohba, S.-Y. & F. Nakasuji, 2006. Dietary items of predacious aquatic bugs Nepoidea: Heteroptera in Japanese wetlands. Limnology 7: 41–43.
Ohba, S-Y. & H. Tatsuta, 2016. Young giant water bug nymphs prefer larger prey: changes in foraging behaviour with nymphal growth in Kirkaldyia deyrolli. Biological Journal of the Linnean Society. https://doi.org/10.1111/bij.12693
Ohba, S., H. Miyasaka & F. Nakasuji, 2008a. The role of amphibian prey in the diet and growth of giant water bug nymphs in Japanese rice fields. Population Ecology 50: 9–16.
Ohba, S., H. Tatsuta & F. Nakasuji, 2008b. Variation in the geometry of foreleg claws in sympatric giant water bug species: an adaptive trait for catching prey? Entomologia Experimentalis et Applicata 129: 223–227.
Okada, H. & F. Nakasuji, 1993a. Pattern of local distribution and coexistence of two giant water bugs, Diplonychus japonicus and D. major Hemiptera: Belostomatidae in Okayama, western Japan. Japanese Journal of Entomology 61: 79–84.
Okada, H. & F. Nakasuji, 1993b. Comparative studies on the seasonal occurrence, nymphal development and food menu in two giant water bugs, Diplonychus japonicas (Vuillefroy) and Diplonychus major (Esaki) Hemiptera: Belostomatidae. Research in Population Ecology 35: 15–22.
Pereira, M. H. & A. L. Melo, 1998. Influencia do tipo de presa no desenvolvimento e na preferencia alimentar de Belostoma anurum Herrich-Schnaffer 1948 e Belostoma plebejum (Stal, 1858) (Heteroptera: Belostomatidae). Ecología de Insectos Acuáticos. Series Oecologia Brasiliensis 5: 41–49.
Perotti, M. G., M. C. Dieguez & F. G. Jara, 2005. Estado del conocimiento de humedales del norte patagónico (Argentina): aspectos relevantes e importancia para la conservación de la biodiversidad regional. Revista Chilena de Historia Natural 78: 723–737.
Persson Vinnersten, T., 2007. Aquatic insects in temporary freshwater wetlands - Predator-prey relationships and how to study them. Introductory Research Essay, Upsala 36 pp. ISSN 140468xx
Raut, S. K., T. C. Saha & B. Mukhopadhyay, 1988. Predacious waterbugs in the control of vector snails. Bicovas 1: 175–185.
Runck, C. & D. W. Blinn, 1994. Role of Belostoma bakeri (Heteroptera) in the trophic ecology of a fishless desert spring. Limnology and Oceanography 39: 1800–1812.
Saha, N., G. Aditya, G. K. Saha & S. E. Hampton, 2010. Opportunistic foraging by heteropteran mosquito predators. Aquatic Ecology 44: 167–176.
Schmidt, B. R. & A. Amezquita, 2001. Predator-induced behavioral responses: tadpoles of neotropical frog Phyllomedusa tarsius do not respond to all predators. Herpetological Journal 11: 9–15.
Schnack, J. A., 1971. Las ninfas del genero Belostoma, (Latreille) Hemiptera: Belostomatidae: Belostoma oxyurum (Dufour) y Belostoma bifoveolatum (Spinola). Revista de la Sociedad Entomológica Argentina 33: 77–85.
Schneider, D. W. & T. M. Frost, 1996. Habitat duration and community structure in temporary ponds. Journal of American Benthological Society 15: 64–86.
Semlitsch, R. D., W. E. Peterman, T. L. Anderson, D. L. Drake & B. H. Ousterhout, 2015. Intermediate pond sizes contain the highest density, richness, and diversity of pond-breeding amphibians. PLoS ONE 10(4): e0123055.
Silveira-Manzotti, B. N., A. R. Manzotti, M. Ceneviva-Bastos & L. Casatti, 2016. Trophic structure of macroinvertebrates in tropical pasture streams. Acta Limnologica Brasiliencia 28: 1–10.
Smith, R. L., 1974. Life history of Abedus herberti in Central Arizona (Hemiptera: Belostomatidae). Psyche 81: 272–283.
Smith, R. L., 1997. Evolution of paternal care in giant water bugs (Hemiptera: Belostomatidae). In Choe, J. C. & B. J. Crespi (eds), The Evolution of Social Behavior in Insects and Arachnids. Cambridge University Press, Cambridge: 116–149.
Sokal, R. R. & F. J. Rohlf, 1995. Biometry. Freeman, New York: 887.
Swart, C. C. & R. C. Taylor, 2004. Behavioral interactions between the giant water bug Belostoma lutarium and tadpoles of Bufo woodhousii. Southwestern Naturalist 3: 13–24.
Tobler, M., K. Roach, K. O. Winemiller, R. L. Morehouse & M. Plath, 2013. Population structure, habitat use, and diet of giant water bugs in a sulfidic cave. Southwestern Naturalist 58: 420–426.
Todd, B. D., D. E. Scott, J. H. K. Pechmann & J. W. Gibbons, 2011. Climate change correlates with rapid delays and advancements in reproductive timing in an amphibian community. Proceedings of the Royal Society of London: Series B 278: 2191–2197.
Toledo, L. F., 2005. Predation of juvenile and adult anurans by invertebrates: current knowledge and perspectives. Herpetological Review 36: 395–400.
Toledo, L. F., R. R. Silva & C. F. B. Haddad, 2007. Anurans as prey: an exploratory analysis and size relationships between predators and their prey. Journal of Zoology 271: 170–177.
Urban, M. C., 2007. Predator size and phenology shape prey survival in temporary ponds. Oecologia 154: 571–580.
Wiggins, G. B., R. J. Mackay & I. M. Smith, 1980. Evolutionary and ecological strategies of animals in annual temporary pools. Archive of Hydrobiology 58: 97–206.
Yang, L. H. & V. H. W. Rudolf, 2010. Phenology, ontogeny and the effects of climate change on the timing of species interactions. Ecology Letters 13: 1–10.
Acknowledgements
This investigation was performed under the institutional animal care guidelines established by the Administración de Parques Nacionales of Argentina (APN). Animals were collected under Permit no. 52-AP-16 (Subsecretaria de Medio Ambiente y Manejo de Áreas Protegidas de San Carlos de Bariloche) and Permit no. 1532 (Secretaria de Ambiente y Desarrollo Sustentable de la Provincia de Rio Negro). A. Shaw reviewed the English text and M.E. Cuello helped with sampling frog eggs. I thank the two reviewers who made valuable comments on earlier drafts of the manuscript. This work was funded partially by research grant PICT 2011 (Agencia, FONCyT) to F. Jara and by the UNComa B166 project.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling editor: Lee B. Kats
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.
10750_2019_3928_MOESM1_ESM.docx
Supplementary material 1 (DOCX 1127 kb). Online Resource 1. Belostoma bifoveolatum, male carrying eggs (A) and studied wetlands, Las Cartas (B), Llao Llao (C) and Camping Musical (E)
10750_2019_3928_MOESM2_ESM.docx
Supplementary material 2 (DOCX 241 kb). Online Resource 2. Belostoma bifoveolatum life stages (A) and average total length (± SE) of each stage used in the experiments (B). Different numbers at the top of the bar indicate significant differences (Dunn’s test pairwise comparison, P < 0.01)
Rights and permissions
About this article
Cite this article
Jara, F.G. The impact of phenology on the interaction between a predaceous aquatic insect and larval amphibians in seasonal ponds. Hydrobiologia 835, 49–61 (2019). https://doi.org/10.1007/s10750-019-3928-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-019-3928-5