Hostname: page-component-669899f699-8p65j Total loading time: 0 Render date: 2025-05-06T06:44:17.543Z Has data issue: false hasContentIssue false
  • English
  • Français

Do sexual gonadic maturity and age determine habitat occupancy of Canthon cyanellus LeConte, 1859 (Coleoptera: Scarabaeidae)?

Published online by Cambridge University Press:  14 April 2021

Renato Portela Salomão Open the ORCID record for Renato Portela Salomão [Opens in a new window] ,
Lucrecia Arellano ,
Carmen Huerta  and
Jorge Leonel León-Cortés
Renato Portela Salomão
Affiliation:
Instituto Nacional de Pesquisas da Amazônia, Av. André Araújo 2936, Manaus, Amazonas, 69060-001, Brazil
Lucrecia Arellano
Affiliation:
Red de Ecoetología, Instituto de Ecología, A. C., Carretera Antigua a Coatepec 351, El Haya, Xalapa, Veracruz, 91070, Mexico
Carmen Huerta*
Affiliation:
Red de Ecoetología, Instituto de Ecología, A. C., Carretera Antigua a Coatepec 351, El Haya, Xalapa, Veracruz, 91070, Mexico
Jorge Leonel León-Cortés
Affiliation:
Departamento de Conservación de la Biodiversidad, El Colegio de la Frontera Sur, Carretera Panamericana and Av. Periférico Sur S/N, San Cristóbal de Las Casas, Chiapas, 29290, Mexico.
*
*Corresponding author. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

High-quality habitats presumably have the resources required to sustain relatively high rates of survival and reproduction. We assessed how habitat type and local environmental conditions determine the distribution of individuals of Canthon cyanellus (Coleoptera: Scarabaeidae), an eurytopic dung beetle, according to age category and sexual gonadic maturity. Beetles were surveyed in forest fragments, live fences, and pastures in Mexico. Individuals were categorised into six age categories according to the glandular volumes in males and oocyte number and length in females. Mature females in forest fragments were the most abundant females found among the habitats. Air humidity and soil hardness were positively and negatively related to mature female abundance, respectively. Mature beetles were the most abundant among males, and higher abundance of males occurred in forest fragments than in live fences and pastures. Light quantity was negatively related to the abundance of young males. Compared to forest fragments, females in pastures had larger oocytes. However, sites with higher soil hardness and air humidity had females with lower numbers of oocytes. Our results demonstrate that, although C. cyanellus occurs across a wide range of habitats, forest habitats might host sexually mature individuals, which translates into more effective individual dispersion and potential reproduction.

Type
Research Papers
Information
The Canadian Entomologist , Volume 153 , Issue 4 , August 2021 , pp. 412 - 427
Check for updates
Copyright
© The Author(s), 2021. Published by Cambridge University Press on behalf of the Entomological Society of Canada

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

Footnotes

Subject editor: Andrew Smith

References

Anderson, M.J. 2006. Distance based tests for homogeneity of multivariate dispersions. Biometrics, 62: 245–253.CrossRefGoogle ScholarPubMed
Arellano, L. and Halffter, G. 2002. Gamma diversity derived from and a determinant of alpha diversity and beta diversity: an analysis of three tropical landscapes. Acta Zoológica Mexicana, 90: 27–76.Google Scholar
Arellano, L., León-Cortés, J.L., and Halffter, G. 2008a. Response of dung beetle assemblages to landscape structure in remnant natural and modified habitats in southern Mexico. Insect Conservation and Diversity, 1: 253–262.CrossRefGoogle Scholar
Arellano, L., León-Cortés, J.L., and Ovaskainen, O. 2008b. Patterns of abundance and movement in relation to landscape structure: a study of a common scarab (Canthon cyanellus cyanellus) in Southern Mexico. Landscape Ecology, 23: 69–78.CrossRefGoogle Scholar
Arellano, L. and León-Cortés, J.L. 2011. Patrones de diversidad y movilidad de escarabajos del estiércol. Editorial Académica Española, Madrid, Spain.Google Scholar
Barretto, J.W., Cultid-Medina, C.A., and Escobar, F. 2018. Annual abundance and population structure of two dung beetle species in a human-modified landscape. Insects, 10: 1–14.CrossRefGoogle Scholar
Bates, D., Maechler, M., Bolker, B., Walker, S., Christensen, R.H.B., Singmann, H., et al. 2019. Package ‘lme4’. Available from https://cran.r-project.org/web/packages/lme4/lme4.pdf [accessed 20 October 2019].Google Scholar
Bell, W.J. 1990. Searching behavior patterns in insects. Annual Review of Entomology, 35: 447–467.CrossRefGoogle Scholar
Bellon, M.R. and Brush, S.B. 1994. Keepers of maize in Chiapas, Mexico. Economic Botany, 48: 196–209.CrossRefGoogle Scholar
Blanckenhorn, W.U. and Henseler, C. 2005. Temperature-dependent ovariole and testis maturation in the yellow dung fly. Entomologia Experimentalis et Applicata, 116: 159–165.CrossRefGoogle Scholar
Chamorro-Florescano, I.A. and Favila, M.E. 2008. Male reproductive status affects contest outcome during nidification in Canthon cyanellus cyanellus LeConte (Coleoptera: Scarabaeidae). Behaviour, 145: 1811–1821.Google Scholar
Chamorro-Florescano, I.A., Favila, M.E., and Macías-Ordóñez, R. 2011. Ownership, size and reproductive status affect the outcome of food ball contests in a dung roller beetle: When do enemies share? Evolutionary Ecology, 25: 277–289.CrossRefGoogle Scholar
Chamorro-Florescano, I.A., Favila, M.E., and Macías-Ordóñez, R. 2017. Contests over reproductive resources in female roller beetles: outcome predictors and sharing as an option. PlosOne, 12: e0182931.CrossRefGoogle ScholarPubMed
Cisneiros, J.J. and Rosenheim, J.A. 1998. Changes in the foraging behavior, within-plant vertical distribution, and microhabitat selection of a generalist insect predator: an age analysis. Environmental Entomology, 27: 949–957.CrossRefGoogle Scholar
Clarke, K.R. and Gorley, R.N. 2006. Primer v6: user manual/tutorial. Primer-e, Albany, New Zealand.Google Scholar
Conrad, K.F., Wilson, K.H., Whitifield, K., Harvey, I.F., Thomas, C.J., and Sherratt, T.N. 2002. Characteristics of dispersing Ischnura elegans and Coenagrion puella (Odonata): age, sex, size, morph and ectoparasitism. Ecography, 25: 439–445.CrossRefGoogle Scholar
Córdoba-Aguilar, A., González-Tokman, D., and González-Santoyo, I. 2018. Insect behavior: from mechanisms to ecological and evolutionary consequences. Oxford University Press, Oxford, United Kingdom.CrossRefGoogle Scholar
Crawley, M.J. 2013. The R book. Second edition. Aptara Inc., Falls Church, Virginia, United States of America.Google Scholar
Cruz, R.M. and Huerta, C. 1998. Comportamiento y actividad reproductora de los machos de Copris incertus Say (Coleoptera, Scarabaeidae, Scarabaeinae). Acta Zoológica Mexicana, 74: 163–173.Google Scholar
Cruz, R.M. and Martínez, I. 1998. Effect of male mesadene secretions on females of Canthon cyanellus cyanellus (Coleoptera: Scarabaeidae). The Florida Entomologist, 81: 23–30.Google Scholar
Edelaar, P., Siepielski, A.M., and Clobert, J. 2008. Matching habitat choice causes directed gene flow: a neglected dimension in evolution and ecology. Evolution, 62: 2462–2472.CrossRefGoogle ScholarPubMed
Damborsky, M.P., Alvarez-Bohle, M.C., Ibarra-Polesel, M.G., Porcel, E.A., and Fontana, J.L. 2015. Spatial and temporal variation of dung beetle assemblages in a fragmented landscape at eastern humid Chaco. Neotropical Entomology, 44: 30–39.Google Scholar
Doube, B.M. 1983. The habitat preference of some bovine dung beetles (Coleoptera: Scarabaeidae) in Hluhluwe Game Reserve, South Africa. Bulletin of Entomological Research, 73: 357–371.CrossRefGoogle Scholar
Edwards, P.B. 1988. Field ecology of a brood-caring dung beetle Kheper nigroaeneus: as habitat predictability and life history strategy. Oecologia, 75: 527–534.CrossRefGoogle ScholarPubMed
Fahrig, L. 2003. Effects of habitat fragmentation on biodiversity. Annual Review of Ecology, Evolution, and Systematics, 34: 487–515.CrossRefGoogle Scholar
Favila, M.E. 1988. Comportamiento durante el periodo de maduración gonádica en un escarabajo rodador (Coleoptera: Scarabaeidae, Scarabaeinae). Folia Entomológica Mexicana, 76: 55–64.Google Scholar
Favila, M.E. 1993. Some ecological factors affecting the life-style of Canthon cyanellus cyanellus (Coleoptera Scarabaeidae): an experimental approach. Ecology, Ethology & Evolution, 5: 319–328.CrossRefGoogle Scholar
Favila, M.E. 2001. Historia de vida y comportamiento de un escarabajo necrofago: Canthon cyanellus cyanellus LeConte (Coleoptera: Scarabaeinae). Folia Entomológica Mexicana, 40: 245–278.Google Scholar
Favila, M.E. and Díaz, A. 1996. Canthon cyanellus cyanellus LeConte (Coleoptera: Scarabaeidae) makes a nest in the field with several brood balls. The Coleopterists Bulletin, 50: 52–60.Google Scholar
Filgueiras, B.K., Tabarelli, M., Leal, I.R., Vaz-de-Mello, F.Z., and Iannuzzi, L. 2015. Dung beetle persistence in human-modified landscapes: combining indicator species with anthropogenic land-use and fragmentation-related effects. Ecological Indicators, 55: 65–73.CrossRefGoogle Scholar
Gabe, M. 1968. Techniques histologiques. Editions Manson et Cie, Paris, France.Google Scholar
Halffter, G. and Arellano, L. 2002. Response of dung beetle diversity to human-induced changes in a tropical landscape. Biotropica, 34: 144–154.CrossRefGoogle Scholar
Halffter, G. and Edmonds, W.D. 1982. The nesting behavior of dung beetles (Scarabaeinae): an ecological and evolutive approach. Instituto de Ecología, México DF, Mexico.Google Scholar
Halffter, G. and Favila, M.E. 1993. The Scarabaeinae (Insecta: Coleoptera) an animal group for analyzing, inventorying and monitoring biodiversity in tropical rainforest and modified landscapes. Biology International, 27: 15–21.Google Scholar
Halffter, G., Favila, M.E., and Halffter, V. 1992. A comparative study on the structure of the scarab guild in Mexican tropical rain forests and derived ecosystems. Folia Entomológica Mexicana, 156: 131–156.Google Scholar
Halffter, G., Halffter, V., and Favila, M. 2011. Food relocation and the nesting behavior in Scarabaeus and Kheper (Coleoptera: Scarabaeinae). Acta Zoológica Mexicana, 27: 305–324.Google Scholar
Halffter, G., Halffter, V., and Huerta, C. 1983. Comportement sexuel et Nidification chez Canthon cyanellus cyanellus LeConte (COL: SCARABAEIDAE). Bulletin de la Société entomologique de France, 88: 585–594.Google Scholar
Hanski, I. 1980. Movement patterns in dung beetles and in the dung fly. Animal Behaviour, 28: 953–954.Google Scholar
Hanski, I. and Cambefort, Y. 1991. Dung beetle ecology. Princeton University Press, Princeton, United States of America.CrossRefGoogle Scholar
Hardie, J., Gibson, G., and Wyatt, T.D. 2001. Insect behaviors associated with resource finding. In Insect movement: mechanisms and consequences. Edited by I.P. Woinwod, D.R. Reynolds, and C.D. Thomas. CABI International Publishing, Wallingford, United Kingdom. Pp. 87–110.Google Scholar
Huerta, C., Halffter, G., and Halffter, V. 2005. Nidification in Eurysternus foedus Guérin-Méneville: its relationship to other dung beetle nesting patterns (Coleoptera: Scarabaeidae, Scarabaeinae). Folia Entomológica Mexicana, 44: 74–84.Google Scholar
Huerta, C. and Martínez, I.M. 2008. Morphological changes in reproductive organs and neuroendocrine centers related to nesting, mating and larvicide behavior in Eurysternus mexicanus Harold (Scarabaeinae: Eurysternini). The Coleopterists Bulletin, 62: 123–132.CrossRefGoogle Scholar
Hothorn, T., Zeileis, A., Farebrother, R.W., Cummins, C., Millo, G., and Mitchell, D. 2018. Package “lmtest”. Available from https://cran.r-project.org/web/packages/lmtest/lmtest.pdf [accessed 15 October 2019].Google Scholar
Jennions, M.D. and Moller, A.P. 2002. Publication bias in ecology and evolution: an empirical assessment using the ‘trim and fill’ method. Biological Reviews, 77: 211–222.CrossRefGoogle ScholarPubMed
Kemp, D.J. 2018. Habitat selection and territoriality. In Insect behavior: from mechanisms to ecological and evolutionary consequences. Edited by A. Córdoba-Aguilar, D. González-Tokman, and I. González-Santoyo. Oxford University Press, Oxford, United Kingdom. Pp. 80–97.Google Scholar
Larsen, T.H., Lopera, A., and Forsyth, A. 2006. Extreme trophic and habitat specialization by Peruvian dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae). The Coleopterists Bulletin, 60: 315–324.CrossRefGoogle Scholar
López-Guerrero, Y. and Halffter, G. 2000. Evolution of the spermatheca in the Scarabaeoidea (Coleoptera). Fragmenta Entomologica, 32: 225–285.Google Scholar
Lumbreras, C.J., Galante, E., and Mena, J. 1991. Ovarian condition as an indicator of the phenology of Bubas bubalus (Coleoptera: Scarabaeidae). Annals of the Entomological Society of America, 84: 190–194.CrossRefGoogle Scholar
Martínez, I. 2015. Bionomía del escarabajo estercolero Planolinellus vittatus (Say, 1825) (Coleoptera: Aphodiinae) en el Volcán Cofre de Perote, Veracruz, México. Dugesiana, 15: 131–140.Google Scholar
Martínez, I. and Cruz, M. 1998. Effects of nourishment on the gonadal maturation in Canthon cyanellus cyanellus LeConte (Coleoptera: Scarabaeidae: Scarabaeinae). The Coleopterists Bulletin, 52: 237–244.Google Scholar
Martínez, I., Lumaret, J.P., Zayas, R.O., and Kadiri, N. 2017. The effects of sublethal and lethal doses of ivermectin on the reproductive physiology and larval development of the dung beetle Euoniticellus intermedius (Coleoptera: Scarabaeidae). The Canadian Entomologist, 149: 461–472.CrossRefGoogle Scholar
Martínez, I. and Montes-de-Oca, E. 1994. Observaciones sobre algunos factores microambientales y el ciclo biologico de dos especies de escarabajos rodadores (Coleoptera, Scarabaeidae, Canthon). Folia Entomológica Mexicana, 91: 47–59.Google Scholar
Martínez, M., Escobar, F., Almendarez, S., Kory-Martínez, A., González-Gómez, L., and González-Tokman, D. 2019. Nuevos datos sobre la distribución y la biología reproductiva de Canthon imitator Brown 1946 (Coleoptera: Scarabaeidae: Scarabaeinae). Acta Zoológica Mexicana, 35: 1–7.CrossRefGoogle Scholar
Martínez, M.I. 2002. Técnicas básicas de anatomía microscópica y de morfometría para estudiar los insectos. Boletín de la Sociedad Entomológica Aragonesa, 30: 187–195.Google Scholar
Martínez, M.I. and Cruz-Rosales, M. 1988. Comportamiento, glándulas accesorias y centros neuroendocrinos en machos de dos especies de Canthon (Coleoptera: Scarabaeinae). Acta Zoológica Mexicana, 27: 1–19.Google Scholar
Martínez, M.I. and Cruz-Rosales, M. 1992. L’activité de l’appareil reproducteur mále pendant la vie imaginales chez deux especes de Canthon (Coleoptera: Scarabaeidae). Acta Zoológica Mexicana, 49: 1–22.Google Scholar
McKinney, M.L. and Lockwood, J.L. 1999. Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends in Ecology & Evolution, 14: 450–453.CrossRefGoogle ScholarPubMed
McPherson, J.M., Jetz, W., and Rogers, D.J. 2004. The effects of species’ range sizes on the accuracy of distribution models: ecological phenomenon or statistical artefact? Journal of Applied Ecology, 41: 811–823.CrossRefGoogle Scholar
Nolasco-Soto, J., Favila, M.E., De Los Monteros, A.E., González-Astorga, J., Halffter, G., Valdez-Carrasco, J., et al. 2020. Variations in genetic structure and male genitalia suggest recent lineage diversification in the neotropical dung beetle complex Canthon cyanellus (Scarabaeidae: Scarabaeinae). Biological Journal of the Linnean Society, in press: blaa131.CrossRefGoogle Scholar
Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O’Hara, R.B., et al. 2016. Vegan: community ecology package. Available from https://CRAN.R-project.org/package=vegan [accessed 15 October 2019].Google Scholar
Otavo, S.E., Parrada-Rosselli, A., and Noriega, J.A. 2013. Scarabaeoidea superfamily (Insecta: Coleoptera) as a bioindicator element of anthropogenic disturbance in an Amazon National Park. Revista de Biología Tropical, 61: 735–752.CrossRefGoogle Scholar
Paukku, S. and Kotiaho, J.S. 2008. Female oviposition decisions and their impact on progeny life-history traits. Journal of Insect Behavior, 21: 505–520.CrossRefGoogle Scholar
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., EISPACK, Heisterkamp, S., et al. 2019. Package ‘nlme’. Available from https://cran.r-project.org/web/packages/nlme/nlme.pdf [accessed 15 October 2019].Google Scholar
R Core Team 2015. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Salomão, R.P., Favila, M.E., González-Tokman, D., and Chamorro-Florescano, I.A. 2019. Contest dynamics for food and reproductive resources are defined by health condition in a dung beetle. Ethology, 125: 343–350.CrossRefGoogle Scholar
Salomão, R.P., González-Tokman, D., Dáttilo, W., López-Acosta, J.C., and Favila, M.E. 2018. Landscape structure and composition define the body condition of dung beetles (Coleoptera: Scarabaeinae) in a fragmented tropical rainforest. Ecological Indicators, 88: 144–151.CrossRefGoogle Scholar
Sarkar, D. 2018. Package ‘lattice’. Available from https://cran.r-project.org/web/packages/lattice/lattice.pdf [accessed 15 October 2020].Google Scholar
Sato, H. and Hiramatsu, K. 1993. Mating behaviour and sexual selection in the African ball-rolling scarab Khepher platynotus (Bates) (Coleoptera: Scarabaeidae). Journal of Natural History, 27: 657–668.CrossRefGoogle Scholar
Scholtz, C.H., Davis, A.L.V., and Kryger, U. 2009. Evolutionary biology and conservation of dung beetles. Pensoft Publishers, Sofia, Bulgaria.Google Scholar
Simpson, G.L., R Core Team, Bates, D.M., and Oksanen, J. 2018. Package ‘permute’. Available from https://cran.r-project.org/web/packages/permute/permute.pdf [accessed 15 October 2019].Google Scholar
Solís, A. and Kohlmann, B. 2002. El género Canthon (Coleoptera: Scarabaeidae) en Costa Rica. Giornale Italiano di Entomologia, 10: 1–68.Google Scholar
Souza, T.B., França, F.M., Barlow, J., Dodonov, P., Santos, J.S., Faria, D., and Baumgarten, J.E. 2020. The relative influence of different landscape attributes on dung beetle communities in the Brazilian Atlantic forest. Ecological Indicators, 117: 106534.CrossRefGoogle Scholar
Tabarelli, M., Aguiar, A.V., Ribeiro, M.C., Metzger, J.P., and Peres, C.A. 2010. Prospects for biodiversity conservation in the Atlantic forest: lessons from aging human-modified landscapes. Biological Conservation, 143: 2328–2340.CrossRefGoogle Scholar
Tabarelli, M., Peres, C.A., and Melo, F.P.L. 2012. The “few winners and many losers” paradigm revisited: emerging prospects for tropical forest biodiversity. Biological Conservation, 155: 136–140.CrossRefGoogle Scholar
Ting, J.J., Judge, K.A., and Gwynne, D.T. 2017. Listening to male song induces female field crickets to differentially allocate reproductive resources. Journal of Orthoptera Research, 26: 205–210.CrossRefGoogle Scholar
Tyndale-Biscoe, M. and López-Guerrero, Y. 1982. Egg resorption in Phanaeus daphnis Harold (Coleoptera: Scarabaeidae). Folia Entomológica Mexicana, 52: 27–39.Google Scholar
Wagner, J.D. and Bakare, A. 2017. Lifetime reproductive effort is equal between the sexes in seed beetles (Callosobruchus maculatus): dispelling the myth of the cheap male. Ethology, Ecology & Evolution, 29: 387–396.CrossRefGoogle Scholar
Zuur, A.F., Ieno, E.N., Walker, N.J., Saveliev, A.A., and Smith, G.M. 2009. Mixed effects models and extensions in ecology with R. Springer, New York, New York, United States of America.CrossRefGoogle Scholar