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Annual reproductive phenology of the coprophagous beetle Dichotomius satanas (Coleoptera: Scarabaeidae, Scarabaeinae) of the cloud forest in eastern Mexico

Published online by Cambridge University Press:  08 January 2021

Julliana Barretto Open the ORCID record for Julliana Barretto [Opens in a new window] ,
Magdalena Cruz  and
Federico Escobar Open the ORCID record for Federico Escobar [Opens in a new window]
Julliana Barretto
Affiliation:
Red de Ecoetología, Instituto de Ecología, A.C., Carretera antigua a Coatepec 351, El Haya, Xalapa, VeracruzC.P. 91073, México
Magdalena Cruz
Affiliation:
Red de Ecoetología, Instituto de Ecología, A.C., Carretera antigua a Coatepec 351, El Haya, Xalapa, VeracruzC.P. 91073, México
Federico Escobar*
Affiliation:
Red de Ecoetología, Instituto de Ecología, A.C., Carretera antigua a Coatepec 351, El Haya, Xalapa, VeracruzC.P. 91073, México
*
*Corresponding author. Email: federico.escobarf@gmail.com
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Abstract

Reproductive phenology of organisms is modulated by biotic and abiotic factors, with direct effects on the demography. This study describes the annual reproductive phenology of Dichotomius satanas (Harold, 1867) (Coleoptera: Scarabaeidae, Scarabaeinae) of the cloud forest in eastern Mexico, through the morphological changes in the reproductive systems of individuals and their relationship with climatic conditions. Three stages of sexual maturity were recognised as occurring throughout the year: immature, maturing, and mature – with a higher occurrence of immature individuals. Abundance of immature and maturing females was explained by minimum temperature, but none of the environmental variables considered was related to mature females. Abundance of immature and maturing males was related to precipitation, while abundance of mature males was related to minimum temperature and precipitation. The phenology of D. satanas was markedly seasonal with a single peak of abundance corresponding to the reproductive period during the warm and rainy season, thus indicating a univoltine pattern of reproduction. Immature females were recorded before immature males, and no synchrony was observed between the maturing and mature males and females. We provide information pertaining to the reproductive biology of coprophagous beetles and highlight the importance of reproductive phenology as a tool with which to understand future environmental scenarios.

Type
Research Papers
Information
The Canadian Entomologist , Volume 153 , Issue 2 , April 2021 , pp. 157 - 171
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Copyright
© The Author(s), 2021 Published by Cambridge University Press on behalf of the Entomological Society of Canada

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Footnotes

Subject Editor: Katie Marshall

References

Bang, H.S., Crespo, C.H., Na, Y.E., Han, M.S., and Lee, J.H. 2008. Reproductive development and seasonal activity of two Korean native Coprini species (Coleoptera: Scarabaeidae). Journal of Asia–Pacific Entomology, 11: 195–199. https://doi.org/10.1016/j.aspen.2008.09.007.CrossRefGoogle 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: 2. https://doi.org/10.3390/insects10010002.CrossRefGoogle Scholar
Blume, R.R. and Aga, A. 1975. Onthophagus gazella: mass rearing and laboratory biology. Environmental Entomology, 4: 735–736. https://doi.org/10.1093/ee/4.5.735.CrossRefGoogle Scholar
Bonal, R., Hernández, M., Espelta, J.M., Muñoz, A., and Aparicio, J.M. 2015. Unexpected consequences of a drier world: evidence that delay in late summer rains biases the population sex ratio of an insect. Royal Society Open Science, 2: 150198. https://doi.org/10.1098/rsos.150198.CrossRefGoogle ScholarPubMed
Bonal, R., Munoz, A., and Espelta, J.M. 2010. Mismatch between the timing of oviposition and the seasonal optimum: the stochastic phenology of Mediterranean acorn weevils. Ecological Entomology, 35: 270–278. https://doi.org/10.1111/j.1365–2311.2010.01178.x.CrossRefGoogle Scholar
Bourg, A., Escobar, F., MacGregor-Fors, I., and Moreno, C.E. 2016. Got dung? Resource selection by dung beetles in Neotropical forest fragments and cattle pastures. Neotropical Entomology, 45: 490–498. https://doi.org/10.1007/s13744–016–0397–7.CrossRefGoogle ScholarPubMed
Breiman, L. 2001. Random forests. Machine Learning, 45: 5–32.CrossRefGoogle Scholar
Burnham, K.P. and Anderson, D.R. 2002. Information and likelihood theory: a basis for model selection and inference. In Model selection and multimodel inference: a practical information-theoretic approach. Edited by Burnham, K.P. and Anderson, D.R.. Springer, New York, New York, United States of America. Pp. 66–67.Google Scholar
Calabrese, J.M., Ries, L., Matter, S.F., Debinski, D.M., Auckland, J.N., Roland, J., and Fagan, W.F. 2008. Reproductive asynchrony in natural butterfly populations and its consequences for female matelessness. Journal of Animal Ecology, 77: 746–756. https://doi.org/10.1111/j.1365-2656.2008.01385.x.CrossRefGoogle ScholarPubMed
Chuine, I. 2010. Why does phenology drive species distribution? Philosophical Transactions of the Royal Society B: Biological Sciences, 365: 3149–3160. https://doi.org/10.1098/rstb.2010.0142.CrossRefGoogle ScholarPubMed
Clark, L.R., Geier, P.W., Hugues, R.D., and Morris, R.F. 1978. The ecology of insect populations in theory and practice. The English Language Book Society and Methuen Book Society, London, United Kingdom.Google Scholar
Cruz, M. and Martínez, I. 1998. Effect of male mesadene secretions on females of Canthon cyanellus cyanellus (Coleoptera: Scarabaeidae). Florida Entomologist, 81: 23–30. https://doi.org/10.2307/3495993.Google Scholar
Cutler, D.R., Edwards, T.C., Beard, K.H., Cutler, A., Hess, K.T., Gibson, J., and Lawler, J.J. 2007. Random forests for classification in ecology. Ecology, 88: 2783–2792. https://doi.org/10.1890/07–0539.1.CrossRefGoogle ScholarPubMed
Degen, T., Hovestadt, T., Mitesser, O., and Hölker, F. 2015. High female survival promotes evolution of protogyny and sexual conflict. PLOS One, 10: e0118354. https://doi.org/10.1371/journal.pone.0118354.CrossRefGoogle ScholarPubMed
Duchenne, F., Thébault, E., Michez, D., Elias, M., Drake, M., Persson, M., et al. 2020. Phenological shifts alter the seasonal structure of pollinator assemblages in Europe. Nature Ecology & Evolution, 4: 115–121. https://doi.org/10.1038/s41559-019-1062-4.CrossRefGoogle ScholarPubMed
Encinas-Viso, F., Revilla, T.A., and Etienne, R.S. 2012. Phenology drives mutualistic network structure and diversity. Ecology Letters, 15: 198–208. https://doi.org/10.1111/j.1461-0248.2011.01726.x.CrossRefGoogle ScholarPubMed
Escobar, F. and Chacón de Ulloa, P. 2000. Distribución espacial y temporal en un gradiente de sucesión de la fauna de coleópteros coprófagos (Scarabaeinae, Aphodiinae) en un bosque tropical montano, Nariño – Colombia. Revista de Biología Tropical, 48: 961–975.Google Scholar
Forrest, J.R. 2016. Complex responses of insect phenology to climate change. Current Opinion in Insect Science, 17: 49–54. https://doi.org/10.1016/j.cois.2016.07.002.CrossRefGoogle ScholarPubMed
González-Megías, A. and Sánchez-Piñero, F. 2004. Resource limitation of nesting: chance favors the prepared dung beetle. Environmental Entomology, 33: 188–196. https://doi.org/10.1603/0046-225X-33.2.188.CrossRefGoogle Scholar
Halffter, G. and Edmonds, W.D. 1982. The nesting behavior of dung beetles (Scarabaeinae). An ecological and evolutive approach. Man and Biosphere Program – UNESCO. Tlalpan, Districto Federal, Mexico.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
Halffter, G. and Lopez, G.Y. 1977. Development of the ovary and mating behavior in Phanaeus . Annals of the Entomological Society of America, 70: 203–213. https://doi.org/10.1093/aesa/70.2.203.CrossRefGoogle Scholar
Halffter, G. and Matthews, E.G. 1966. The natural history of dung beetles of the subfamily Scarabaeinae (Coleoptera: Scarabaeidae). Folia Entomologia Mexicana, Distrito Féderal, Mexico.Google Scholar
Halffter, G., Pineda, E., Arellano, L., and Escobar, F. 2007. Instability of copronecrophagous beetle assemblages (Coleoptera: Scarabaeinae) in a mountainous tropical landscape of Mexico. Environmental Entomology, 36: 1397–1407.CrossRefGoogle Scholar
Hanski, I. and Cambefort, Y. 1991. Dung beetle ecology. Princeton University Press, Princeton, New Jersey, United States of America.CrossRefGoogle Scholar
Hernández-Martínez, G. and Martínez, M.I. 2003. Desarrollo larval de Canthon cyanellus cyanellus LeConte 1859 (Coleoptera: Scarabaeidae). Acta Zoológica Mexicana, 89: 185–200.Google Scholar
Huerta, C. and Bang, H.S. 2004. Fecundity and offspring survival of Copris tripartitus Waterhouse (Coleoptera, Scarabaeidae: Scarabaeinae) under laboratory rearing conditions. The Coleopterists Bulletin, 58: 501–508. https://doi.org/10.1649/638.CrossRefGoogle 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
Ishihara, M. 1999. Adaptive phenotypic plasticity and its difference between univoltine and multivoltine populations in a bruchid beetle, Kytorhinus sharpianus . Evolution, 53: 1979–1986. https://doi.org/10.1111/j.1558-5646.1999.tb04579.x.CrossRefGoogle Scholar
Kendall, M.G. and Gibbons, J.D. 1990. Rank correlation methods. Oxford University Press, New York, New York, United States of America.Google Scholar
Kingston, T.J. and Coe, M. 1977. The biology of a giant dung-beetle (Heliocopris dilloni) (Coleoptera: Scarabaeidae). Journal of Zoology, 181: 243–263. https://doi.org/10.1111/j.1469-7998.1977.tb03239.x.CrossRefGoogle Scholar
Liaw, A. and Wiener, M. 2018. Classification and regression based on a forest of trees using random inputs. R Package.Google Scholar
Martínez, I. 1992. Données comparatives sur l’activité reproductrice de Canthon indigaceus chevrolati Harold et Canthon cyanellus cyanellus LeConte (Coleoptera: Scarabaeidae). In Annales de la Société Entomologique de France. Edited by la Société Entomologique de France. Pp. 397–408.Google Scholar
Martínez, I. 2002. Metodologías: técnicas básicas de anatomía microscópica y de morfometría para estudiar los insectos. Bolletín de la Sociedad Entomológica Aragonesa, 30: 187–195.Google Scholar
Martínez, I. and Cruz, M. 1999. The effects of male glandular secretions on female endocrine centers in Canthon cyanellus cyanellus LeConte (Coleoptera: Scarabaeidae, Scarabaeinae). The Coleopterists Bulletin, 53: 208–216.Google Scholar
Martínez, I. and Huerta, C. 1997. Coordinated activity of the ovary, pars intercerebralis and corpus allatum during the prenesting and nesting cycles of Copris incertus Say (Coleoptera Scarabaeidae: Scarabaeinae). The Coleopterists’ Bulletin, 51: 351–363.Google Scholar
Martínez, I. and Montes de Oca, E. 1988. Comportamiento, ovario y centros neuroendocrinos en hembras de dos especies de Canthon (Coleoptera: Scarabaeinae). Folia Entomologica Mexicana, 75: 33–46.Google 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). Sociedad Mexicana de Entomologia, Veracruz (Mexico).Google Scholar
Martínez, M.I., Montes De Oca, E., and Cruz, M. 1998. Contribución al conocimiento de la biología del escarabajo coprófago Onthophagus incensus Say (Coleoptera: Scarabaeidae: Scarabaeinae): datos ecológicos y reproductivos en relación a su fenología. Folia Entomológica Mexicana, 103: 1–13.Google Scholar
Menu, F. 1993. Strategies of emergence in the chestnut weevil Curculio elephas (Coleoptera: Curculionidae). Oecologia, 96: 383–390. https://doi.org/10.1007/BF00317509.CrossRefGoogle Scholar
Moisen, G.G. 2008. Classification and regression trees. In Encyclopedia of Ecology. Edited by Jorgensen, S.E. and Fath, B.D.. Elsevier Inc., Oxford, United Kingdom. Pp. 582–588.CrossRefGoogle Scholar
Pardo-Diaz, C., Lopera Toro, A., Peña-Tovar, S.A., Sarmiento-Garcés, R., Sánchez-Herrera, M., and Salazar, C. 2019. Taxonomic reassessment of the genus Dichotomius (Coleoptera: Scarabaeinae) through integrative taxonomy. PeerJ, 7: e7332. http://doi.org/10.7717/peerj.7332.CrossRefGoogle ScholarPubMed
Pineda, E., Moreno, C., Escobar, F., and Halffter, G. 2005. Frog, bat, and dung beetle diversity in the cloud forest and coffee agroecosystems of Veracruz, Mexico. Conservation Biology, 19: 400–410. https://doi.org/10.1111/j.1523-1739.2005.00531.x.CrossRefGoogle Scholar
Pomfret, J.C. and Knell, R.J. 2008. Crowding, sex ratio and horn evolution in a South African beetle community. Proceedings of Royal Society B, 275: 315–321. https://doi.org/10.1098/rspb.2007.1498.CrossRefGoogle Scholar
Pozsgai, G. and Littlewood, N.A. 2014. Ground beetle (Coleoptera: Carabidae) population declines and phenological changes: is there a connection? Ecological Indicators, 41: 15–24. https://doi.org/10.1016/j.ecolind.2014.01.029.CrossRefGoogle Scholar
Régnière, J. 2009. Predicting insect continental distributions from species physiology. Unasylva, 60: 37–42.Google Scholar
Rhainds, M. 2010. Female mating failures in insects. Entomologia Experimentalis et Applicata, 136: 211–226.CrossRefGoogle Scholar
Rös, M., Escobar, F., and Halffter, G. 2012. How dung beetles respond to a human-modified variegated landscape in Mexican cloud forest: a study of biodiversity integrating ecological and biogeographical perspectives. Diversity and Distributions, 18: 377–389. https://doi.org/10.1111/j.1472-4642.2011.00834.x.CrossRefGoogle Scholar
Sánchez-Carrillo, M., Huerta, C., Carrillo-Ruiz, H., and Escobar, F. 2017. Anatomical description of the reproductive system and maturation states in females of Omorgus suberosus (Fabricius) (Coleoptera: Trogidae). The Coleopterists Bulletin, 71: 137–142. https://doi.org/10.1649/0010-065X-71.1.137.CrossRefGoogle Scholar
Takeda, M. 2004. Effects of temperature on oviposition in overwintering females and hatch in first-generation larvae of Pseudaulacaspis pentagona (Hemiptera: Diaspididae). Applied Entomology and Zoology, 39: 15–26. https://doi.org/10.1303/aez.2004.15.CrossRefGoogle Scholar
Thornhill, R. and Alcock, J. 1983. The evolution of insect mating systems. Harvard University Press, Cambridge, Massachusetts, United States of America.CrossRefGoogle Scholar
Trivers, R. 1972. Parental investment and sexual selection. In Sexual selection & the descent of man. Edited by Campbell, B.C.. Aldine Press, New York, New York, United States of America. Pp. 139–179.Google Scholar
Tyndale-Biscoe, M. 1983. Effects of ovarian condition on nesting behaviour in a brood-caring dung beetle, Copris diversus Waterhouse (Coleoptera: Scarabaeidae). Bulletin of Entomological Research, 73: 45–45. https://doi.org/10.1017/S000748530001378X.CrossRefGoogle Scholar
Van Timmerman, S.J., Switzer, P.V., and Kruse, K.C. 2000. Emergence and reproductive patterns in the Japanese beetle, Popillia japonica (Coleoptera: Scarabaeidae). Journal of the Kansas Entomological Society, 70: 17–27.Google Scholar
Varley, G., Gradwell, G., and Hassell, M. 1973. Insect population ecology: an analytical approach. University of California Press, Oakland, California, United States of America.Google Scholar
Williams-Linera, G. 2002. Tree species richness complementarity, disturbance and fragmentation in a Mexican tropical montane cloud forest. Biodiversity and Conservation, 11: 1825–1843. https://doi.org/10.1023/A:1020346519085.CrossRefGoogle Scholar
Williams-Linera, G. and Vizcaíno-Bravo, Q. 2016. Cloud forests on rock outcrop and volcanic soil differ in indicator tree species in Veracruz, Mexico. Revista Mexicana de Biodiversidad, 87: 1265–1274. https://doi.org/10.1016/j.rmb.2016.09.003.CrossRefGoogle Scholar
Zuur, A.F., Ieno, E.N., Walker, N., 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. Pp. 209–259.CrossRefGoogle Scholar
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