Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.1590/1984-3143-AR2020-0213
Animal Reproduction (AR)
REVIEW ARTICLE

Understanding how environmental factors influence reproductive aspects of wild myomorphic and hystricomorphic rodents

Maiko Roberto Tavares Dantas; João Batista Freire Souza-Junior; Thibério de Souza Castelo; Arthur Emannuel de Araújo Lago; Alexandre Rodrigues Silva

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Abstract

Abstract: Myomorphic and hystricomorphic rodents are vital for maintaining various ecosystems around the planet. This review enables a better understanding of how these rodents respond to environmental factors and adapt to climate adversities. Innumerable factors, such as photoperiod, rainfall, and temperature, can impair or contribute to the quality of rodent reproductive parameters. Prolonged animal exposure to high ambient temperatures alters thermoregulation mechanisms and causes testicular and ovarian tissue degeneration and hormonal deregulation. Photoperiod influences the biological circannual rhythm and reproductive cycles of rodents because it strongly regulates melatonin secretion by the pineal gland, which modulates gonadotropic hormone secretion. Rainfall quantity directly regulates the abundance of fruits in an ecosystem, which modulates the reproductive seasonality of species which are most dependent on a seasonal fruit-based diet. Species with a more diversified fruit diet have smaller reproductive seasonality. As such, habitats are chosen by animals for various reasons, including the availability of food, sexual partners, intra-and inter-specific competition, and predation. This knowledge allows us to monitor and establish management plans to aid in conservation strategies for wild rodent species.

Keywords

climate, seasonality, reproductive physiology, Rodentia, wildlife

References

Acosta M, Mohamed F. Effect of the photoperiod and administration of melatonin on folliculostellate cells of the pituitary pars distalis of adult male viscacha (Lagostomus maximus maximus). Acta Histochem. 2011;113(6):640-6. https://doi: 10.1016/j.acthis.2010.08.003. PMID: 20828800.

Aguilera-Merlo C, Fogal T, Sator T, Dominguez S, Sosa M, Scardapane L, Piezzi R. Ultrastructural and biochemical seasonal changes in epididymal corpus and cauda of viscacha (Lagostomus maximus maximus). J Morphol. 2009;270(7):805-14. https://doi: 10.1002/jmor.10718. PMid: 19123245.

Bodmer R, Mayor P, Antunez M, Chota K, Fang T, Puertas P, Pittet M, Kirkland M, Walkey M, Rios C, Perez-Peña P, Henderson P, Bodmer W, Bicerra A, Zegarra J, Docherty E. Major shifts in Amazon wildlife populations from recent intensification of floods and drought. Conserv Biol. 2018;32(2):333-44. http://dx.doi.org/10.1111/cobi.12993. PMid:28766738.

Bronson FH, Heideman PD. Seasonal regulation of reproduction in mammals. In: Knobil E, Neil JD, editors. The physiology of reproduction. New York: Raven Press Ltd.; 1994. p. 541-73.

Busolini FI, Rodríguez GB, Filippa VP, Mohamed FH. Pigmented cells in the pineal gland of female viscacha (Lagostomus maximus maximus): a histochemical and ultrastructural study. Int J Endocrinol. 2017;2017:7492960. https://doi: 10.1155/2017/7492960. PMID: 29391866.

Carleton MD, Musser GG. Order Rodentia. In: Wilson DE, Reeder DM, editors. Mammal species of the world a taxonomic and geographic reference. 2nd ed. Baltimore: Johns Hopkins University Press; 2005. p. 745-52.

Castelo TS, Souza ALP, Lima GL, Peixoto GCX, Campos LB, Oliveira MF, Silva AR. Interactions among different devices and electrical stimulus on the electroejaculation of captive agoutis (Dasyprocta leporina). Reprod Domest Anim. 2015;50(3):492-6. http://dx.doi.org/10.1111/rda.12517. PMid:25800458.

Comizzoli P, Crosier AE, Songsasen N, Gunther MS, Howard JG, Wildt DE. Advances in reproductive science for wild carnivore conservation. Reprod Domest Anim. 2009;44(2, Suppl 2):47-52. http://dx.doi.org/10.1111/j.1439-0531.2009.01373.x. PMid:19754535.

Comizzoli P. Biotechnologies for wildlife fertility preservation. Anim Front. 2015;5(1):73-8. http://dx.doi.org/10.2527/af.2015-0011.

Cruceño AM, de Rosas JC, Fóscolo M, Chaves EM, Scardapane L, Dominguez S, Aguilera-Merlo C. Effects of photoperiod on epididymal and sperm morphology in a Wild Rodent, the Viscacha (Lagostomus maximus maximus). Int Schol Res Not. 2013:128921. https://doi.org/10.5402/2013/128921.

Dubost G, Henry O, Comizzoli P. Seasonality of reproduction in the three largest terrestrial rodents of French Guiana forest. Mamm Biol. 2005;70(2):93-109. http://dx.doi.org/10.1016/j.mambio.2004.09.001.

Dubost G, Henry O. Seasonal reproduction in neotropical rainforest mammals. Zool Stud. 2017;56:e2. http://dx.doi.org/10.6620/ZS.2017.56-02. PMid:31966201.

Durairajanayagam D, Agarwal A, Ong C. Causes, effects and molecular mechanisms of testicular heat stress. Reprod Biomed Online. 2014;30(1):14-27. http://dx.doi.org/10.1016/j.rbmo.2014.09.018. PMid:25456164.

El Bizri HF, Fa JE, Bowler M, Valsecchi J, Bodmer R, Mayor P. Breeding seasonality in the lowland paca (Cuniculus paca) in Amazonia: interactions with rainfall, fruiting, and sustainable hunting. J Mammal. 2018;99(5):1101-11. http://dx.doi.org/10.1093/jmammal/gyy102.

El-Sabrout K. Effect of rearing system and season on behaviour, productive performance and carcass quality of rabbit: a review. J Anim Behav Biometeorol. 2018;6(4):102-8. http://dx.doi.org/10.31893/2318-1265jabb.v6n4p102-108.

Fabio-Braga AP, Klein W. Temperature and circadian effects on metabolic rate of South American echimyid rodents, Trinomys setosus and Clyomys bishopi (Rodentia: echimyidae). Zoologia (Curitiba). 2018;35:e24572. http://dx.doi.org/10.3897/zoologia.35.e24572.

Frankham R. Genetic adaptation to captivity in species conservation programs. Mol Ecol. 2008;17(1):325-33. http://dx.doi.org/10.1111/j.1365-294X.2007.03399.x. PMid:18173504.

Gallol LE, Busolini FI, Mohamed FH. Influence of melatonin and sexual hormones on the expression of proliferating cell nuclear antigen in the adrenal cortex of a seasonal breeder (Lagostomus maximus). Anat Rec (Hoboken). 2020;303(12):3052-67. http://dx.doi.org/10.1002/ar.24457. PMid: 32445505.

Gentile R, Fernandez FAS. Influence of habitat structure on a streamside small mammal community in a Brazilian rural area. Mammalia. 1999;63(1):29-40. http://dx.doi.org/10.1515/mamm.1999.63.1.29.

Goulart FVB, Cáceres NC, Graipel ME, Tortato MA, Ghizoni IR Jr, Oliveira-Santos LGR. Habitat selection by large mammals in a southern Brazilian Atlantic Forest. Mamm Biol. 2009;74(3):182-90. http://dx.doi.org/10.1016/j.mambio.2009.02.006.

Henry O, Dubost G. Breeding periods of Gerbillus cheesmani (Rodentia, Muridae) in Saudi Arabia. Mammalia. 2012;76(4):383-7. http://dx.doi.org/10.1515/mammalia-2012-0017.

IUCN Global Species Programme Red List Unit – IUCN. The IUCN red list of threatened species. Version, 2019. United Kingdom: IUCN Global Species Programme Red List Unit; 2019 [cited 2019 Oct 25]. Avaliable from: http://www.iucnredlist.org

Kleisner K, Ivell R, Flegr J. The evolutionary history of testicular externalization and the origin of the scrotum. J Biosci. 2010;35(1):27-37. http://dx.doi.org/10.1007/s12038-010-0005-7. PMid:20413907.

Maia KM, Silva AR. Influence of seasonality on mammals reproduction. Research & Reviews: Zool Sci. 2016;4:43-50.

Mascarenhas NMH, Costa ANL, Pereira MLL, Caldas ACA, Batista LF, Gonçalves EL. Thermal conditioning in the broiler production: challenges and possibilities. J Anim Behav Biometeorol. 2018;6(2):52-5. http://dx.doi.org/10.31893/2318-1265jabb.v6n2p52-55.

Maurya VP, Sejian V, Kumar D, Naqvi SMK. Impact of heat stress, nutritional stress and their combinations on the adaptive capability of Malpura sheep under hot semi-arid tropical environment. J Anim Behav Biometeorol. 2019;7(1):31-8. http://dx.doi.org/10.31893/2318-1265jabb.v7n1p31-38.

Mayor P, Bodmer RE, Lopez-Bejar M. Functional anatomy of the female genital organs of the wild black agouti (Dasyprocta fuliginosa) female in the Peruvian Amazon. Anim Reprod Sci. 2011;123(3-4):249-57. http://dx.doi.org/10.1016/j.anireprosci.2010.12.006. PMid:21216112.

Muñoz A, Bonal R, Díaz M. Ungulates, rodents, shrubs: interactions in a diverse Mediterranean ecosystem. Basic Appl Ecol. 2009;10(2):151-60. http://dx.doi.org/10.1016/j.baae.2008.01.003.

Muñoz A, Bonal R. Linking seed dispersal to cache protection strategies. Ecology. 2011;99(4):1016-25. http://dx.doi.org/10.1111/j.1365-2745.2011.01818.x.

Muteka SP, Chimimba CT, Bennett NC. Reproductive seasonality in the Tete veld rat (Aethomys ineptus) (Rodentia: Muridae) from southern Africa. J Zool (Lond). 2006a;270(6):314-23. http://dx.doi.org/10.1111/j.1469-7998.2006.00140.x.

Muteka SP, Chimimba CT, Bennett NC. Reproductive seasonality in Aethomys namaquensis (Rodentia: Muridae) from southern Africa. J Mammal. 2006b;87(1):67-74. http://dx.doi.org/10.1644/05-MAMM-A-088R2.1.

Muteka SP, Chimimba CT, Bennett NC. Reproductive photoresponsiveness in Aethomys ineptus and A. namaquensis (Rodentia: Muridae) from southern Africa. J Zool (Lond). 2006c;268(3):225-31. http://dx.doi.org/10.1111/j.1469-7998.2005.00022.x.

Muteka SP, Chimimba CT, Bastos AD, Bennett NC. the reproduction pattern of in the Gerbilliscus cf. leucogaster (Rodentia: Muridae) from Namibia. Can J Zool. 2018;97(1):57-62. http://dx.doi.org/10.1139/cjz-2018-0090.

O’Malley B. Introduction to small mammals. In: O’Malley B, editor. Clinical anatomy and physiology of exotic species: structure and function of mammals, birds, reptiles, and amphibians. London, UK: Elsevier Saunders; 2005. p. 165.

Praxedes ECG, Peixoto GCX, Silva AM, Silva AR. Reproduction in agouti (Dasyprocta spp.): A review of reproductive physiology for developing assisted reproductive techniques. Anim Reprod. 2018;15(4):1181-92. http://dx.doi.org/10.21451/1984-3143-AR2018-0058.

Queiroz JPAF, Souza JBF Jr, Oliveira VRM, Castelo TS, Dantas MRT, Costa LLM, Oliveira MF. Sensible heat transfer and thermal windows in Dasyprocta leporina (Mammalia, Rodentia). Biol Rhythm Res. 2019;50(2):1-13. http://dx.doi.org/10.1080/09291016.2018.1440771.

Queiroz JPAF, Souza-Junior JBF, Oliveira VRM, Costa LLM, Oliveira MF. How does Spix’s yellow-toothed cavy (Galea spixii Wagler, 1831) face the thermal challenges of the Brazilian tropical dry forest? J Therm Biol. 2020;88:102525. http://dx.doi.org/10.1016/j.jtherbio.2020.102525. PMid:32126000.

Rashamol VP, Sejian V, Bagath M, Krishnan G, Archana PR, Bhatta R. Physiological adaptability of livestock to heat stress: an updated review. J Anim Behav Biometeorol. 2018;6(3):62-72. http://dx.doi.org/10.31893/2318-1265jabb.v6n3p62-71.

Rezende EL, Bozinovic F. Thermal performance across levels of biological organization. Philos Trans R Soc Lond B Biol Sci. 2019;374(1778):20180549. http://dx.doi.org/10.1098/rstb.2018.0549. PMid:31203764.

Rocha RMP, Lima LF, Alves AMCV, Celestino JJH, Matos MHT, Lima‐Verde IB, Bernuci MP, Lopes CAP, Báo SN, Campello CC, Rodrigues APR, Figueiredo JR. Interaction between melatonin and follicle‐stimulating hormone promotes in vitro development of caprine preantral follicles. Domest Anim Endocrinol. 2013;44(1):1-9. http://dx.doi.org/10.1016/j.domaniend.2012.07.001. PMid:22920266.

Romanovsky AA, Ivanov AI, Shimansky YP. Selected contribution: ambient temperature for experiments in rats: a new method for determining the zone of thermal neutrality. J Appl Physiol. 2002;92(6):2667-79. http://dx.doi.org/10.1152/japplphysiol.01173.2001. PMid:12015388.

Salman SA, Shahid S, Ismail T, Chung ES, Al-Abadi AM. Long-term trends in daily temperature extremes in Iraq. Atmos Res. 2017;198:97-107. http://dx.doi.org/10.1016/j.atmosres.2017.08.011.

Santos BF. Macro e microambientes. In: Andrade A, Pinto SC, Oliveira RS, editors. Animais de laboratório: criação e experimentação. Rio de Janeiro: Fiocruz; 2002. p. 388.

Santos-Filho M, Da Silva DJ, Sanaiotti TM. Variação sazonal na riqueza e na abundância de pequenos mamíferos, na estrutura da floresta e na disponibilidade de artrópodes em fragmentos florestais no Mato Grosso, Brasil. Biota Neotrop. 2008;8(1):115-21. http://dx.doi.org/10.1590/S1676-06032008000100014.

Santos-Filho M, Frieiro-Costa F, Ignácio ÁR, Silva MN. Use of habitats by non-volant small mammals in Cerrado in Central Brazil. Braz J Biol. 2012;72(4):893-902. http://dx.doi.org/10.1590/S1519-69842012000500016. PMid:23295519.

Sarli J, Lutermann H, Alagaili AN, Mohammed OB, Bennett NC. Seasonal reproduction in the Arabian spiny mouse, Acomys dimidiatus (Rodentia: Muridae) from Saudi Arabia: The role of rainfall and temperature. J Arid Environ. 2016;124:352-9. http://dx.doi.org/10.1016/j.jaridenv.2015.09.008.

Setchell BP. The effects of heat on the testes of mammals. Anim Reprod. 2006;3(2):81-91. http://dx.doi.org/10.1007/s12522-011-0105-6.

Silva RG. Introdução à bioclimatologia animal. São Paulo: Nobel; 2000. p. 286.

Slade B, Parrott ML, Paproth A, Magrath MJ, Gillespie GR, Jessop TS. Assortative mating among animals of captive and wild origin following experimental conservation releases. Biol Lett. 2014;10(11):20140656. http://dx.doi.org/10.1098/rsbl.2014.0656. PMid:25411380.

Stapp P. Habitat selection by insectivorous rodent: patterns and mechanisms across multiple scales. J Mammal. 1997;78(4):1128-43. http://dx.doi.org/10.2307/1383055.

Šumbera R, Zelová J, Kunc P, Knížková I, Burda H. Patterns of surface temperatures in two molerats (Bathyergidae) with different social systems as revealed by IR-thermography. Physiol Behav. 2007;92(3):526-32. http://dx.doi.org/10.1016/j.physbeh.2007.04.029. PMid:17544016.

Tavolaro FM, Thomson LM, Ross AW, Morgan PJG. Photoperiodic effects on seasonal physiology, reproductive status and hypothalamic gene expression in young male F344 rats. J Neuroendocrinol. 2015;27(2):79-87. https://doi.org/10.1111/jne.12241. PMid:25443173.

Trillmich F, Mueller B, Kaiser S, Krause J. Puberty in female cavies (Cavia aperea) is affected by photoperiod and social conditions. Physiol Behav. 2009;96(3):476-80. http://dx.doi.org/10.1016/j.physbeh.2008.11.014. PMid:19087883.

Wang D, Li N, Tian L, Ren F, Li Z, Chen Y, Liu L, Hu X, Zhang X, Song Y, Hut RA, Liu XH. Dynamic expressions of hypothalamic genes regulate seasonal breeding in a natural rodent population. Mol Ecol. 2019;28(15):3508-22. http://dx.doi.org/10.1111/mec.15161. PMid:31233652.

Wube T, Haim A, Fares F. Effect of increased dietary salinity on the reproductive status and energy intake of xeric and mesic populations of the spiny mouse, Acomys. Physiol Behav. 2009;96(1):122-7. http://dx.doi.org/10.1016/j.physbeh.2008.09.006. PMid:18824007.

Zhang P, Zheng Y, Lv Y, Li F, Su L, Qin Y, Zeng W. Melatonin protects the mouse testis against heat-induced damage. Mol Hum Reprod. 2020;29(2):65-79. http://dx.doi.org/10.1093/molehr/gaaa002. PMid:31943111.

Zheng M, Nagaoka K, Watanabe G. Pre-pubertal exposure to high temperature impairs ovarian and adrenal gland function in female rats. J Vet Med Sci. 2019;81(2):279-86. http://dx.doi.org/10.1292/jvms.18-0644. PMid:30587674.
 


Submitted date:
09/22/2020

Accepted date:
02/15/2021

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