Neotropical carnivores include a large number of threatened and endangered species. It is critical to develop conservation efforts to ensure the sustainability of populations in situ and ex situ. The highest priorities are to protect natural habitats and better understand the biology of rare species. Conservation efforts also are directed toward the implementation of breeding programs and the development of reproductive biotechnologies in which the cryopreservation of male gametes plays a major role. It also is fundamental to create semen banks that contribute to maintaining genetic diversity in small and endangered populations. The present article aims at reviewing the state of the art in cryopreservation of semen from neotropical carnivores and discuss the development of systematic banking for the conservation of these understudied species.
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References
1.
Renctas. I relatório nacional sobre gestão e uso sustentável da fauna silvestre. [I national report on management and sustainable use of wildlife].Brasília, DF, Brasil: Rede Nacional de Combate ao Tráfico de Animais Silvestres (RENCTAS); 2016: 668.
2.
CeballosG, EhrlichPR, BarnoskyAD, et al.Accelerated modern human-induced species losses: Entering the sixth mass extinction. Sci Adv, 2015; 1:e1400253.
3.
SalvadorS, ClavernoM, PitmanRL. Large mammal species richness and habitat use in an upper Amazonian forest used for ecotourism. Mamm Biol, 2011; 76:115–123.
4.
WildtDE. Genetic resource banks for conserving wildlife species: Justification, examples and becoming organized on a global basis. Anim Reprod Sci, 1992; 28:247–257.
5.
ComizzoliP, HoltWV. Recent advances and prospects in germplasm preservation of rare and endangered species. Adv Exp Med Biol, 2014; 753:331–356.
6.
ComizzoliP. Biobanking and fertility preservation for rare and endangered species. Anim Reprod, 2017; 14:30–33.
7.
PeggDE. Principles of cryopreservation. Methods Mol Biol, 2007; 368:39–57.
8.
YuI, LeiboSP. Recovery of motile, membrane-intact spermatozoa from canine epididymides stored for 8 days at 4°C. Theriogenology, 2001; 57:1179–1190.
9.
LuvoniGC, KalchschmidtE, LeoniS, et al.Conservation of feline semen. Part I: Cooling and freezing protocols. J Feline Med Surg, 2003; 5:1–6.
10.
LuvoniGC. Gamete cryopreservation in the domestic cat. Theriogenology, 2006; 66:101–111.
11.
TeodoroLO, Melo-JuniorAA, SpercoskiAA, et al.Seasonal aspects of reproductive physiology in captive male Maned Wolves (Chrysocyon brachyurus, Illiger, 1815). Reprod Domest Anim, 2012; 47:250–255.
12.
WildtDE, BushM, HowardJG, et al.Unique seminal quality in the South African cheetah and a comparative evaluation in the domestic cat. Biol Reprod, 1983; 29:1019–1025.
13.
BarrosFFPC, QueirozJPAF, FilhoACM, et al.Use of two anesthetic combinations for semen collection by electroejaculation from captive coatis (Nasua nasua). Theriogenology, 2009; 71:1261–1266.
14.
MaklerA, DavidR, BlumenfeldZ, et al.Factors affecting sperm motility. VII. Sperm viability as affected by change of pH and osmolarity of semen and urine specimens. Fertil Steril, 1981; 36:507–511.
15.
SouzaNP, GuimarãesLD'A, PazRCR. Dosagem hormonal e avaliação testicular em cachorro do mato (Cerdocyon thous) utilizando-se diferentes protocolos anestésicos. [Hormone dosing and testicular evaluation in crab-eating fox (Cerdocyon thous) using different anesthetic protocols]. Arq Bras Med Vet Zootec, 2011; 63:1224–1228.
16.
JohnsonAEM, FreemanEW, WildtDE, et al.Spermatozoa from the maned wolf (Chrysocyon brachyurus) display typical canid hyper-sensitivity to osmotic and freezing-induced injury, but respond favorably to dimethyl sulfoxide. Cryobiology, 2014; 68:361–370.
17.
AraujoGR, PaulaTAR, Deco-SouzaT, et al.Ocelot and oncilla spermatozoa can bind hen egg perivitelline membranes. Anim Reprod Sci, 2015; 163:56–62.
18.
PazRCR. Reprodução assistida em canídeos e procionídeos neotropicais. [Assisted reproduction in neotropical canidae and procyonidae]. Rev Bras Reprod Anim, 2015; 39:77–82.
19.
OkanoT, NakamuraS, KomatsuT, et al.Characteristics of frozen–thawed spermatozoa cryopreserved with different concentrations of glycerol in captive Japanese black bears (Ursus thibetanus japonicus) J Vet Med Sci, 2006; 68:1101–1104.
20.
HowardJG. Semen collection and analysis in carnivores. In: FowlerME (ed). Zoo & Wild Animal Medicine Current Therapy, 3rd ed. Philadelphia, PA: W.B. Saunders; 1993: 390–399.
21.
PazRCR, GuidoMC, CostaEO, et al.Microbiota Prepucial de onças pintadas (Panthera onca) mantidas em cativeiro. [Preputial Microbiota of jaguars (Panthera onca) kept in captivity]. Proceedings of Congresso Brasileiro para Conservação de Felinos Neotropicais, Jundiaí, São Paulo, Brasil; 1999.
22.
GuidoMC, PazRCR, CostaEO, et al.Microbiota prepucial e vaginal de felinos neotropicais mantidos em cativeiro. [Preputial and vaginal microbiota of neotropical felines kept in captivity]. Proceedings of Combravet XVII Congresso Brasileiro de Medicina Veterinária, Águas de Lindóia, São Paulo, Brasil; 2000: 03.
23.
JordanHL, HowardJG, SellonRK. Transmission of feline immunodeficiency virus in domestic cats via artificial insemination. J Virol, 1996; 70:8224–8228.
24.
LuedersI, LutherI, MüllerK, et al.Semen collection via urethral catheter in exotic feline and canine species: A simple alternative to electroejaculation. International Conference on Diseases of Zoo and Wild Animals, Vienna, Austria; 2013.
25.
AraujoGR, PaulaTAR, Deco-SouzaT, et al.Comparison of semen samples collected from wild and captive jaguars (Panthera onca) by urethral catheterization after pharmacological induction. Anim Reprod Sci, 2018; 195:1–7.
26.
JewgenowS, BlottnerS, LengwinatT, et al.New methods for gamete rescue from gonads of non-domestic felids. J Reprod Fertil Suppl, 1997; 51:33–39.
27.
MaksudovGY, ShishovaNV, KatkovII. In the cycle of life: Cryopreservation of post-mortem sperm as a valuable source in restoration of rare and endangered species. In ColumbusAM, KuznetsovLV (eds). Endangered Species: New Research Edition, 1st ed. New York: NOVA Publishers; 2008: 189–240.
28.
ChristensenBW, AsaCS, WangC, et al.Effect of semen collection method on sperm motility of gray wolves (Canis lupus) and domestic dogs (C. l. familiaris). Theriogenology, 2011; 76:975–980.
29.
SilvaAR, MoratoRG, SilvaLDM. The potential for gamete recovery from non-domestic canids and felids. Anim Reprod Sci, 2004; 81:159–175.
30.
BergeronA, ManjunathP. New insights towards understanding the mechanisms of sperm protection by egg yolk and milk. Mol Reprod Dev, 2006; 73:1338–1344.
31.
ErdmannRH. Protocolos de criopreservação de sêmen em felídeos do gênero Leopardus e quantificação de metabólitos fecais de andrógenos e glicocorticoides. [Semen cryopreservation protocols in the felids of Leopardus gender and androgens and glucocorticoids fecal metabolites quantification]. Thesis—Universidade Federal do Paraná, Curitiba/PR, Brasil; 2014: 142.
32.
SilvaHVR, NunesTGP, FreitasLA, et al.Avaliação dos parâmetros seminais em onça-pintada (Panthera onca) durante a curva de resfriamento comparando os diluidores Tris e ACP-117c. [Evaluation of the semen parameters in jaguar (Panthera onca) during the cooling curve comparing the Tris and ACP-117c extenders]. Rev Bras Reprod Anim Anais CBRA 2017, 2017; 41:589.
33.
PazRCR, ZugeRM, BarnabeVH. Frozen Jaguar (Panthera onca) sperm capacitation and ability to penetrate zona free hamster oocytes. Braz J Vet Res Anim Sci, 2007; 44:337–344.
34.
BaudiDLK, JewgenowK, PukazhenthiBS, et al.Influence of cooling rate on the ability of frozen–thawed sperm to bind to heterologous zona pellucida, as assessed by competitive in vitro binding assays in the ocelot (Leopardus pardalis) and tigrina (Leopardus tigrinus). Theriogenology, 2008; 69:204–211.
35.
AraujoGR. Coleta farmacológica e criopreservação de sêmen de grandes felinos, mantidos em cativeiro e capturados em vida livre com o uso de armadilhas de laço: Reprodução assistida em onças pintadas e onças pardas. [Pharmacological collection and seminal cryopreservation of large felines kept in captivity and in the wildlife, caught using snares: Assisted reproduction in jaguars and pumas]. Thesis—Universidade Federal de Viçosa, Viçosa/BH, Brasil; 2016: 81.
36.
PazRCR, AvilaHBS. Coatis (Nasua nasua) semen cryopreservation. Braz J Vet Res Anim Sci, 2015; 52:151–157.
37.
AmstislavskyS, LindebergH, LuvoniGC. Reproductive technologies relevant to the genome resource bank in Carnivora. Reprod Domest Anim, 2012; 47:164–175.
38.
Deco-SouzaT, PaulaTAR, CostaDS, et al.Comparação entre duas concentrações de glicerol para a criopreservação de sêmen de suçuarana (Puma concolor). [Comparison between two glycerol concentrations to cryopreservation of semen of mountain lions (Puma concolor)]. Pesq Vet Bras, 2013; 33:512–516.
TebetJM. Efeito da criopreservação sobre a célula espermática em três espécies de felinos: A jaguatirica (Leopardus pardalis), o tigrina (L. tigrinus) e o gato doméstico (Felis catus). [Cryopreservation effect on sperm cell in three species of felids: Ocelot (Leopardus pardalis), tigrina (L. tigrinus) and domestic cat (Felis catus)]. Thesis—Faculty of Veterinary Medicine and Animal Science, Universidade Estadual Paulista, Botucatu/SP, Brasil; 2004: 117.
41.
MoraisRN. Reproduction in small felids males. In: FowlerME, CubasZS (ed). Biology, Medicine and Surgery of South America Wild Animals, 1st ed. Ames, IA: Iowa State University Press; 2001: 312–316.
42.
MonfortSL. Reproductive Sciences in Animal Conservation. New York, NY: Springer; 2014: 15–31.
43.
WildtDE, ComizzoliP, PukazhenthiB, et al.Lessons from biodiversity-the value of nontraditional species to advance reproductive science, conservation, and human health. Mol Reprod Dev, 2010; 77:397–409.
44.
HuangY, WangP, ZhangG, et al.Use of artificial insemination to enhance propagation of giant pandas at the Wolong Breeding Center. Proceedings of the 2nd International Symposium on Assisted Reproductive Technologies for Conservation and Genetic Management of Wildlife; Henry Doorly Zoo, Omaha, NE, September 28–29, 2002; 172–179.
45.
HowardJG, LynchC, SantymireRM, et al.Recovery of gene diversity using long-term cryopreserved spermatozoa and artificial insemination in the endangered black-footed ferret. Anim Conserv, 2015; 19:102–111.
46.
HowardJG, WildtDE. Approaches and efficacy of artificial insemination in felids and mustelids. Theriogenology, 2009; 71:130–148.
47.
SeagerSWJ, PlatzCC, HodgeW. Successfull pregnancy using frozen semen in the wolf. Int Zoo Yearb, 1975; 15:140–143.
48.
SwansonWF, HowardJG, RothTL, et al.Responsiveness of ovaries to exogenous gonadotrophins and laparoscopic artificial insemination with frozen-thawed spermatozoa in ocelots (Felis pardalis). J Reprod Fertil, 1996; 106:87–94.
49.
BaroneMA, WildtDE, ByersAP, et al.Gonadotrophin dose and timing of anaesthesia for laparoscopic artificial insemination in the puma (Felis concolor). J Reprod Fertil, 1994; 101:103–108.
50.
MoraesW, MoraisRN, MoreiraN, et al.Successful artificial insemination after exogenous gonadotropin treatment in the ocelot (Leopardus pardalis) and tigrina (Leopardus tigrina). Proceedings American Association of Zoo Veterinarians Conference. Houston, TX, October26–30, 1997:334–335.
