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Comparison of Semen Characteristics and Sperm Cryopreservation in Common Marmoset (Callithrix Jacchus) and Black-­Tufted-­Ear Marmoset (Callithrix Penicillata)

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Comparison of Semen Characteristics and Sperm Cryopreservation in Common Marmoset (Callithrix Jacchus) and Black-­Tufted-­Ear Marmoset (Callithrix Penicillata) Received: 24 May 2018 | Accepted: 13 September 2018 DOI: 10.1111/jmp.12388 ORIGINAL ARTICLE Comparison of semen characteristics and sperm cryopreservation in common marmoset (Callithrix jacchus) and black- tufted- ear marmoset (Callithrix penicillata) Paloma Rocha Arakaki1 | Marcílio Nichi1 | Frederico Ozanan Barros Monteiro2 | José Augusto Pereira Carneiro Muniz3 | Marcelo Alcindo de Barros Vaz Guimarães1 | Rodrigo del Rio do Valle4 1Department of Animal Reproduction, College of Veterinary Abstract Medicine and Animal Science, University of Background: The common marmoset (Callithrix jacchus) is one of the most studied São Paulo, São Paulo, SP, Brazil Neotropical primates regarding reproduction. However, little has been reported on 2Postgraduate Program in Animal Health and Production in Amazonia, Federal Rural the black- tufted- ear marmoset (Callithrix penicillata), which may produce fertile hy- University of the Amazon, Belém, PA, Brazil brids with other Callithrix. This is the first study to evaluate sperm freezing from 3National Primate Center, Health Ministry, black-tufted- ear marmoset. Ananindeua, PA, Brazil 4Institute of Health Sciences, Paulista Methods: Testicles from all animals were measured, and semen was collected by pe- University, São Paulo, SP, Brazil nile vibrostimulation. Samples were analyzed after collection, after chilling and addi- Correspondence tion of glycerol, and after thawing. Paloma Rocha Arakaki, Department of Results and Conclusions: Fresh semen from both species was similar in many as- Animal Reproduction, College of Veterinary Medicine and Animal Science, University of pects. Additionally, there is a relationship between total motility, plasma membrane São Paulo, São Paulo, SP, Brazil. integrity, and acrosome integrity observed in sperm samples from both species. We Email: [email protected] managed to evaluate fresh and thawed sperm with suitable methods for use under Funding information zoo or field conditions. However, TEST egg yolk with glycerol at 4% and 6% concen- Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) tration was not effective for sperm protection in both species during cryopreservation. KEYWORDS glycerol, penile vibratory stimulation, primate conservation, semen evaluation, TES-TRIS 1 | INTRODUCTION five occur in Neotropics.4 In this context, the creation of genetic re- sources banks, consisting in the organized collection, storage, and Currently, some non-human primates (NHP) are classified as threat- use of germplasm—including sperm, from individuals of threatened ened or endangered by the International Union for Conservation or non- threatened species—to be used in the future, is an important of Nature (IUCN). Their populations are declining mainly because tool to contribute to the conservation of these animals.5,6 of habitat loss or hunting. Conservation of biological diversity is a Attempts to cryopreserve semen of NHP, especially the most major challenge nowadays, mostly because of increasing anthropic commonly found species in captivity, have occurred in recent actions influence in the environment. Worldwide, the Neotropical decades. However, reliable information on the most appropriate region stands out for being among the regions presenting greatest methodologies is still limited.7 Cryopreservation of sperm from biodiversity, however, some areas in this region are in risk of loss of Neotropical primates has been reported for some species, in- biodiversity.1-3 Of the world’s 25 most endangered primates species, cluding squirrel monkeys (Saimiri sciureus, S. boliviensis, S. collinsi, J Med Primatol. 2018;1–11. wileyonlinelibrary.com/journal/jmp © 2018 John Wiley & Sons A/S. | 1 Published by John Wiley & Sons Ltd 2 | ARAKAKI ET AL. (A) (B) FIGURE 1 The species studied (A) common marmoset (Callithrix jacchus) and (B) black- tufted ear marmoset (Callithrix penicillata). Photos: Luis Claúdio Marigo S. vanzolinii, S. cassiquiarensis, S. macrodon), spider monkeys National Primate Center – CENP, located at Ananindeua city, (Ateles paniscus, A. marginatus), and one species of capuchin mon- state of Pará, Northern Brazil. Animals were housed in enclosures key (Sapajus apella), tamarin (Saguinus labiatus), howler monkey (1.5 m × 0.9 m × 2 m) positioned in a north- south orientation to re- (Alouatta caraya), and common marmoset (Callithrix jacchus).8-18 ceive 12 hours of natural light each day, with groups’ compositions As described for Old World monkeys,7 the cryoprotectants used typically consisting of a male, a female, and their young prole. The usually contain glycerol in different concentrations—ranging from average temperature was 33°C, and humidity was 85%. Evaluated 1.5% to 8%, alone or in combination with egg yolk (used most males were adults, with a mean age of 4.5 years for both species, often), or soy lecithin.8-18 ranging from 3 to 9 years in common marmoset and from 3 to Based on sperm motility, the studies that presented the best results 7 years in black- tufted- ear marmoset, all with a proven history of in frozen- thawed sperm were in S. sciureus and S. labiatus,8,16 which fertility (presence of offspring). The diet consisted of daily fresh presented a loss of 18.55% and 12.5% in sperm motility, respectively. fruits, vegetables, and primate pellets (Callitrichidae P25 Megazoo®, The first study used a medium containing 11% of lactose, 4% of glyc- Betim, MG, Brazil); animals also received beetle larvae twice a week, erol, and 20% of egg yolk, with freezing in dry ice blocks, and in the and water was available ad libitum. second one, epididimal samples were frozen in liquid nitrogen vapor, in a Tes-, Tris-, and egg yolk-based medium, with 5% of glycerol. 2.3 | Testicular morphometry and semen collection There are six species in Callithrix genus (C. jacchus, C. penicillata, C. kuhlii, C. geoffroyi, C. aurita, and C. flaviceps).19 Regarding their repro- During procedures, an expert animal keeper physically restrained ductive biology, the common marmoset (C. jacchus) is the best known the animals. To evaluate testicular morphometry, animals were kept model from this genus. Despite this, there are only a few reports re- in the dorsal decubitus position, and both testes were measured with garding semen cryopreservation for the common marmoset and none a digital caliper. We determined testicular volume by Lambert’s em- for the black- tufted- ear marmoset (C. penicillata). The objectives of pirical formula: volume = length × width × height × 0.71,20 already this study were (a) to collect semen using the penile vibrostimulation applied for other Neotropical primate, Goeldi’s monkey (Callimico technique and describe its characteristics from the black- tufted- ear goeldii).21 Total testicular volume was calculated by adding the vol- marmoset; (b) to compare fresh semen from common marmoset and umes of the right and left testicles. We measured the scrotal circum- black- tufted- ear marmoset; and (c) to test two glycerol concentrations ference with a measuring tape. (4% and 6%) for semen cryopreservation of these two species. After inspection and palpation of testicles, genital area was washed with liquid soap (hypoallergenic glycerinated baby soap, Casa Granado® Laboratórios, Farmácias e Drogarias SA, Belém, PA, 2 | MATERIALS AND METHODS Brazil), rinsed with water at 37°C, and dried with soft paper, to min- imize animal discomfort. We performed all semen collections in the morning before feed- 2.1 | Humane care guidelines ing, and the interval between collections from the same male was at This research complied with protocols approved by the Ethics least 1 week. Semen was collected from February to May in 2013 Committee in the Use of Animals from College of Veterinary Medicine (rainy season). and Animal Science, University of São Paulo (no 2275/2013) and ad- During semen collection, animals remained restrained by the hered to the Brazilian legal requirements (SISBIO/ICMBio/MMA no hands of the assistant; one hand held the head, thorax, and fore- 28608- 2). limb of the animal, and the other hand contained the left leg and tail, exposing the genital region to receive the artificial stimuli from the vibrostimulation apparatus. 2.2 | Animals and housing conditions Semen samples from the common marmoset (n = 18) and the Common marmoset males (n = 8) and black- tufted- ear marmo- black- tufted- ear marmoset (n = 6) were collected by penile vibro- set males (n = 10) (Figure 1) were maintained in captivity at the stimulation technique (PVS) using a vibrostimulation apparatus ARAKAKI ET AL. | 3 (FertiCare® -­ Multicept ApS, Rungsted, Denmark), with modifications samples, we diluted semen with TALP- HEPES at a ratio of 1:1, prior of a published protocol22 previously used for common marmoset.23 to addition of staining, in order to reduce the presence of debris (a The stimuli applied for obtaining the ejaculates varied according reaction of staining solution with egg yolk contained in the cryopro- to the responses of individuals and between species. For common tectant) in background.25 Both stainings were validated for common marmoset, frequency of 70- 80 Hz and amplitude of 1.0 mm, and for marmoset semen by Valle et al23 black- tufted- ear marmoset, frequency of 75- 85 Hz and amplitude Mitochondrial activity was evaluated by 3,3′diaminobenzidine of 1.0- 1.5 mm. Semen collection procedure consisted of repeated (DAB) staining.26 Semen was placed in an amber tube with the same series of two minutes of stimulation, followed by resting phases of quantity of
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