Are Anthelminthic Treatments of Captive Ruminants Necessary?

Anthelmintics are frequently administered to animals to limit fecal egg elimination, so that wild animals in captive breeding programs are treated to maintain a proper health condition. This is effective from a health management perspective, but on the other hand, it could prevent captive animals from developing an effective immunity against parasites that they might encounter when reintroduced into their original geographic areas. The aim of this study was to describe the dynamics of parasite infections in captive Cuvier's gazelles (Gazella cuvieri) not treated with anthelmintics for two years and to evaluate the factors related to their fecal egg shedding. Fifteen one-year-old males were enclosed together and captured monthly to collect feces directly from the rectum. Fecal egg counts were performed, and eggs were classified as strongylid-like, Nematodirus sp., or Trichuris sp. Fecal egg shedding for the three groups of parasites did not vary significantly over the duration of the study. Only precipitation affected the egg-shedding pattern of all parasites, while inbreeding was positively associated with the number of strongylid-like parasites. These findings suggest an equilibrium between hosts and parasites in absence of treatment during the study. The anthelmintic treatment as a systematic prophylaxis method in captive animals should be avoided and replaced by systematic coprological and clinical vigilance, as well as targeted treatment in the case of a significant rise of fecal egg counts.

Zoological institutions as hotspots of gastrointestinal parasites that may affect the success of ungulate reintroduction programmes.

BACKGROUND: Ungulates from zoological institutions are frequently used as founders in reintroduction programmes. These animals are subject to specific parasite management as parasitic infections have previously been associated with failed Bovidae reintroductions. METHODS: Questionnaires to obtain data on how these institutions screen for seasonal parasite presence and the clinical signs they induced in threatened ungulates were sent to 65 institutions involved in European Ex situ Programmes (58.5% response rate). Temperature and relative humidity data were also obtained to categorize each zoological centre. RESULTS: Strongyloides spp. (52.6%), Trichuris spp. (42.1%), Trichostrongylidae family (39.4%) and Eimeria spp. (36.8%) were the most frequently reported parasites in the received questionnaires. Climatic variables did not influence parasite presence. CONCLUSION: Our results suggest that artificial microenvironments created by husbandry practices and enclosure design in zoos could create hotspots for gastrointestinal parasites. To maximise the success of reintroduction projects, we recommend that the influence of microclimates on parasite burdens be evaluated.

Effect of Season and Social Environment on Semen Quality and Endocrine Profiles of Three Endangered Ungulates (Gazella cuvieri, G. dorcas and Nanger dama).

Knowledge of factors affecting semen quality could be of great importance for the collection and preservation of semen from threatened animals. To assess the effect of seasonality, sperm parameters and testosterone levels were examined throughout the year and compared with the distribution of conceptions. Cuvier's gazelle showed higher sperm quantity in April, coinciding with one peak of conceptions. In dorcas gazelle, sperm parameters showed a drop in October. However, percentage of conceptions increased during that month. In Mohor gazelle, sperm quality was best in April and August, in agreement with higher conception rates and high testosterone levels. Percentage of conceptions was correlated with photoperiod and rainfall in Cuvier's gazelle and with temperature in Mohor gazelle. To assess the effect of social environment, semen quality, testosterone and cortisol levels were quantified in males housed alone, in bachelor groups or with females. No differences were seen in Cuvier's and Mohor gazelles' semen traits, whereas dorcas males housed with females showed lower semen quality than males kept alone or with other males. Overall, ejaculate quality is influenced by seasonal factors in the three gazelle species, while social factors only appear to affect that of dorcas gazelle.

Survey of husbandry practices for bovidae in zoos: the importance of parasite management for reintroduction programmes.

Animals from zoological institutions may be used for reintroductions. These individuals are considered healthy, but they are not necessarily free of parasites, despite the minimum husbandry standards required of zoological institutions as described in the European Association of Zoos and Aquaria guidelines. In this sense, parasitism has been identified as the cause of failure, or has added difficulties, in some reintroduction programmes. Here the authors attempt to summarise the risk of parasitism to animals originating from zoological institutions by analysing a questionnaire about parasite prevalence, sampling methods, treatment and control in three ungulates in European zoos. Completed questionnaires were received from 38 institutions (58.5 per cent response rate). Most of the responding institutions (97 per cent) detected the eggs of endoparasites in faeces, but only one reported ectoparasites. Most institutions followed a similar preventive schedule, with ivermectin as the preferred prophylactic treatment for parasites, commonly administered in food every six months. The frequent use of concentrating flotation techniques as the sole method to evaluate the presence of parasite eggs in faecal samples is not recommended because it fails to detect trematode and lung nematode infections, so it would be better to use flotation techniques together with sedimentation procedures or serological and molecular tests. The results suggest that parasite control in zoological institutions can be complicated, indicating the need to implement a specific management schedule for institutions involved in reintroduction projects.

Coxiella burnetii detected in three species of endangered North African gazelles that recently aborted.

Coxiella (C.) burnetii is the etiological agent of the zoonotic disease known a Q fever. This agent can infect multiple hosts although its pathogenic potential in wild ruminants has been poorly studied. The polymerase chain reaction and the serological test detected the presence of C. burnetii in a population of North African gazelles (n = 355), comprising dorcas gazelle (Gazella dorcas neglecta), dama gazelle (Nanger dama mhorr) and Cuvier's gazelle (Gazella cuvieri) which, some of them, they recently aborted. Serological tests for Brucella spp., C. burnetii, Chlamydophila abortus, border disease pestivirus, and Toxoplasma spp. were performed together with specific cultures to detect Salmonella spp., Listeria spp., and Campylobacter spp. and a polymerase chain reaction for C. burnetii on serum and vaginal swabs samples collected from a representative number of animals (n = 65). These tests only detected the presence of C. burnetii in 18 specimens (27.3%). C. burnetii was the only pathogen detected, with eight animals testing positive on the polymerase chain reaction, 15 on the serological test, and five on both the tests. This article reveals the presence of C. burnetii during a medium and late-stage abortions occurred in a population of North African gazelles. The presence of C. burnetii as causal agent of abortions in Cuvier's gazelles has never been reported. The consequences of the findings are discussed here, showing the need to adopt urgent control measures to prevent the spread of C. burnetii in captive populations that are essential for the conservation of these endangered species.

Heterozygosity-fitness correlations and inbreeding depression in two critically endangered mammals.

The relation among inbreeding, heterozygosity, and fitness has been studied primarily among outbred populations, and little is known about these phenomena in endangered populations. Most researchers conclude that the relation between coefficient of inbreeding estimated from pedigrees and fitness traits (inbreeding-fitness correlations) better reflects inbreeding depression than the relation between marker heterozygosity and fitness traits (heterozygosity-fitness correlations). However, it has been suggested recently that heterozygosity-fitness correlations should only be expected when inbreeding generates extensive identity disequilibrium (correlations in heterozygosity and homozygosity across loci throughout the genome). We tested this hypothesis in Mohor gazelle (Gazella dama mhorr) and Iberian lynx (Lynx pardinus). For Mohor gazelle, we calculated the inbreeding coefficient and measured heterozygosity at 17 microsatellite loci. For Iberian lynx, we measured heterozygosity at 36 microsatellite loci. In both species we estimated semen quality, a phenotypic trait directly related to fitness that is controlled by many loci and is affected by inbreeding depression. Both species showed evidence of extensive identity disequilibrium, and in both species heterozygosity was associated with semen quality. In the Iberian lynx the low proportion of normal sperm associated with low levels of heterozygosity was so extreme that it is likely to limit the fertility of males. In Mohor gazelle, although heterozygosity was associated with semen quality, inbreeding coefficient was not. This result suggests that when coefficient of inbreeding is calculated on the basis of a genealogy that begins after a long history of inbreeding, the coefficient of inbreeding fails to capture previous demographic information because it is a poor estimator of accumulated individual inbreeding. We conclude that among highly endangered species with extensive identity disequilibrium, examination of heterozygosity-fitness correlations may be an effective way to detect inbreeding depression, whereas inbreeding-fitness correlations may be poor indicators of inbreeding depression if the pedigree does not accurately reflect the history of inbreeding.

Changes in Habitat Structure May Explain Decrease in Reintroduced Mohor Gazelle Population in the Guembeul Fauna Reserve, Senegal.

Reintroduction is a widespread method for saving populations of endangered species from extinction. In spite of recent reviews, it is difficult to reach general conclusions about its value as a conservation tool, as authors are reluctant to publish unsuccessful results. The Mohor gazelle is a North African gazelle, extinct in the wild. Eight individuals were reintroduced in Senegal in 1984. The population grew progressively, albeit slowly, during the first 20 years after release, but then declined dramatically, until the population in 2009 was estimated at no more than 13-15 individuals. This study attempts to determine the likelihood of gazelle-habitat relationships to explain why the size of the gazelle population has diminished. Our results show that the Mohor gazelle in Guembeul is found in open habitats with less developed canopy where the grass is shorter, suggesting the possibility that changes in habitat structure have taken place during the time the gazelles have been in the Reserve, reducing the amount of suitable habitat. Reintroduction design usually concentrates on short-term factors that may affect survival of the released animals and their descendants (short-term achievement), while the key factors for assessing its success may be those that affect the long-term evolution of the population.

High levels of DNA fragmentation in spermatozoa are associated with inbreeding and poor sperm quality in endangered ungulates.

Inbreeding is known to cause deleterious effects upon reproduction and survival, but its effects upon sperm DNA integrity have not been examined. In the present study, we analyzed this relationship among three endangered ungulates: Gazella cuvieri, Gazella dama mhorr, and Gazella dorcas neglecta. In addition, we examined whether levels of sperm DNA fragmentation are associated with semen quality. The magnitude of sperm DNA damage in the two species with high levels of inbreeding (G. cuvieri and G. dama mhorr) was extremely high when compared to the species with low levels of inbreeding (G. dorcas neglecta) and to values previously reported for outbred populations. Levels of sperm DNA fragmentation significantly increased with inbreeding and age. Increased DNA damage in sperm was associated with increased sperm head abnormalities, lower percentage of sperm with an intact acrosome, and poor motility. Our findings suggest that the link between inbreeding and semen quality is mediated by the effects of inbreeding upon sperm DNA damage. The deleterious effects of inbreeding upon the paternal genome likely decrease male fertility and may cause genetic damage to future generations. Because inbreeding is common among endangered species, high levels of sperm DNA damage may have considerable impact upon the viability of their populations.

Paternal levels of DNA damage in spermatozoa and maternal parity influence offspring mortality in an endangered ungulate.

Understanding which factors influence offspring mortality rates is a major challenge since it influences population dynamics and may constrain the chances of recovery among endangered species. Most studies have focused on the effects of maternal and environmental factors, but little is known about paternal factors. Among most polygynous mammals, males only contribute the haploid genome to their offspring, but the possibility that sperm DNA integrity may influence offspring survival has not been explored. We examined several maternal, paternal and individual factors that may influence offspring survival in an endangered species (Gazella cuvieri). Levels of sperm DNA damage had the largest impact upon offspring mortality rates, followed by maternal parity. In addition, there was a significant interaction between these two variables, so that offspring born to primiparous mothers were more likely to die if their father had high levels of sperm DNA damage, but this was not the case among multiparous mothers. Thus, multiparous mothers seem to protect their offspring from the deleterious effects of sperm DNA damage. Since levels of sperm DNA damage seem to be higher among endangered species, more attention should be paid to the impact of this largely ignored factor among the viability of endangered species.

Pedigrees and microsatellites among endangered ungulates: what do they tell us?

Relationships between pedigree coefficients of inbreeding and molecular metrics are generally weak, suggesting that measures of heterozygosity estimated using microsatellites may be poor surrogates of genome-wide inbreeding. We compare three endangered species of gazelles (Gazella) with different degrees of threat in their natural habitats, for which captive breeding programmes exist. For G. dorcas, the species with the largest founding population, the highest and most recent number of founding events, the correlation between pedigree coefficient of inbreeding and molecular metrics was higher than for outbred populations of mammals, probably because it has both higher mean f and variance. For the two species with smaller founding populations, conventional assumptions about founders, i.e. outbred and unrelated, are unrealistic. When realistic assumptions about the founders were made, clear relationships between pedigree coefficients of inbreeding and molecular metrics were revealed for G. cuvieri. This population had a small founding population, but it did experience admixture years later; thus, the relationship between inbreeding and molecular metrics in G. cuvieri is very similar to the expected values but lower than in G. dorcas. In contrast, no relationship was found for G. dama mhorr which had a much smaller founding population than had been previously assumed, which probably had high levels of inbreeding and low levels of genetic variability, and no admixture. In conclusion, the strength of the association between pedigree coefficient of inbreeding and molecular metrics among endangered species depends on the level of inbreeding and genetic variability present in the founding population, its size and its history.

Output of gastrointestinal nematode eggs in the feces of captive gazelles (Gazella dama mhorr, Gazella cuvieri and Gazella dorcas neglecta) in a semiarid region of southeastern Spain.

Feces from 62 captive African gazelles, including Mhorr gazelles (Gazella dama mhorr), Cuvier's gazelles (Gazella cuvieri), and Dorcas gazelles (Gazella dorcas neglecta), were examined over the course of a year to quantitate nematode egg excretion patterns. Strongyloides sp. eggs appeared only in G. dama during the rainy season. Trichostrongylidae egg excretion showed a marked seasonal variation, with very low levels during the dry and hot period, a finding that is probably attributable to hypobiosis of the predominant species (Camelostrongylus mentulatus). Eggs of the Nematodirus sp., predominantly Nematodirus spathiger, were excreted throughout the year. No seasonal pattern was observed in Trichuris sp. egg excretion.