Palaeozoological insights into management options for a threatened mammal: southern Africa’s Cape mountain zebra (Equus zebra zebra)

Aim Promoting population growth of genetically distinct subpopulations of Cape mountain zebra (Equus zebra zebra) is crucial to the survival of the subspecies. Several important Cape mountain zebra reserves are dominated by fynbos vegetation, and population growth is limited by a lack of grassland habitat. A fossil ungulate sequence spanning the last c. 18,000 years is examined to understand the long‐term history of this conservation challenge. Location Boomplaas Cave (BPA), South Africa. Methods The fossil sequence from BPA is examined to reconstruct ungulate community dynamics in relation to climate and vegetation change over the last 18,000 years. Results Ungulates from 18,000 to 12,000 years ago suggest an expansion of open grasslands that supported a grazing ecosystem dominated by an extinct caprine antelope and equid remains attributed to E. zebra and E. quagga. At the onset of the Holocene, the grazing ungulate community disappears and small browsers and mixed feeders dominate the assemblage, indicating the loss of open grassland vegetation. Several open‐habitat grazers go extinct at this time, and Equus persists at much lower abundances. This shift can be explained by global climate change across the Pleistocene–Holocene transition. Main conclusions The fossil sequence supports contemporary observations indicating that access to open grassland is crucial to maintaining large Cape mountain zebra subpopulations. Although fynbos is abundant throughout the historic range of the Cape mountain zebra, fossil evidence suggests that such vegetation is unlikely to support dense populations. It has been suggested that the acquisition of agricultural lands that were historically converted to open grasslands for livestock could promote Cape mountain zebra population growth. Results presented here support this management option, as the open grasslands in these converted landscapes likely approximate the vegetation structure during latest Pleistocene, when grasslands were widespread and grazing ungulates abundant.     

Treatment of equine sarcoid in seven Cape mountain zebra (Equus zebra zebra)

Equine sarcoid has been diagnosed in endangered Cape mountain zebra (Equus zebra zebra) in at least two game reserves in South Africa, with prevalence as high as 53% in Bontebok National Park. Seven Cape mountain zebras with sarcoids were treated with either surgical excision, 5-fluorouracil, allogenous vaccine, or a combination of 5-fluorouracil and allogenous vaccine. One of the two sarcoids on one of the 5-fluorouracil-treated zebras was left untreated. The microscopic features of the tumors evaluated showed either all or most of the typical epidermal and dermal histologic features of equine sarcoid. The zebras were examined 2 yr posttreatment to determine outcome. All sarcoids had resolved except on the zebra on which one of the sarcoids was left untreated. The efficacy of the three treatment methods in Cape mountain zebra is encouraging.     

Cape mountain zebra in the Baviaanskloof Nature Reserve,South Africa: resource use reveals limitations to zebra performance in a dystrophic mountainous ecosystem

Resource use of Cape mountain zebra was studied in the Baviaanskloof Nature Reserve (BNR) over concerns of the poor performance in population growth. We assessed the seasonal diet, habitat suitability and forage quality of the Bergplaas area in BNR for mountain zebra. Grasses contributed 95.2% to the annual diet of mountain zebra, Tristachya leucothrix contributing the most (39.4%), followed by Themeda triandra (27.6%). Seasonally, T. triandra contributed most to the diet in winter, while T. leucothrix became more important in the summer and also was the only species preferred in all seasons. Mountain zebra concentrated their feeding in Kouga Grassy Fynbos and from our assessment this was the only habitat suitable for mountain zebra. Our analysis of mountain zebra dung indicated that the seasonal nitrogen and phosphorus content was below the threshold values prescribed for grazers, and our study suggests that mountain zebra at Bergplaas are severely resource limited. We emphasize the importance of fire and access to nutrient‐rich lowlands in influencing the nutritional ecology of mountain zebra and provide conservation management recommendations.     

Reproductive characteristics of a free-ranging population of Cape mountain zebra (Equus zebra zebra)

In a population of free-ranging Cape mountain zebra, median age at first foaling was 67 months (range 38-105 months), median foaling interval was 25 months (range 13-69 months) and annual foaling rate was 32%. Foaling rates of younger and older mares were similar. Foals were born all year round with a peak corresponding to the rainy season (summer). Conception occurred later in the season when the spring was dry.     

Testis size and onset of spermatogenesis in Cape mountain zebras (Equus zebra zebra)

Testis mass of adult Cape mountain zebra stallions (mean 70.0 g) was appreciably less than that of other zebra species and domestic horses. The histological appearance of the testes of 11-, 24- and 29-month-old colts was typically prepubertal. Spermatogenic activity of a 4-year-old stallion obtained at the end of summer was at a very low level, while a 4.5-year-old stallion obtained 6 weeks after the winter solstice showed a marked increase in spermatogenesis compared with the 4-year-old. Stallions 6.5-19 years of age collected in different seasons all showed active spermatogenesis.     

Population structuring in mountain zebras (<Emphasis Type="Italic">Equus zebra</Emphasis>): The molecular consequences of divergent demographic histories

The endangered mountain zebra (Equus zebra) is endemic to the semi-arid inhospitable mountainous escarpments of southern Africa. The species is divided taxonomically into two geographically separated subspecies, each with differing recent population histories. In Namibia, Hartmann’s mountain zebra (E. z. hartmannae) is common and occurs in large free-ranging populations, whereas in South Africa, prolonged hunting and habitat destruction over the last 300 years has decimated populations of the Cape mountain zebra (E. z. zebra). In this study, we investigate the consequences of these divergent demographic histories for population genetic diversity and structure. We also examine the phylogeographic relationship between the two taxonomic groups. Genetic information was obtained at 15 microsatellite loci for 291 individuals from a total of 10 populations as well as 445 bp of the mitochondrial control region sequence data from 77 individuals. Both model-based and standard analytical approaches were used to examine the data. Both types of marker returned levels of diversity and structure that were consistent with population history. Low genetic variation within individual Cape mountain zebra populations, the characteristic indicator of population fragmentation and drift, was offset by moderate variation in the entire E. z. zebra sample. This implies that higher levels of diversity still exist within the Cape mountain zebra gene pool. A management strategy that entailed the mixing of aboriginal populations is therefore advocated in order to halt the further loss of Cape mountain zebra genetic diversity. Allele frequencies in Hartmann’s mountain zebra were relatively resilient to demographic fluctuations. Due to the high incidence of mitochondrial haplotype sharing between populations, the hypothesis that Cape and Hartmann’s mountain zebra mitochondrial lineages were reciprocally monophyletic was not supported. However, the presence of private alleles at nuclear loci rendered the two subspecies genetically distinct evolutionary significant units.     

The ecology of motherhood: the structuring of lactation costs by chacma baboons

1. Data from a long-term study of Papio hamadryas ursinus (L.) in the De Hoop Nature Reserve, Western Cape, South Africa, were used to test the assumptions and predictions of Altmann's model of maternal time budgets. 2. Female baboons' feeding time was below model predictions, and there was no evidence for a consistent increase in feeding time with infant age. In addition, female feeding time was not significantly higher than observed baseline feeding times for nonlactating females. 3. Female baboons reduced activity levels in the first few months post-partum, as reflected in significant increases in resting time, and there was some indication that females lost body mass over the course of lactation. When feeding demand was high, females sacrificed social time, and conserved resting time. 4. Females increased vigilance levels during the first 4 months of infant life and were more vigilant overall during lactation than when nonlactating. There was a negative relationship between feeding time and vigilance, but a positive relationship between resting time and vigilance. 5. Female baboons at De Hoop appear to cope with the energetic costs of lactation by reducing activity levels, although this cannot compensate completely for increased energetic costs. This may not be so much an'energy-sparing' strategy as a response to threats presented by infanticidal males in this population. Females therefore trade-off feeding time against vigilance.     

Reproductive deficits in male freshwater turtle Chrysemys picta from Cape Cod, Massachusetts

Contaminated groundwater plumes have formed on the Massachusetts Military Reservation (MMR), a Superfund site on Cape Cod, Massachusetts, as a result of chemical waste disposal. The plumes are of concern to the local people who rely on groundwater as a drinking water source. We used the freshwater turtle as a sentinel species to monitor the reproductive effects of exposure and, by inference, the potential for impact on human health. Our observations of male Chrysemys picta field-trapped from Moody Pond (an impacted site) and Washburn Pond (a reference site) on Cape Cod extended and supported prior observations of reproductive deficits. Morphometric comparison of precloacal length (PCL), which is a sexually dimorphic trait in the turtle, showed that Moody Pond males had a significantly longer PCL than Washburn Pond males. Moody Pond turtles showed reduced testicular weight, which was associated with significantly smaller seminiferous tubule diameter. Epididymal sperm counts were also markedly reduced in Moody Pond animals compared to Washburn Pond animals. Testicular histology and gonial proliferation, as determined by PCNA, were similar in both male populations, while the Moody Pond males had significantly higher germ cell apoptosis than the animals in Washburn Pond. These results suggest that a low-level mixture of xenobiotic contaminants impairs the reproductive functions of turtles exposed to the impacted site but not to the reference site environment.     

The decline and rise of the Kransberg Cape Vulture colony over 35 years has implications for composite population indices and survey frequency

Long-term monitoring is key for detecting population declines. Composite indices allow researchers to combine trends from disparate monitoring programmes into a single estimate of population change. Inferences from composite indices, however, are limited to the time periods and areas studied. We show that the number of breeding pairs in a colony of Cape Vultures Gyps coprotheres in South Africa declined between the years 1983 and 2003 but increased in both the number of breeding pairs and fledglings per pair from 2004 to 2017. We performed a retrospective power analysis determining the minimum annual frequency with which the colony could have been monitored without sacrificing inference into population trends. This power analysis revealed the post-2003 population increase would not have been apparent if we skipped more than 2 years between surveys. We incorporated our estimates into a previously published composite index for Cape Vultures that considered only data collected pre-2000 and demonstrate that the inference is unchanged if the trend from the decline period or the entire study is incorporated, yet if only the trend during the period of population increase is used, there is no longer a statistically significant decline across the species’ range. Our results demonstrate the utility of long-term monitoring because if our study had concluded before 2003, there would be little evidence of the current population increase at Kransberg.     

Global climate patterns explain range-wide synchronicity in survival of a migratory seabird

To predict the impact of climate change over the whole species distribution range, comparison of adult survival variations over large spatial scale is of primary concern for long-lived species populations that are particularly susceptible to decline if adult survival is reduced. In this study, we estimated and compared adult survival rates between 1989 and 1997 of six populations of Cory's shearwater ( Calonectris diomedea ) spread across 4600 km using capture–recapture models. We showed that mean annual adult survival rates are different among populations along a longitudinal gradient and between sexes. Variation in adult survival is synchronized among populations, with three distinct groups: (1) both females and males of Corsica, Tremiti, and Selvagem (annual survival range 0.88–0.96); (2) both females and males of Frioul and females from Crete (0.82–0.92); and (3) both females and males of Malta and males from Crete (0.74–0.88). The total variation accounted for by the common pattern of variation is on average 71%, suggesting strong environmental forcing. At least 61% of the variation in survival is explained by the Southern Oscillation Index fluctuations. We suggested that Atlantic hurricanes and storms during La Niña years may increase adult mortality for Cory's shearwater during winter months. For long-lived seabird species, variation in adult survival is buffered against environmental variability, although extreme climate conditions such as storms significantly affect adult survival. The effect of climate at large spatial scales on adult survival during the nonbreeding period may lead to synchronization of variation in adult survival over the species' range and has large effects on the meta-population trends. One can thus worry about the future of such long-lived seabirds species under the predictions of higher frequency of extreme large-scale climatic events.     

Strategic egg allocation in the zebra fish, Danio rerio

Females across a range of taxa have been shown to differentiallyallocate their reproductive resources according to the attractivenessof their mate. Previous studies demonstrated a female preferencefor larger males in the zebra fish but have so far failed touncover a size-mediated difference in male mating success, possiblydue to the effects of male–male competition. By controllingfor male–male competition in the present study, we showthat females strategically allocate their reproductive resources(i.e., eggs) toward larger males. When females were mated sequentiallywith a large and small male, they released a greater numberof eggs to the second male when he was large than when he wassmall. Furthermore, there was also a trend for females to releasea greater proportion of their eggs to the first male when hewas large. Across females, the total number of eggs laid byeach female increased with the average standard length of themale pair, whereas the number of eggs laid to the second malealso increased with his standard length. This study representsone of the first attempts at identifying differential allocationin a resource-free egg scatterer and suggests that female preferencesmay play a greater role in the reproductive success of malesin this species than previously envisaged.     

An eye for detail: selective sexual imprinting in zebra finches

To investigate the idea that sexual imprinting creates incipient reproductive isolation between phenotypically diverging populations, I performed experiments to determine whether colony-reared zebra finches would imprint on details of artificial white crests. In the first experiment, adults in one breeding colony wore white crests with a vertical black stripe, while in another colony adults wore crests having a horizontal black stripe; except for their crests, breeders possessed wild-type plumage and conformation. Offspring of both sexes reared in these colonies developed mate preferences for opposite-sexed birds wearing the crest type with which they were reared; neither sex developed a social preference for crested individuals of the same sex. In a second experiment, females reared by crested parents preferred crested males versus males with red leg bands, while control females (reared in a colony of wild-type, uncrested birds) preferred red-banded males in the same test. Results of a third experiment that used sexually dimorphic crest phenotypes indicate that both sexes of offspring imprinted on maternal crest patterns. Results support the hypothesis that sexual imprinting can facilitate isolation both by engendering a preference for population-typical traits and by prioritizing such an imprinting-based preference over species-typical preferences for other traits used in mate choice. Comparison with results of other recent studies indicates that imprinting tendencies of both sexes vary with the characteristics of traits presented as an imprinting stimuli. Tendency to imprint may vary with the perceived information content (e.g., kin, sex, or population indicator) of parental traits, a process dubbed selective sexual imprinting.     

Conservation implications of a long-term decline in body condition of the Brothers Island tuatara (Sphenodon guntheri)

Understanding the factors that drive the dynamics of remnant populations of long-lived species presents a unique challenge for conservation management. The long-lived Brothers Island tuatara Sphenodon guntheri is represented by one natural, self-sustaining population on 4-ha North Brother Island, New Zealand, and two small, translocated populations. The North Brother Island population was almost driven to extinction by extreme habitat modification and collecting in the late 19th century. Analysis of a long-term (1957–2001) dataset, following the population's recovery, reveals a significant decline in tuatara body condition over time, which is more pronounced in females. Declining body condition, coupled with very low reproductive output, may be symptomatic of a density-dependent response to elevated population size exacerbated by resource limitation. Sex-specific effects that disadvantage females could compromise this small population, particularly as it exhibits a male-biased sex ratio. We recommend removal of infrequently used structures and habitat restoration to alleviate intense resource competition. Population-level manipulation should be considered if future monitoring indicates an increasingly male-biased sex ratio and continued decline of female body condition.     

Reproductive ecology of Aloe plicatilis,a fynbos tree aloe endemic to the Cape Winelands,South Africa

While the pollination ecology of many Aloe species is well-documented, knowledge on aloe seed ecology, and hence aloe reproductive ecology in its entirety is limited. The aim of this study was to investigate the reproductive ecology of Aloe plicatilis, a Cape fynbos tree aloe endemic to the Cape Winelands, South Africa. Results from a pollinator exclusion experiment conducted at an A. plicatilis population on Paarl mountain suggests pollination primarily by insects, although bird visitation significantly increased seed set/fruit indicating possible co-pollination with insects. The species' long-tubed flowers and production of concentrated nectar, with observations of malachite sunbirds as the most common avian visitors to A. plicatilis flowers indicate the importance of long-billed specialist avian nectarivores as floral visitors. Analysis of the relationship between plant size and inflorescence production for five populations combined revealed a significant, positive linear relationship between plant size and the logarithm of the number of inflorescences/plant. Natural fruit and seed set determined for three populations (1325, 27,930 and 251,616 seeds/population) suggests low reproductive output compared to several other Aloe species. The smallest (31 individuals) and least dense (75 plants/ha) A. plicatilis population produced the lowest seed set/plant (128 seeds) and per population (1325 seeds), suggesting an Allee effect. Evaluation of seed dispersal potential showed that potential dispersal distances were approximately three times the canopy height; however, the occurrence of A. plicatilis on mountains isolated from more continuous mountain ranges on which the species also occurs suggests the possibility of long-distance dispersal by strong, gusty, summer winds. Soil seed bank samples collected from 13 populations yielded close to zero seedling emergence, indicating the absence of persistent seed banks. A. plicatilis seeds stored under ambient laboratory conditions for 3, 18 and 24 months were germinated in an environmental control chamber and a laboratory. High percentage germination was recorded for 18- and 24-month-seed (86 and 80%, respectively), while germination of 3-month-old seeds was three times lower, suggesting the need for after-ripening. Germination of fresh and one-year-old seed under ambient nursery conditions at the Karoo Desert National Botanical Garden in Worcester yielded emergence percentages of 67 and 44%, respectively, and were therefore less successful than germination under more controlled conditions. This is the first known study to investigate the reproductive ecology of a tree aloe species and that of a Cape fynbos aloe. The study highlights the importance of further studies on aloe seed ecology, particularly for rare and threatened species.     

Exploring patterns of population subdivision in the net-winged midge, Elporia barnardi (Diptera: Blephariceridae), in mountain streams of the south-western Cape, South Africa

1. The net-winged midges (Diptera: Blephariceridae) are a highly specialized group whose morphological characteristics and specific habitat requirements suggest a limited potential for dispersal. Levels of genetic variation were examined within streams, between streams in the same range and between mountain ranges in larval populations of Elporia barnardi in the south-western Cape of South Africa. The aim was to examine the hypothesis that population structure would reflect the poor potential for dispersal.
2. Significant deviations from Hardy–Weinberg equilibrium in 17 of the 57 individual comparisons indicate a non-random mating population. Given the swarming behaviour and life history traits, larvae sampled may reflect the product of limited matings.
3. Analysis of population substructuring revealed significant levels of differentiation among geographically proximate populations. Large differences between streams within Table Mountain, similar in magnitude to those between mountain ranges, suggest that movement of individuals out of the stream catchment is rare. Observed F _ST values are more similar to those of fully aquatic species than other lotic insects with winged adult stages.
4. Results suggest that mountain ridges provided effective physical barriers to the dispersal of E. barnardi , with the catchment representing the effective population unit.     

Social structure,vigilance and behaviour of plains zebra (<Emphasis Type="Italic">Equus burchellii</Emphasis>): a 5-year case study of individuals living on a managed wildlife reserve

Most studies of plains zebra (Equus burchellii) have focused on population ecology and have not included long-term observations of identified individuals. Over a 5-year period, we studied the crepuscular activities of 13 individual zebras within a focal group held within a managed game reserve. We also examined individual residency within the group by recording births, mortalities and longevity of group membership by adults. Residency of individuals living in other groups on the reserve was similarly monitored to examine variability in social structure within this closed population over an extended period of time. Stable, female groups were the mainstay of group sociality with male mean residency at 31.6 months being variable in length or even absent. Social interactions across all categories of zebras were free from aggression. Despite an absence of non-human predators, the proportion of dusk time budget allocated to vigilance was high, at 41% for males during periods when they accompanied stable female groups and 12% for females during these same periods. Female vigilance increased significantly to 19% when males were not resident. Females spent 70% of the time grazing and males just 36%. Due to its long-term nature, we concluded this study established a base line for plains zebra activity that could assist in understanding the factors that influence the successful management and conservation of healthy populations.     

Mitochondrial haplotype does not affect sperm velocity in the zebra finch Taeniopygia guttata

Mitochondrial DNA (mtDNA) variation has been suggested as a possible cause of variation in male fertility because sperm activity is tightly coupled to mitochondrial oxidative phosphorylation and ATP production, both of which are sensitive to mtDNA mutations. Since male‐specific phenotypes such as sperm have no fitness consequences for mitochondria due to maternal mitochondrial (and mtDNA) inheritance, mtDNA mutations that are deleterious in males but which have negligible or no fitness effect in females can persist in populations. How often such mutations arise and persist is virtually unknown. To test whether there were associations between mtDNA variation and sperm performance, we haplotyped 250 zebra finches Taeniopygia guttata from a large pedigreed‐population and measured sperm velocity using computer‐assisted sperm analysis. Using quantitative genetic ‘animal’ models, we found no effect of mtDNA haplotype on sperm velocity. Therefore, there is no evidence that in this system mitochondrial mutations have asymmetric fitness effects on males and females, leading to genetic variation in male fertility that is blind to natural selection.     

Incubation effort in relation to male attractiveness in zebra finches Taeniopygia guttata

The division of labour in parental care between the two sexes varies between and within species. In birds, parents have been shown to invest more into egg production and nestling care when paired with an attractive rather than an unattractive mate, as predicted by the differential allocation hypothesis. Here we investigate variation in the female's and male's share of incubation behaviour, a vital, and costly, period of parental care during which the embryo is vulnerable to perturbations in developmental conditions. We manipulated the attractiveness of male zebra finches Taeniopygia guttata , using red or green leg-rings. To simulate their natural social environment we allowed them to breed in outdoor aviaries. All males within an aviary were given the same coloured ring to avoid ring-colour related assortative mating. Males within a colony, however, were still expected to show some variation in attractiveness with the earliest laying females possibly pairing with the most attractive males. Indeed we found that both factors played a role in explaining female incubation effort. Among females mated to red ringed males, earlier laying females contributed significantly more to incubation than late laying females, but no such pattern was found in females mated to green ringed males. Overall, there were no differences in the level of incubation provided by both parents between treatment groups, suggesting some compensation within the pair. Hatching success was correlated with a pair's total incubation effort. These results suggest that variation in the division of parental care between the sexes is in agreement with both increased effort of females mated with attractive males, and females compensating for the reduced effort of attractive males seeking further mating opportunities. These two factors can act at the same time in natural populations and both should be considered when explaining variation in division of labour between the sexes.     

Population fluctuations, reproduction and survival in the Striped fieldmouse Rhabdomys pumilio on the Cape Flats, South Africa

A wild population of Striped fieldmice was studied for a continuous period of five years in an area of alien Acacio bush about 24 km from Cape Town, South Africa. Mice were live-trapped, marked by toe-clipping and released on a 60-station grid, and also kill-trapped in a separate area. Marked annual fluctuations in the population size were correlated with a 6–8 month summer breeding season. There were also marked inter-annual differences in peak population size. The age of sexual maturity of females was determined from the first pregnancy which occurred at 6–7 weeks old; and of males from the presence of visible spermatozoa in the vas deferens which occurred at about 11 weeks old. Litter size was affected by both the age and the body mass of the female. It appeared that mean survival from birth was only approximately 1.5 months and that survival from first capture was about 1.9–2.5 months. This high mortality appeared to be the major reason for the sharp seasonal fluctuations in population size and may also have been responsible for the interannual differences since marked changes in survival were recorded between some years.     

Sex-biased dispersal in a salmonid fish

We tested the hypothesis that dispersal is sex biased in an unexploited population of brook trout, Salvelinus fontinalis, on Cape Race, Newfoundland, Canada. Based on the assumptions that trout are promiscuous and that reproductive success is limited primarily by either number of mates (males) or fecundity (females), we predicted that males would disperse greater distances than females. We also tested the hypothesis that trout populations comprise stationary and mobile individuals, predicting that males have greater mobility than females. Based on a mark-recapture study of 943 individually tagged fishes, 191 of which were recaptured over 5 years, we find strong support for our hypothesis of male-biased dispersal in brook trout. Averaged among all 11 resampling periods, males dispersed 2.5 times as far as females; during the spawning period only, male dispersal exceeded that by females almost fourfold. Both sexes were heterogeneous with respect to movement, with a lower incidence of mobility among females (29.6%) than males (41.1%); mobile males dispersed six times further than mobile females. We conclude that this sex bias reduces mate competition among male kin and decreases the probability that males will reproduce with related females.