Mother-infant interactions in slow lorises (Nycticebus bengalensis) and pygmy lorises (Nycticebus pygmaeus)

The study had three purposes: (1) to obtain information about mother-infant interactions in a rarely studied nocturnal prosimian, the pygmy loris (Nycticebus pygmaeus); (2) to compare pygmy lorises with a closely related and better-studied nocturnal prosimian, the Bengal slow loris (Nycticebus bengalensis); and (3) to determine how the presence of a second offspring affected mother-infant interactions in pygmy lorises. Three Bengal slow loris mothers and 3 pygmy loris mothers served as subjects, along with their 10 offspring (4 Bengal slow loris singletons, 2 pygmy loris singletons and 2 sets of pygmy loris twins). Observations were carried out in a zoo research facility for the first 24 weeks of the infants' lives. Although the two species differ in size and reproductive patterns, mother-infant interactions were similar. The primary modes of infant and adult contact were ventral and passive contact, respectively. Mothers parked their infants from the first week, and infants followed from the second week. Mothers displayed little protection or rejection, and there was little aggression. Infants solicited play and social grooming from their mothers. Pygmy loris mothers engaged in social grooming and play with their infants more frequently and for longer periods if the infant was a singleton rather than a twin.     

Energy metabolism and thermoregulation in pygmy lorises (Nycticebus pygmaeus) from Yunnan Daweishan Nature Reserve

The pygmy loris (Nycticebus pygmaeus) is a small prosimian living in Vietnam, Laos, eastern Cambodia and the south part of China. In China it is only found in Pingbian, Hekou, Jinping, Luchun of Yunnan. As N. pygmaeus is seriously threatened by hunting, trade and habitat destruction, it is listed in Appendix II of CITES, and in 2006 the IUCN classified it as “vulnerable”. In order to understand the characteristics of energy metabolism and thermoregulation of N. pygmaeus, the resting metabolic rate (RMR) and body temperature (T_b) at different ambient temperature (T_a) of pygmy lorises, as well as body mass, energy intake, digestable energy intake, digestability and the thermal conductance were measured in captivity. The results obtained mainly are as follows: (1) Pygmy loris feed dry food averaged 12.90 ± 1.02 g/d. They could gain 214.87 ± 16.65 kJ/d from food intake, and earned 200.15 ± 16.36 kJ digestable energy intake per day with 90.13 ± 1.34% of the digestability. (2) The T_b at room temperatures was a little low (35.23 ± 0.16 °C) and varied with T_a from 25 °C to 35 °C. There was a positive relationship between T_b and T_a, which was described as: T_b = 27.22 + 0.34T_a (r = 0.880). (3) The resting metabolic rate (RMR) of the pygmy loris was 0.3844 ± 0.0162 mlO₂/g/h, which was 51.91 ± 1.90% of the previous predicted rate by Kleiber (1961) [21]. (4) The average thermal conductance of the pygmy loris (N. pygmaeus) was 0.0449 ± 0.0031 mlO₂/g/h/°C. These characteristics of energy metabolism and thermoregulation of N. pygmaeus in Yunnan Daweishan Nature Reserve might be considered as the adaptive characteristics to their environment in tropical semi-evergreen forests and secondary forests.     

Reproductive parameters of clouded leopards (Neofelis nebulosa)

Reproductive data compiled from the International Clouded Leopard Studbook revealed that 75% of all litters were born to females between one and five years of age. Sixty-three percent of the males had sired litters by four years of age with reproduction declining after six years of age. Sixteen zoological institutions surveyed worldwide contributed estrous cycle data from 28 clouded leopards. Sexual maturity (age at first estrus) for these females ranged from 17 to 28 months of age with a mean estrous cycle length of 29.9 ± 13.8 days. The mean length of estrus was six days. Gestation length ranged from 85 to 121 days (X? = 93.4 ± 6.3). There was a significantly higher incidence of estrus in fall and winter compared with spring and summer over latitudes ranging from 36°–45° and 51°–55° (P < .005). Mating occurred in all months except June and October, and cubs were produced in all months except December. The highest frequency of mating occurred during the month of December corresponding with a birth peak in March.     

Signaling of Reproductive Status in Captive Female Golden-Headed Lion Tamarins (Leontopithecus chrysomelas)

In species in which paternal care has an important impact on the offspring's fitness, concealment of reproductive status has been proposed as a strategy employed by females to prevent males from practicing desertion and polygamy, which would then lead to monogamous or polyandrous mating systems or both. We investigated whether the female's reproductive status is being concealed in golden-headed lion tamarins, which exhibit extensive paternal care and a mainly monogamous/polyandrous mating system. We used a combination of behavioral observations and endocrine data to determine female reproductive status and to examine changes in sociosexual behaviors over the ovarian cycle and between conceptive and nonconceptive cycles. Females clearly signaled their reproductive status by way of proceptive sexual presenting. Males showed increased frequencies of anogenital sniffing and mounting during the fertile period, indicating that they detected changes in olfactory and behavioral cues emitted by females, and they adjusted their mounting behavior accordingly. Males and females also remained in closer proximity before and during the fertile period, which suggests the existence of mate guarding. We discuss a possible function of behavioral advertisement of reproductive status in shaping the mating system in Leontopithecus chrysomelas.     

Non-invasive detection and monitoring of estrus,pregnancy and the postpartum period in pygmy loris (Nycticebus pygmaeus) using fecal estrogen metabolites

Estrone-conjugates (E₁C) were measured in the feces of six female pygmy lorises (Nycticebus pygmaeus) during estrus (n = 12), pregnancy (n = 4) and the postpartum period (n = 3). Noninvasive feces collection permitted frequent sampling throughout estrus and pregnancy, without disturbance of animals. The estrous period was defined as an increase in fecal E₁C levels above an average of 70 ng/g feces with peaks above 100 ng/g feces obtained in consecutive fecal samples collected over a 6- to 11-day period between the end of July and the first third of October. Comparison of the periovulatory profile of E₁C and the stage of labial opening of the vagina revealed a high agreement (P < 0.001). In all pregnant females, an E₁C rise was found approximately 47 days postestrus, the source of which may be the growing fetal placental unit. Estimated gestation lengths ranged between 187 and 198 days (n = 4). Am. J. Primatol. 41:103–115, 1997. © 1997 Wiley-Liss, Inc.     

Mother-infant interactions in captive slow lorises (Nycticebus coucang)

Information is presented about mother-infant interactions and infant development in a rarely studied prosimian primate, the slow loris (Nycticebus coucang). Four dyads were observed, by means of closed circuit TV, in a semi-natural environment for 1 hour per day three times a week. Infants were inactive for the first 6–8 weeks. Although mothers carried infants, they also left them alone for substantial periods of time after the 1st week. Over the 20-week study period, there was a significant decline in ventral contact but not in sitting within 12 inches or engaging in active social interactions. By the end of the study, infants were not yet fully independent. Three of the 4 were primarily responsible for maintaining physical closeness to the mother; they made most of the approaches and mothers made most of the departures. However, only 2 of the 4 infants had assumed responsibility for the initiation and maintenance of social interactions with the mother. By comparison with other nocturnal prosimians of similar size, the rate of development is relatively slow. Unlike many anthropoids, mothers were not strongly protective or rejecting. They did not bring infants back to a fixed location or try to prevent infants from leaving them; and the decline in ventral contact was not accompanied by fights between the pair. The 3 group-living mothers were more protective than the single individually housed mother, and it would seem advisable to isolate mother-infant pairs in laboratory breeding colonies.     

Behavioral indices of estrus in a group of captive African elephants (Loxodonta africana)

This study investigated behavioral signals of estrus by systematically monitoring the interactions of one male with four female African elephants housed in a naturalistic outdoor enclosure at Disney's Animal Kingdom over a period of 11 months. We measured changes in five spatial behaviors and 22 tactile‐contact behaviors, as well as changes in serum progestagen and LH concentrations, across three ovarian cycles for each female. Two females did not cycle during the study. Three different phases of the ovarian cycle were identified: mid luteal, anovulatory follicular, ovulatory follicular. The male followed more and carried out more genital inspections, flehmen, and trunk‐to‐mouth behaviors toward cycling females during their ovulatory phase. Genital inspections by the male peaked above baseline levels on the day of an LH surge, and up to 9 days before, in both cycling females and, thus, might be a useful behavioral index of estrus. The male also carried out more genital inspections, flehmen, and trunk touches to the back leg toward ovulatory cycling than noncycling females. Overall, our results indicated that: 1) a single subadult African elephant male could discriminate two females in the ovulatory phase of their cycle (i.e., during the 3 weeks preceding ovulation) from the mid luteal phase; 2) the male also discriminated two cycling females in the ovulatory and anovulatory follicular phases from two noncycling females; 3) two females in the ovulatory phase of the cycle displayed a greater variety of tactile‐contact behavior toward the male compared to the other cycle phases. Zoo Biol 0:1–19, 2005. © 2005 Wiley‐Liss, Inc.     

Reproductive biology of Bagrus docmak in the Victoria Nile,Uganda

Aspects of the reproductive biology of Bagrus docmak in the Victoria Nile were investigated between November 2005 and October 2006. Macroscopic and histological analysis of the gonads confirmed it as an asynchronous batch spawner which spawns throughout the year with bimodal spawning peaks coinciding with rainfall seasons. The first spawning peak occurred from March to May, the second from September to November. The sex ratio did not significantly deviate from 1:1. Length at sexual maturity was 33.6 cm and 31.6 cm fork length (FL) for females and males, respectively. Batch fecundity ranged from 1 000 eggs in 34 cm FL fish to 43 000 eggs in 79 cm FL fish, and correlated linearly with FL (r = 0.72) and body weight (r = 0.79). Mean relative batch fecundity was 6 eggs g^?1 (SE 2). These results could guide research into the possibility of artificially inducing the fish to spawn, and its subsequent culture.     

Reproductive biology of captive Arabian oryx (Oryx leucoryx) in Saudi Arabia

Reproductive data on captive Arabian oryx (Oryx leucoryx) were collected from June 1986 through April 1992 at the National Wildlife Research Center (Taif, Saudi Arabia). Oryx females are polyestrous. The estrous cycle averaged 22 days and mean gestation length was 260 ± 5.5 days (S.D). Sex ratio at birth was unbiased and mean weight was 6.5 ± 0.7 kg (S.D.), with no difference between sexes. Under captive breeding conditions, births occurred throughout the year. Females gave birth to a single calf at any time during the day and produced 1.03 young per year. Abortion rate was 3.6%. Mortality rate of young was 6.1% before weaning at 3 months of age. The interbirth interval averaged 295 ± 42 days (S.D.), with 53% lasting between 270 and 279 days. Females reached sexual maturity at the age of 13 months. © 1996 Wiley-Liss, Inc.     

Cranial allometry and geographic variation in slow lorises (Nycticebus)

A series of 20 craniodental measurements was obtained for two sister taxa: Nycticebus coucang (common slow loris) and N. pygmaeus (pygmy slow loris). Multivariate analysis of variance was performed with adult data to describe patterns of subspecific and specific variation in this genus. The geometric mean of adult cranial dimensions was compared to field data on latitudinal coordinates for available specimens to investigate if size variation in Nycticebus is clinal in nature. Ontogenetic series for larger-bodied N. coucang and smaller-bodied N. pygmaeus were compared to test the hypothesis that species and subspecific variation in skull form results from the differential extension of common patterns of relative growth. A MANOVA provides independent support of Groves's [pp. 44–53 in Proceedings of the Third International Congress on Primatology, Vol. 1 (Basel: S. Karger), 1971] classification of Nycticebus into two species, with four subspecies in the common slow loris and one form of the pygmy slow loris. Within N. coucang, cranial proportions for all four subspecies are ontogenetically scaled, and size differentiation is mainly clinal (Bergmann's Rule). N. c. bengalensis represents the most northerly disposed and the largest form. N. c. javanicus represents the next-largest form and is located in a southerly direction the next-farthest away from the equator. N. c. coucang and N. c. menagensis are both equatorial; however, the latter subspecies is the smallest. A genetic basis for some of the taxonomic variation between N. c. coucang and N. c. menagensis is supported by such nonclinal variation in body size. Variation in the presence/absence of I² is not size-related but rather tracks geographic proximity and isolating factors which predate the most recent inundation of the Sunda Shelf. Although they inhabit a nonequatorial environment, pygmy slow lorises are the smallest of all Nycticebus. As N. pygmaeus is sympatric with N. c. bengalensis, the largest slow loris, it appears that the evolution of its smaller body size represents a case of character displacement. Unlike N. coucang, skull size becomes significantly smaller in more northern N. pygmaeus. This may also reflect character displacement between sympatric sister taxa underlain by a cline-dependent ecological factor which is marked in more northerly latitudes. On the other hand, the negative correlation between body size and latitude in N. pygmaeus could be due to the influence of nonprimate fauna, such as predators, which themselves evince a similar clinal pattern. Analyses of relative growth indicate that skull proportions in the two species of Nycticebus are ontogenetically scaled in two-thirds of the cases. All but one of the seven comparisons (interorbital breadth) which do not indicate ontogenetic scaling represent part of the masticatory complex. This likely reflects a reorganization of N. pygmaeus maxillomandibular proportions linked to smaller size and changes in diet. Am. J. Primatol. 45:225–243, 1998. © 1998 Wiley-Liss, Inc.     

Patterns of testosterone in male white‐tailed deer (Odocoileus virginianus): Seasonal and lifetime variation

Testosterone is strongly associated with the annual development of antlers in cervids, but endocrine research on wild, freely breeding ungulates is often done without repeated capture of known‐aged individuals. As a result, our knowledge on how testosterone fluctuates over the course of a lifetime and variation in lifetime patterns among individuals is limited. We investigated patterns of testosterone in a freely breeding population of white‐tailed deer (Odocoileus virginianus) in Alabama, USA, that breeds in January. Testosterone peaked during the height of the breeding season, despite this period occurring approximately 2 months later than in most temperate‐region white‐tailed deer populations. Age‐related differences in testosterone were only prevalent during the breeding season, with bucks ≥3.5 years old having greater testosterone (853 ng/dl ± 96 SE; p = 0.012) than bucks 1.5–2.5 years old (364 ng/dl ± 100 SE). Additionally, an individual''s testosterone level as a yearling was not positively associated with their lifetime maximum testosterone level (p = 0.583), and an individual''s mean testosterone level was positively associated with lifetime testosterone variation (p < 0.001). To our knowledge, our study is one of the first to assess how testosterone early in life might relate to individual testosterone later in life. We believe these data provide insight into lifetime hormonal patterns in cervids, and that these patterns may indicate intraspecific variation of lifetime reproductive strategies.     

Reproductive biology of the greeneye spurdog Squalus chloroculus (Squaliformes,Squalidae)

The reproduction of the greeneye spurdog Squalus chloroculus was studied based on animals caught in the multispecies and multi‐gear southern and eastern scalefish and shark fishery on the upper continental slope off southern Australia. One hundred and ninety‐nine females (502–990 mm, total length, L_T) and 189 males (515–810 mm L_T) were examined. The female reproductive cycle, based on 41 breeding animals, is continuous and triennial, with the pregnancy period estimated to be 31–34 months, seasonal and synchronous with the ovarian cycle; a third of the breeding female population is estimated to give birth between September and December each year. The estimated L_T at which 50% of females are mature is 799 mm (95% c.i. : 794, 804), whereas the L_T at which 50% are maternal is 825 mm (95% c.i. : 817–833), but these estimates are probably biased by the phenomenon of apparent change of L_T at maternity and L_T at maturity following severe length‐selective fishing mortality. Litters ranged from four to 15 embryos with a 1:1 sex ratio, and litter size increased with maternal length. The breeding cycle of males is neither seasonal nor synchronous with the female cycle. The estimated L_T of males where 50% are mature was 629 mm (95% c.i. : 603, 645).     

Reproductive seasonality and maturity of male Neophocaena phocaenoides asiaeorientalis in captivity: A case study based on the hormone evidence

To provide hormone evidence on reproductive seasonality and maturity of the Yangtze finless porpoise, the authors monitored the monthly variations of serum reproductive hormones of a male Yangtze finless porpoise in captivity via radioimmunoassay from 1997 to 2003. It was demonstrated that the immature animal had a serum T level of 28-101 ng dL^-1 (65 ± 52 ng dL^-1), reached puberty with the serum T concentration ranging between 250 and 590 ng dL^-1 (390 ± 130 ng dL^-1), and attained reproductive maturity when the serum T level went beyond 1120 ± 180 ng dL^-1 in the breeding season. The body length growth of the animal showed a pattern similar to the serum T variations during its adolescent period from the age of 4 to 6 years. Moreover, the serum T concentration of the male porpoise exhibited significant seasonal variations, indicating that its breeding season may start as early as March and end as late as September.     

Behavioral correlates of physiological estrus in cheetahs

Historically, the cheetah (Acinonyx jubatus) has been known for its poor reproductive performance in captivity. Although breeding success has improved over the past decade, the percentage of breeders in the captive population is still low and successful propagation unpredictable. Estrus in this species has been reported as “silent” by some, therefore contributing to breeding problems by making appropriate timing of pair introductions difficult. To investigate whether any observable behavioral changes may be associated with estrus, we carried out quantitative behavioral observations and concomitant noninvasive monitoring of estradiol metabolites excreted in feces of 14 captive female cheetahs for periods of 5–22 consecutive weeks. We found that changes in fecal estradiol concentrations correlated significantly with variation in the occurrence of several types of behaviors, including rolling, rubbing, sniffing, vocalizing, and urine spraying. However, the number and types of correlated behaviors varied across females, revealing no single behavior indicative of estrus, but rather a constellation of behaviors that increased in frequency when estradiol concentrations were elevated. There was no significant difference in the overall average estradiol concentrations or peak values of the females that had previously mated and conceived compared to those of the females that had failed to breed. Successful breeders appeared to show significantly higher rates of rubbing and rolling than nonbreeders. However, rates of rubbing, rolling, and urine spraying also were found to increase with age, and older individuals were more likely to have bred. The results of this study indicate that estrus in the cheetah cannot be regarded as “silent” since the frequencies of some behaviors appear to covary with fluctuating estradiol levels. However, behavioral monitoring of estrus may nevertheless be difficult and time-consuming due to individual variation and subtle changes in behavioral frequencies rather than changes in the types of behaviors displayed. Zoo Biol 17:193–209, 1998. © 1998 Wiley-Liss, Inc.     

Reproductive biology of the rock shrimp Sicyonia dorsalis (Decapoda: Penaeoidea) from the southeastern coast of Brazil

Summary

Sicyonia dorsalis is not commercially exploited in Brazil, but it forms a critical link in marine food chains by converting detritus food sources into microorganism biomass that is available for higher trophic levels. We examined the reproductive biology of this species, sampled for five and a half years in a tropical locality, the southeastern coast of São Paulo (23° S), Brazil. Monthly samples were taken from January 1998 to June 2003 at depths of 5 to 45 m. Degree of ovarian development was used to examine breeding in adult females. Recruitment was estimated by changes in proportion of individuals in juvenile size classes of carapace length (CL #8.2 mm) in relationship to the total number of individuals. The largest immature female measured 9.2 mm CL, but 75% of females were smaller than 7.3 mm CL. The largest immature male measured 6.8 mm CL. The relative frequency of reproductive females was negatively correlated with the relative frequency of recruitment (p <0.001). Reproductive females were found in every season, with peaks in December-February following the recruitment peak in March-June, and a second peak of spawning in May-July and of recruitment in September-November. The continuous reproductive pattern observed for S. dorsalis, combined with the hypothesis that during spring and summer the phytoplankton production is higher, when the South Atlantic central water mass intrudes into the region during upwelling events, suggests that food availability for protozoeal and mysis larvae may be an important selective factor shaping the seasonal breeding pattern for S. dorsalis. The classical paradigm of continuous reproduction at lower latitudes, with increased seasonality of the breeding period at higher latitudes, seems to be valid for this species.     

Reproduction in free-ranging male Propithecus verreauxi: The hormonal correlates of mating and aggression

Endocrine studies of captive strepsirrhine primates suggest that physical environment and social factors mediate inter-individual variations in testicular function and serum testosterone (sT) in males. While these studies have made major contributions to our understanding of the individual proximate mechanisms influencing androgen activity in male strepsirrhines, none have investigated how these mechanisms work coincidentally in free-ranging populations. In this study we used fecal steroid analysis to examine androgen-behavior interactions associated with reproduction in free-ranging male Propithecus verreauxi. Behavioral and hormone data were collected from two social groups during the 1990–91 and 1991–92 breeding seasons at Beza Mahafaly, Madagascar. Solid phase and radioimmunoassay techniques were used to quantify testosterone (T) in 105 desiccated fecal samples collected weekly from seven males. Results suggest that 1) solid phase extraction and radioimmunoassay techniques were reliable and accurate methods for quantifying T in sifaka feces; 2) fecal T (fT) elevations spanned a minimum of 4 months, peak levels occurring 1 month prior to the January onset of the breeding season; 3) fecal T concentrations were influenced by developmental factors and, among mature males, social factors associated with rank, intergroup aggression, and group instability. Am J Phys Anthropol 105:137–151, 1998. © 1998 Wiley-Liss, Inc.