The historical development of zoo elephant survivorship.

In the discussion about zoo elephant husbandry, the report of Clubb et al. (2008, Science 322: 1649) that zoo elephants had a "compromised survivorship" compared to certain non-zoo populations is a grave argument, and was possibly one of the triggers of a large variety of investigations into zoo elephant welfare, and changes in zoo elephant management. A side observation of that report was that whereas survivorship in African elephants (Loxodonta africana) improved since 1960, this was not the case in Asian elephants (Elephas maximus). We used historical data (based on the Species360 database) to revisit this aspect, including recent developments since 2008. Assessing the North American and European populations from 1910 until today, there were significant improvements of adult (≥10 years) survivorship in both species. For the period from 1960 until today, survivorship improvement was significant for African elephants and close to a significant improvement in Asian elephants; Asian elephants generally had a higher survivorship than Africans. Juvenile (<10 years) survivorship did not change significantly since 1960 and was higher in African elephants, most likely due to the effect of elephant herpes virus on Asian elephants. Current zoo elephant survivorship is higher than some, and lower than some other non-zoo populations. We discuss that in our view, the shape of the survivorship curve, and its change over time, are more relevant than comparisons with specific populations. Zoo elephant survivorship should be monitored continuously, and the expectation of a continuous trend towards improvement should be met.

Diurnal variation of salivary cortisol in captive African elephants (Loxodonta africana) under routine management conditions and in relation to a translocation event.

The present study assessed the diurnal variation in salivary cortisol in captive African elephants during routine management (baseline) and in relation to a potential stressor (translocation) to evaluate to what extent acute stress may affect diurnal cortisol patterns. Under baseline conditions, we collected morning and afternoon saliva samples of 10 animals (three zoos) on different days in two study periods (n = 3-10 per animal, daytime and period). Under stress conditions, we sampled the transported cow (newcomer) and the two cows of the destination zoo before and after the transport in the morning and afternoon (n = 3-9 per animal, daytime and transport phase), as well as after the first introduction of the newcomer to the bull (n = 1 per animal). Cortisol was measured in unextracted samples by enzyme immunoassay. Under baseline conditions, we observed the expected diurnal variation with higher cortisol levels in the morning than in the afternoon. Under stress conditions, neither a significant difference between pre- and posttransport, nor between morning and afternoon levels was found. The percentage difference between morning and afternoon cortisol after the transport, however, was remarkably lower than before the transport in the newcomer potentially indicating a stress response to familiarization. Saliva samples taken immediately after the introduction of the newcomer to the bull revealed a marked cortisol increase. Our findings indicate that stressors may disturb the diurnal cortisol rhythm. Furthermore, provided that samples can be collected promptly, salivary cortisol is a useful minimally invasive measure of physiological stress in the African elephant.

Long-Term Olfactory Memory in African Elephants.

African elephants are capable of discriminating scents up to a single changed molecule and show the largest reported repertoire of olfactory receptor genes. Olfaction plays an important role in family bonding. However, to the best of our knowledge, no empirical data exist on their ability to remember familiar scents long-term. In an ethological experiment, two mother-daughter pairs were presented with feces of absent kin, absent non-kin, and present non-kin. Video recordings showed reactions of elephants recognizing kin after long-term separation but only minor reactions to non-kin. Results give the empirical implication that elephants have an olfactory memory longer than 1 year and up to 12 years and can distinguish between kin and non-kin just by scent. These findings confirm the significance of scent for family bonds in African elephants.

Differences in Mother-Infant Bond and Social Behavior of African Elephant Calves Living In Situ and Ex Situ.

African zoo elephants live in safe environments with sufficient resources, are protected from threats, and have their health and body conditions cared for. Calves ex situ undergo the same developmental stages as in situ and are raised by the whole family unit. However, due to environmental differences, there might be behavioral modifications between calves in situ and ex situ. We hypothesize that these differences increase with ongoing generations. This ethological study compares social and general behavior and the distance calves kept to their mothers' between calves of the first (F1) and second (F2) zoo generation and the wild. Using ethological methods, data were collected for ~90 in situ calves and 16 ex situ (8 F1, 8 F2) between the ages of 0.5 to 4 years (120 observation hours per group). Results showed that in situ calves spent significantly more time close to mothers than the F1 and the F2 zoo generations (F1/in situ: p = <0.001; F2/in situ: p = 0.007). The behaviors of eating, drinking, trunk movement, washing, and affiliative behaviors showed significant differences between in situ and ex situ calves. The amount and distribution of affiliative and agonistic behavior initiated and received by calves was displayed with a greater variety ex situ. Ex situ calves not only performed affiliative but, in contrast to the in situ, also agonistic behavior (F1/in situ: initiated p = 0.002, received p = 0.010; F2/in situ: initiated p = 0.050, received p = 0.037). The comparison of zoo generations suggests that differences did not increase with the generation. The more casual binding between mothers and offspring in zoos and the age-dependent improvement of social behavior of zoo-born calves are seen as a result of elephants' adaptation to secure zoo conditions. The results of this study agree with the faster development of ex situ African elephants, like earlier puberty and more frequent breeding patterns, as known from the literature.

Effects of Positive Reinforcement Training and Novel Object Exposure on Salivary Cortisol Levels under Consideration of Individual Variation in Captive African Elephants (Loxodonta africana).

Dealing with potential stress in species that have high husbandry requirements, such as elephants, is a challenge for zoos. The objective of the present study was to determine whether positive reinforcement training (PRT) and exposure to a novel object (NOV) for enrichment induced a salivary cortisol response indicative of activation of the hypothalamic-pituitary-adrenal (HPA) axis and which factors determine individual variation in this regard in captive African elephants. We repeatedly sampled the saliva of ten animals (three zoos) for the analysis of cortisol (SACort) before and up to 60 min (in 10-15 min intervals) after the onset of PRT (three repeats) or NOV (nine repeats), which lasted 10 min. There was considerable individual variation in SACort in response to PRT or NOV. Using mixed models, we were able to control these and to reveal that PRT was associated with high SACort before and relatively low SACort after PRT, while NOV induced a moderate SACort increase. The individual differences in SACort were related to age and sex (NOV), while the effects of zoo, handling method (free vs. protected contact) and reproductive and social status were variable. We conclude that positive affective states, such as anticipation or arousal, should be taken into account when interpreting the differences in the SACort responses between PRT and NOV. In addition, understanding the individuality of stress will support management decisions aimed at promoting captive elephant welfare.

Monitoring Behaviour in African Elephants during Introduction into a New Group: Differences between Related and Unrelated Animals.

The introduction of elephants into new groups is necessary for breeding programmes. However, behavioural studies on the reactions of these animals at first encounters are missing. In the present study, female African elephants (Loxodonta africana) living in zoos were observed during unifications with unfamiliar elephants (introduction of two to one females and one to two females; n = 6) and reunifications with related elephants (two mother-daughter-pairs; n = 4) that were separated for 2 and 12 years, respectively. First encounters of the elephants were observed and recorded by scan sampling. The parameters measured were (a) signs of the characteristic Greeting Ceremony, (b) distance to the fence separating the elephants during first contact, and (c) time until trunks touched for the first time. The data were statistically analysed with SPSS. The results showed that related elephants performed a full Greeting Ceremony on reunifications. Unrelated elephants only expressed a minor greeting. During first encounters, related elephants predominantly showed affiliative behaviour (p = 0.001), whilst unrelated elephants expressed more agonistic behaviour (p = 0.001). The distance to the fence was significantly smaller for related elephants than for unrelated elephants (p = 0.038). first contact of trunks occurred on average after 3.00 s. in related elephants and 1026.25 s. in unrelated elephants. These findings indicate that related elephants recognise their kin after up to 12 years of separation, meet them with a full Greeting Ceremony during reunification, and seek contact to the related elephant, while unrelated elephants are hesitant during unifications with unfamiliar elephants and express more agonistic behaviour. The results testify that zoo elephants show the same species-specific social behaviour as their conspecifics in the wild. It also confirms the cognitive abilities of elephants and the significance of matrilines for breeding programmes.

Prolonged luteal lifespan and pseudopregnancy in Asian elephants (Elephas maximus).

Pseudopregnancy is a physiological occurrence in mammals which have copulation induced ovulation, but is rarely described in spontaneous ovulating species. In this study, three cases of prolonged luteal lifespan are reported in non-pregnant Asian elephants (Elephas maximus). Case 1 was a 25-year-old female that had produced three calves previously; Case 2 was a nulliparous and 32-year-old at the start of the pseudopregnancy episode; and Case 3 occurred in a 49-year-old nulliparous elephant. Serum progesterone metabolite concentrations remained elevated for 10 months in Case 1. Urinary progestagens were high for >16 months in Case 2 and for five months in Case 3. In Case 1, multiple persistent corpora lutea were visualized monthly by ultrasonography. In all three cases, uterine leiomyoma were present and progestagen concentrations decreased spontaneously. In Case 1, the elephant became pregnant 3 years later, whilst with Case 2, the female resumed estrous cycling normally, and for the Case 3 female, there was continuation with another prolonged luteal phase before ovarian function was purposely suppressed. These examples indicate that persistently elevated progestagen concentrations may not always be indicative of pregnancy in elephants. The reasons for prolonged luteal lifespan are not understood, although serum prolactin concentrations quantified in the Case 1 female were elevated compared to values from previous reports and two other herd mates. Furthermore, all three elephants had varying degrees of uterine pathologies. It is believed that the resulting damage to the endometrium may have led to a reaction similar to implantation, which includes prolactin secretion. Prolactin may exert luteotropic properties and is thought to initiate luteal rescue during pregnancy in elephants.

Fetal and infant head circumference sexual dimorphism in primates.

Studies have shown that after controlling for the effects of body size on brain size, the brains of adult humans, rhesus monkeys, and chimpanzees differ in relative size, where males have a greater volume of cerebral tissue than females. We assess whether head circumference sexual dimorphism is present during early development by evaluating sex differences in relative head circumference in living fetuses and infants within the first year of life. Head circumference is used as a proxy for brain size in the fetus and infant. Femur length is used as a proxy for body length in the fetus. Ultrasonography was used to obtain fetal measures, and anthropometry was used to obtain postnatal measures in humans, rhesus monkeys, baboons, and common marmosets. We show that statistically significant but low levels of head circumference sexual dimorphism are present in humans, rhesus monkeys, and baboons in early life. On average, males have head circumferences about 2% larger than females of comparable femur/body length in humans, rhesus monkeys, and baboons. No evidence for head circumference sexual dimorphism in the common marmoset was found. Dimorphism was present across all body size ranges. We suggest that head circumference sexual dimorphism emerges largely postnatally and increases throughout maturation, particularly in humans who reach adult dimorphism values greater than the monkeys. We suggest that brain dimorphism is not likely to impose an additional energetic burden to the gestating or lactating mother. Finally, some of the problems with ascribing functional significance to brain size sexual dimorphism are discussed, and the energetic implications for brain size sexual dimorphism in infancy are assessed.