The effect of melatonin on the seasonal embryonic diapause of the Bennett's wallaby (Macropus rufogriseus rufogriseus)

In seasonally breeding mammals, the hormone melatonin, produced at night by the pineal gland, is known to be important in transducing the effect of photoperiod in timing reproduction. In the Bennett's wallaby, an unimplanted unilaminar blastocyst is held in a state of seasonal diapause from mid-winter to mid-summer. Here we show that an implant of the hormone melatonin rapidly terminates seasonal diapause in this species. Blastocyst reactivation is not accompanied by a significant reduction in levels of the hormone prolactin, thereby refuting earlier suggestions that this hormone is responsible for maintaining seasonal embryonic diapause.     

The reproductive biology of Bennett's wallaby (Macropus rufogriseus rufogriseus) ranging free at Whipsnade Park

Between August 1981 and October 1982, 76 female and 50 male of the estimated 400 Bennett's wallabies at Whipsnade were caught and examined. Sixty-four of the adult females inspected (84%) were carrying pouch young. A small captive breeding colony was established in the laboratory. Weight and growth curves were established for captive born pouch young and these curves were used to determine the approximate age of pouch young examined at Whipsnade. Eighty-four percent of births occurred in August and September, exactly a six month difference from births reported for this species in Tasmania. The mean length of pouch life of wild living wallabies was 247 days with a range of185–284 days. Young wallabies were observed accompanying their mothers for up to 204 days after emerging permanently from the pouch. Sixty-three percent of young vacated the pouch in May. Sixty-three percent of the total (104) pouch young examined in the course of this study, from animals caught or from post mortem records, were male, but teat selection showed a random distribution. The gestation period from removal of pouch young to day of birth was 27·3 days. The Bennett's wallaby showed precise seasonal breeding with embryonic diapause that may extend for up to 11 months.     

Evidence that the seasonally breeding Bennett's wallaby (Macropus rufogriseus rufogriseus) does not exhibit short-day photorefractoriness

Adult female Bennett's wallabies (N = 6) were maintained in artificial winter solstitial daylengths commencing 3 weeks before the winter solstice for 16 or 42 weeks. Such treatment effectively prevented the normal establishment of seasonal reproductive quiescence with animals continuing to exhibit reproductive cycles beyond the time of the normal termination of the breeding season. Animals maintained in natural photoperiods or simulated natural changes in daylength after the winter solstice all entered reproductive quiescence by early February. In the Bennett's wallaby, therefore, the breeding season does not terminate as a result of refractoriness to short daylengths. Our results indicate that the relatively small increases in photoperiod shortly after the winter solstice provide the environmental signal responsible for initiating the onset of seasonal reproductive quiescence which normally occurs 5-8 weeks after the solstice. These results contrast with the effect of fixed artificial summer solstitial daylengths on the onset of the breeding season in which breeding begins spontaneously at the normal time of year as a result of long-day photorefractoriness.     

Refractoriness to melatonin and short daylengths in early seasonal quiescence in the Bennett's wallaby (Macropus rufogriseus rufogriseus)

Adult female Bennett's wallabies were treated with reductions in daylength, melatonin implants or injections of melatonin 2 h before dusk in early or mid-seasonal reproductive quiescence. In early reproductive quiescence (5 weeks after the winter solstice) reproductive quiescence did not end in response to 3 or 5 h of reduced daylength or in response to injections (400 ng/kg) or implants (0.5 g in a Silastic rubber envelope) of melatonin. Reductions in daylength at this time of year did, however, result in an extension of the circadian pattern of melatonin secretion. In mid-reproductive quiescence (21 weeks after the winter solstice) treatment with a 5 h reduction in daylength, melatonin injections administered 2 h before dusk or melatonin implants did result in the termination of reproductive quiescence and reactivation of the quiescent corpus luteum within a period of 5 days. The results of these experiments indicate that, in early reproductive quiescence, the Bennett's wallaby is refractory to the influence of reduced daylength or melatonin, although capable of responding to such reduced days in terms of an increased duration of melatonin secretion. Bennett's wallabies therefore exhibit a refractoriness to short days similar to that of some seasonal eutherians although it remains to be established whether this refractory response is the cause of the transition to seasonal reproductive quiescence.     

The role of refractorinesss to long daylength in the annual reproductive cycle of the female Bennett's Wallaby (Macropus rufogriseus rufogriseus)

The beginning of the breeding season of the female Bennett's wallaby occurs when seasonal quiescence terminates 1-2 months after the summer solstice. In this study, the role of photoperiod in terminating seasonal quiescence was examined. One week before the summer solstice, five non-lactating wallabies were transferred from natural to artificial summer solstice daylength for 5 months. The beginning of the breeding season in these animals as indicated by births, matings, and peripheral progesterone profiles was not different from that of five control animals maintained on natural photoperiod. The following year, three animals were transferred from natural to summer solstice daylength on February 25 and were held on the artificial photoperiod until September 30. Changes in plasma progesterone concentrations indicative of the beginning of the breeding season occurred on June 12-30 (range), which was significantly (P less than 0.01) advanced by 29 days when compared with six control animals. These results indicate that the decrease in daylength that occurs after the summer solstice is not required to induce the termination of seasonal quiescence at the beginning of the breeding season. Further, the beginning of the breeding season can be advanced by transferring animals to long daylength early in seasonal quiescence. Photorefractoriness to long daylengths may therefore be important in the initiation of the breeding season in this species. In further experiments, groups of six animals were transferred from natural to artificial summer solstice daylength on September 26 and December 9 and pouch young were removed 7 days after the transfer. In September, reactivation of the quiescent corpus luteum followed soon after removal of pouch young (RPY) indicating that exposure to long daylength had not induced a transition into seasonal quiescence. In December, RPY was not followed by reactivation of the quiescent corpus luteum indicating that animals were in seasonal quiescence. These results suggest that the female Bennett's wallaby may need to experience a period of shortening days after the summer solstice before exposure to long days can again initiate seasonal quiescence.     

Social interactions and reproductive tactics in red–necked wallabies (Macropus rufogriseus banksianus)

Male red–necked wallabies established dominance relationships by fighting, and dominance rankings among males were positively correlated with body size. Females became outstandingly attractive to males during the week preceding mating, and males, who normally ranged widely and solitarily in search of mates, gathered in groups around such females. It is suggested that females, by prolonging their advertisement of oestrus, and thereby inciting sustained competitive interactions among the males who were attracted to them, contributed to a bias in the distribution of male mating success in favour of very large dominant individuals. High–ranking males mated within discrete but undefended areas of absolute dominance ('dominions'). Direct interactions between dominion–holding males were rare, but males just below dominion–holding status often fought with one another, and were frequently harassed by dominional males.     

The breeding biology of Bennett's wallaby (Macropus rufogriseus jruticus) in South Canterbury,New Zealand

Abstract

The lipid and amino acid composition of the egg contents of captive dwarf cassowary (Casuarius bennetti) was investigated. Although the proportions of triacylglycerol (65%) and phospholipids (27%) were similar to those found in domestic hen eggs, the fatty acid content of the lipids was different. Egg lipids contained less than 2% linoleic acid and this is probably inadequate for chick development. An oil of high linoleic acid content — such as com oil — as a supplement to the maternal diet could improve the breeding success of these birds in captivity.     

Reproductive biology of the Red-necked wallaby (Macropus rufogriseus banksianus) and Bennett's wallaby (M. r. rufogriseus) in captivity

Bennett's wallaby ( Macropus r. rufogriseus ) of Tasmania give birth from late January to early August in marked contrast to the Red-necked wallaby ( M. r. banksianus ) of mainland south-eastern Australia which produced young in all months. Within the breeding season however, the lengths of the oestrous cycle and gestation period are similar in the two forms and did not differ by more than 0.5 days. The gestation period of about 30 days extended to almost the length of the oestrous cycle of approximately 33 days. Birth was closely followed by mating which normally resulted in fertilization and subsequent embryonic diapause. Renewed blastocyst development was initiated by removal or loss of a pouch young and birth followed about 27 days later.
Unlike other macropodids with a similar breeding pattern, birth, as a result of renewed blastocyst development near the end of a large young's pouch life, did not occur within a day or two of the permanent emergence of the young, but followed 16 to 29 days later. In M. r. rufogriseus , young that left the pouch permanently in the non-breeding period were not replaced by new young until the beginning of the next breeding season two to four months later, and blastocysts resulting from mating of females without pouch young at the end of the breeding season remained quiescent until the next breeding season five to eight months later.
Females of both subspecies first mated at an age of about 14 months, and males were producing mature spermatozoa by about 19 months.
Young first left the pouch for short periods at about 230 days of age and permanently at about 280 days.
Observations are also given on reproductive behaviour, interpretation of vaginal smears, sex ratio of young, selection of teat by pouch young, and development of morphological features in known-age young that may be used as an aid in age determination.     

Toxoplasmosis in wallabies (Macropus rufogriseus and Macropus eugenii): blindness, treatment with atovaquone, and isolation of Toxoplasma gondii

Australasian marsupials, especially wallabies, are highly susceptible to clinical toxoplasmosis. This paper describes the use of atovaquone for effective treatment of toxoplasmosis in 4 Bennett's wallabies (Macropus rufogriseus), along with the serology, isolation of Toxoplasma gondii, and genotyping of 3 T. gondii isolates from 5 captive wallabies. This is the first report of success in treating acute toxoplasmosis in wallabies, the first report of serology followed over a significant period of time, and the first report of isolation and genetic typing of T. gondii from wallabies in the United States.     

Social behaviour and heart rate in tammar wallabies (Macropodidae: Macropus eugenii)

In an enclosed group of tammar wallabies the behaviour of all individuals and the heart rate (HR) of three males were recorded simultaneously. The social structure was characterized by the dominance relationships between the males and the sexual preference of all males for the oldest female. During non-oestrus, dominance was obvious when a male intervened terminating the sexual behaviour of a subdominant one. The relatively low amount of agonistic behaviour between the males is assumed to be due to the clear dominance relationships. Locomotion as well as sexual and agonistic behaviour were accompanied by an acceleration of HR. The HR pattern depended on the intensity of the behaviour, its duration and the animal's identity. Commonly performed sexual behaviour and approach/retreat encounters gave rise to HR values not different from HR values during locomotor activity without interactive components. Social events that occurred infrequently—like fights, and the mating of an oestrous female—were accompanied by strong accelerations of HR indicating high cardiac effort. The mild cardiac activity during common social encounters is consistent with a strategy of maximizing energy conservation. HR patterns during specific behaviour could not entirely be accounted for by the energetic costs of activity. Spreading the forelimbs in response to specific stimuli—like the fly-over of raptors—was indicative of a strong HR response even if the animal was motionless. During specific social encounters like the sexual behaviour of the alpha-male following an intervention—HR responses revealed that arousal might exceed motor activity in affecting HR. Individual differences of these HR responses are attributed to the age, experience and social status of a male.     

Seasonal changes in the reproductive organs and plasma and pituitary hormone content of the male Bennett's wallaby (Macropus rufogriseus vufogriseus)

In a number of species of seasonally breeding marsupial, the male is fertile throughout the year but there is a marked seasonal change in weight of the accessory sexual glands. In this study, body weight, prostate, epididymis and testis weights and plasma concentrations of testosterone, LH and prolactin and pituitary content of LH and prolactin were determined in male Bennett's wallabies shot at 1–2 month intervals over a period of 17 months. There was a highly significant increase in prostate weight which was coincident with the breeding season for this species. A small but significant increase in testis weight was also observed but epididymis weight remained unchanged. Plasma testosterone concentrations were significantly increased at a time coincident with the increase in prostate weight. Plasma prolactin and LH concentrations were low in most animals and remained unchanged during the study. In contrast, pituitary prolactin and LH contents showed highly significant changes, with increasing and peak hormone content preceding maximum prostate weight and plasma testosterone concentrations by several months. While these latter results suggest a role for prolactin and LH in the seasonal control of the reproductive organs in the male wallaby, a more intensive study of the pattern of secretion of these hormones and possibly more sensitive hormone assays are required to understand their relative roles in regulating the annual cycle of prostate growth.     

Sexual behaviour of male and female tammar wallabies (Macropus eugenii) at post-partum oestrus

This study describes the sexual behaviour of the adult male and female tammar wallaby from the time a female gives birth to the end of post-partum oestrus. Eleven females were continuously observed from around the time of birth until up to 3 h after the last observed mating attempt. Males began to associate with females from around the time of birth, thus females appear to be attractive to males at, but not prior to parturition. Females subsequently allowed males to mate with them from 1.3±0.8h (mean±S.D.) post-partum, although the first ejaculation was delayed until 1.8±0.8h after birth owing to intense intermale aggression directed towards any male which attempted to mate with an oestrous female. Mating chases, in which a post-partum female was pursued by several males, were observed from 1.3±0.8h post-partum. All of this mating activity usually occurred within the first 6h after birth.     

The role of tendon elasticity in hopping in a wallaby (Macropus rufogriseus)

The elastic properties of the major tendons of wallaby feet have been investigated in dynamic tensile tests at a frequency close to normal hopping frequencies. In addition, bending tests have been performed on the intertarsal and tarso-metatarsal joints. The data are used to calculate the strain energy stored temporarily in the tendons and ligaments of the legs during a typical hopping stride. The contribution made by stored strain energy to the work required for hopping is assessed.     

Peace-Making in Marsupials: The First Study in the Red-Necked Wallaby (Macropus rufogriseus)

The issue of reconciliation has been widely investigated in many eutherian mammal species. Nevertheless, no data are available for marsupial mammals. Indeed, the majority of reports focus on group dynamics from an ecological and reproductive perspective, but no study has investigated them from a social point of view. We observed the red-necked wallaby colony (Macropus rufogriseus) hosted at the Tierparc Zoo Berlin (Germany) and collected data on aggressive and post-conflict interactions between group members. We found that the phenomenon of reconciliation is present in the study species (mean group CCT 27.40% ±8.89% SE). Therefore, we demonstrated, for the first time, the occurrence of reconciliation in a gregarious marsupial mammal. Post-conflict reunion was not affected by the relationship quality between individuals (friendship or kinship) but it was fine-tuned according to the aggression intensity. For example, low intensity conflicts were reconciled whereas high intensity ones were not. Reconciliation reduced anxiety-related scratching in both of the former opponents and limited further attacks towards the victim during the post-conflict period. These findings suggest that the red-necked wallaby, like many eutherian species, can evaluate the costs of reconciliation and engage in peace-making behavior in the right contexts, in order to maximize its pay-offs.     

Age-related Differences in Playfighting Strategies of Captive Male Red-necked Wallabies (Macropus rufogriseus banksianus)

Age-related differences in the playfighting strategy of captive male red-necked wallabies Macropus rufogriseus banksianus was examined. Our purpose was to determine whether wallabies adjusted their play in response to their partner's age and, if so, how. The way in which a wallaby played was dependent on the relative age of its partner, and this pattern tended to be the same regardless of whether it was the initiator or reactor of the interaction. If a wallaby's partner was younger than itself it adopted a defensive strategy in which it self-handicapped by standing flat-footed, Pawing rather than Sparring, and by not using its full strength. Its greater rate of Shaking suggests that this act may function as an appeasement signal in play. Furthermore, it was highly tolerant of the tactics used by its younger partner and took the more active role in prolonging interactions. If, on the other hand, its partner was older than itself, it adopted an offensive strategy involving vigorous Sparring, increased time in the High-stance posture and a greater percentage of bouts that were of high intensity. Indeed, it played with even more vigour than when it playfought with wallabies of the same age as itself. Differences in the play of same-aged partners were in the non-fighting components of play, while those of differently-aged partners were in the fighting components. Play between same-aged partners, however, tended to be more stable and more competitive than that between partners of differing age. These results are discussed with emphasis on the compromises made in order for play to occur and the potential benefits to each partner of play in mixed-age class encounters. We briefly consider the implications of self-handicapping in the categorization of macropodid fights as play or aggression.     

On the synchronization of breathing with running in wallabies (Macropus spp.) and horses (Equus caballus)

Previous investigations have shown that, when they run, wallabies and various quadrupedal mammals take exactly one breath per stride. It has been suggested that their breathing movements may be driven by the movements of running, and three mechanisms have been proposed: the lungs may be compressed and expanded by vibrations of a 'visceral piston', by bending and extension of the back or by the forces imposed on the rib cage by the forelegs.
The three mechanisms are tested against published observations on wallabies and horses. Simple mathematical models are used to predict the phase relationship between running and breathing for each mechanism, and the amplitudes of breathing that they could cause. The observed breathing movements of hopping wallabies are consistent with a visceral piston mechanism tuned to the stride frequency, but cannot be explained by either of the other mechanisms. Those of cantering and galloping horses are not consistent with a tuned visceral piston mechanism, but could be driven by the bending and extension of the back.     

Intestinal lactase (beta-galactosidase) and other glycosidase activities in suckling and adult tammar wallabies (Macropus eugenii)

The activities of various glycosidases in homogenates of the small intestinal mucosa of two adult and 18 suckling tammar wallabies (M. eugenii) aged from 6 to 50 weeks were investigated. Lactase (beta-D-galactosidase), beta-N-acetylglucosaminidase, alpha-L-fucosidase and neuraminidase activities were high during the first 34 weeks post partum and then declined to very low levels. Maltase, isomaltase, sucrase and trehalase activities were very low or absent during the first 34 weeks, and then increased. The lactase activity was unusual in being greater in the distal than the middle or proximal thirds of the intestine, and in its low pH optimum (pH 4.6), inhibition by p-chloromercuribenzene sulfonate but not by Tris, and lack of cellobiase activity. These properties are those of a lysosomal acid beta-galactosidase rather than of a brush border neutral lactase. The maltase activity had the characteristics of a lysosomal acid alpha-glucosidase early in lactation and of a brush border neutral maltase in adult animals. The significance of these findings is discussed in relation to changes in dietary carbohydrates during weaning and to the mode of digestion of milk carbohydrates by the pouch young.