Monotremes
Before discussing the behavior of the short-beaked echidnas, it may be useful to examine the behavior of other monotremes. Uniquely among mammals, monotremes are not viviparous, laying single eggs. Unlike birds, considerable development of the embryo occurs prior to egg laying. The three genera have normal body temperatures (31-33 degreees C) lower than other mammals (Brice 2009). The platypus is the most homeothermic of the monotremes, maintaining near-normal temperature even for hours-long exposures to cold air or water. The observed variability in body temperatures under natural conditions is less than 2 degrees C.
The long-beaked echidna (Zaglossus Bartoni) is found in the mountains of New Guinea. In laboratory studies, they maintained temperatures in a narrow range during exposures to ambient temperatures from 15 to 30 degrees C, likely related to their thick fur and ability to sweat. Long-term temperature monitoring has only been reported for 1 male and 1 female long-beaked echidna living in an outdoor enclosure at a zoo in the temperate climate of Sydney (Grigg et al. 2003).
The long-beaked echidnas were nocturnal with body temperature rising with activity and a daily temperature variation generally of 2-4 degrees C. There were short times of more extreme temperature variation, colder during rain or warmer in the hotter months. There were some departures from the ‘normal’ temperature pattern in the long-beaked echidna when the daily temperature variations were very reduced (sometime less than 0.5 degrees C), which occurred at different times between males and females and generally were longer lasting in females. This could occur any time of the year and the animals remained underground when this occurred. To my knowledge, whether and when in development this occurs for reproductive females is unknown.
Two captured short-beaked echidnas (Tachyglossus aculeatus) were in the same zoo and reported on by Grigg et al. They entered hibernation several times between late fall and late winter with shorter intervals of normal temperatures. This different behavior presumably reflects the adaptation to their colder native climate, smaller size, and less dense fur.
The short-beaked echidna is found as far north as New Guinea and as far south as Tasmania, and in Australia is the native mammal with the widest distribution. Its adaptability to a wide range of climates appears connected to variability in several features related to latitude, elevation, and food supply that have led to it being classified into at least five sub-species. Among these features are variability in fur density and length, mating behavior, torpor/hibernation, and temperature regulation during reproduction.
It has been reported that the short-beaked echidna does not tolerate temperatures much above its normal range, possibly related to having few or no sweat glands. It is an excellent burrower and likely retreats to burrows or hollow logs or lose leaf litter to escape the heat. In parts of its range the winters are mild, but it has been claimed ( ) that all short-beaked echidnas utilize torpor to some extent, presumably to save energy. This may be particularly important in females who do not forage for a long period prior to egg hatching in colder regions.
The reproductive behavior of short-beaked echidnas in a temperate climate has been most extensively studied on Kangaroo Island off the coast of South Australia. It has been reported that at this and other temperate locations both sexes utilize occasional torpor during winter (Rismiller and McKelvey 1996). To my knowledge, at none of these locations has it ever been reported that torpor occurs in females between mating and egg hatching.
Prior to the 1980s and the advent of implantable data loggers, detailed and long-term data on temperature variability could not be obtained. It had been thought that torpor and hibernation was not used during reproduction in female short-beaked echidna during the normal breeding season of July to September (mid to late winter in Australia). However, observations in the Snowy mountains in New South Wales of females hibernating during this time subsequently found them with offspring. This prompted Beard et al. (1992) to monitor temperature behavior at elevations greater than 1000 meters. Non-reproductive females did hibernate throughout this period. However, three females were observed to arouse from hibernation in mid-July to late August, which were later observed with young. The temperature record of one is shown below.
Part of Figure 2 of Beard et al.(1992)
There was a period from a few days before egg laying until hatching when the temperature variability was less than before or after. For cases in this and later studies, when the timing of such stable temperature period relative to egg laying and hatching was not directly observed, these were inferred from the mating date combined with a gestation (conception to egg laying) time of 20-24 days and time to hatching of 10.5 days (Griffiths 1978, Green et al. 1985), or extrapolated back in time based on the weight of young during lactation utilizing unpublished growth curves of Griffiths. From what I can infer, all these estimates were derived from observations in temperate areas of south and southwestern Australia and may not necessarily be accurate for sites at colder sites.
For the two other females there were gaps in the temperature records, but both showed indications of a period of lower variability. They found evidence that the beginning of the low variability period corresponded to the female entering and plugging with dirt the “incubation burrow” in which she remained until after egg hatching. In all three cases, egg-laying and hatching were estimated to be within a low variability period. After laying the egg is deposited into a pouch, so even then the temperature, although likely lower than the core temperature of the mother, should show variations principally reflecting those occurring in the mother.
I estimated that the egg laying happened 3-5 days after the beginning of the low-variability period. Eggs are laid around the time the 19th somite forms (Werneburg and Sanchez-Vallera 2011), corresponding to the late gastrula or early neurala stages. This estimate of the stage at which egg laying occurs was based on samples taken of the Tasmanian sub-specie in the 1920s by Theodore Thompson Flynn, incidentally the father of actor Errol Flynn (Carter 2021). In mice the 19th somite forms around 9.3 days post coitus and the time between somite formation is about 90 minutes ( ). Assuming the development stages take 2.4 times as long to occur in echidna as in mice, somites would form about every 3 and a half hours, or less than 3 days for 19 somites to form. If all these underlying assumptions are correct, the period of low temperature variability likely begins before somites form in the neck/thoracic region and even possibly before gastrulation begins.
Beard and Grigg (2000) also reported in a study from the highlands of south-east Queensland a period of low temperature variability for reproducing females. The site was at a lower elevation, around 500m, and farther north than the previous site, so the winters should be milder. The technology of data loggers had advanced enough that readings could be obtained more frequently as shown below for one female in the second of two consecutive reproductive years.
Part of Figure 3 of Beard and Grigg (2000) T:torpor, A:arousal, H: hibernation, M:mating, arrow brackets: period of low temperature variability
Females at this site during spring through summer show periods of a few days in which their daily temperatures vary up to 5 degrees C interspersed with periods of larger fluctuations of up to 10 degrees C, even in summer, with their lowest temperatures approaching ambient temperatures, which the authors interpreted as torpor (T). In this reproductive cycle, this female showed periods of hibernation (H) starting in the early fall, with temperatures decreasing up to 20 degrees C below the normal range, with short periods of arousal (A). In the prior year, this female did not begin hibernation until late fall. Final arousal to an active phase occurred in late July or early August.
Following the final arousal in mid-winter, there appear to be at least five periods with distinct temperature behaviors. Initially, this female had daily fluctuations of around 8oC, but with lowest temperatures much above the ambient temperatures, so likely not torpor. There was then a period of a few days with higher daily low temperatures. The authors had reported earlier (Beard and Grigg 1992) that “the body temperatures of paired echidnas in a retreat were higher than those of solitary echidnas in similar retreats and attributed this to the activity associated with mating.” For all subspecies of short-beaked Echidna at lower elevations there have been observation at times of reproductive females being followed by a more by than one male (Rismiller and Grutzner 2019) and for male-female interactions to last for a considerable time. On Kangaroo Island in South Australia this may last as long as two months, ending in a “shoving match” in which the winner subsequently mates with the female (Rismiller 1991).
After this mating encounter, there was again a period of larger daily temperature fluctuations lasting about 10 days, but the low daily temperatures appear to be less than immediately after the final arousal. When the females entered and plugged the brooding burrow, the daily temperature variation was very low for a period of around 22 days.
For the female who reproduced in two consecutive years, assuming that the prior short low temperature variability period was indeed the time of fertilization, I estimated using the same procedure as previously the eggs were laid between 4 and 7 days after the stabile period began, and it is likely the eggs hatched before the stable period ended. A similar pattern was observed in a third pregnancy and a consistent temperature pattern was observed in a fourth pregnancy with intermittent temperature measurements rather than continuous monitoring. These observations seem consistent with gastrulation starting after the beginning of the long low temperature variability period.
Following the time of presumed egg hatching, the daily temperature variations again became large in spring, indicating the resumption of active foraging with occasional torpor.
The temperature history of reproductive females has been most extensively studied in Tasmania by Nicol and his colleagues (Nicol and Andersen 2002, Nicol 2005, Nicol and Andersen 2006 and 2007, Morrow et al. 2017). The somewhat different behavior they observed presumably reflects the cooler climate and/or lower availability of food.
In this location, daily temperature fluctuation during the active phase prior to hibernation was generally less than 5 degrees C, with much fewer large daily fluctuations that may indicate torpor than reported for the milder Queensland site. This may seem counter-intuitive to torpor being used to conserve energy. It may instead reflect the necessity for this insectivore to forage more in the cooler climate.
Females go into a period of daily torpor in late summer, then in fall enter periods of hibernation in burrows. Body temperatures may drop as much as 25 degrees C below normal in winter, interrupted by short periods of near normal temperatures. Males enter hibernation earlier than females and arouse in early winter, even seeking out females in their hibernation burrows and mating with them. If pregnancy has not occurred by late July (midwinter), the females arouse, mate shortly after, and do not reenter hibernation prior to egg-laying.
If pregnancy occurs earlier, females may arouse and then re-enter hibernation, with the time until egg laying increasing (to as much as 50 days later), corresponding to cumulative duration of subsequent hibernation(s) in addition to the normal gestation time (Morrow and Nicol 2009). They re-enter hibernation no more than 5 days later, when the embryo is probably not more advanced than the blastocyst. It thus appears development comes to a standstill during the hibernation periods. This behavior may be like diapause, which is observed in some marsupials and placentals.
The figure at right shows the temperature variation and visual observations after the final arousal from hibernation in one female that reproduced four times in a five-year period (Nicol and Andersen 2006). Similar data was also presented for five other females (one twice) which progressed at least through egg laying. Following the final arousal, body temperatures fluctuated daily about 3-4 degrees C. When females entered the closed nursery burrow, the variation in body temperature became considerably less (about 1 degrees C) than during the arousal period, and the variation no longer had 24-hour periodicity.
Two females that left the burrows and became active 3 and 6 days after the start of the low temperature variability period were observed to have eggs in their pouches. Within ten days they began undergoing hibernation, so apparently the eggs or new hatchlings were lost.
For five of the pregnancies, live births were later confirmed. In one case (5DSE 1999) the hatchling was estimated to be 0-2 days old and the female had previously been observed with a male shortly after arousal. This information led to an estimated time of egg-laying being two days prior to the beginning of the low temperature variability period. For three other cases, the young were not observed until approximate ages of 19, 30, and 51 days. Assuming a 10.5-day incubation and using growth curves from Rismiller and McKelvey (2003), the mid-ranges of the estimated time of egg laying were 1, 6, and 5 days after the beginning of the low temperature variability period.
Internal temperature data for a different female over a three-year period was used in a later report to illustrate how the period of hibernation lasted much longer for her one non-reproductive year than for two reproductive years (Nicol and Andersen 2007). They did not comment that in the two reproductive years the time after the final arousal before the start of the low temperature variability period, by my estimate around 9 and 17 days, was considerably shorter than the estimated gestation time of 20-24 days. This suggests that in some cases conception may have occurred prior to the final arousal and that some development had already occurred.
That this could be the case was addressed by an extensive study of matings occurring prior to the final arousal (Morrow and Nicol 2009). In prior studies “on several occasions … we found males with females which were torpid or which subsequently re-entered hibernation.” In this study, both males and females were radio-tracked and information on the timing and conditions of mating were variously obtained by cameras, direct measurements of internal temperature and presence of sperm, and external temperature loggers glued to spines. One to four males at a time were found to be present with females, who frequently appeared torpid with sperm present in the cloaca, some of which subsequently entered torpor.
Part of Figure 2 from Nicol and Andersen (2006). Circles-observed in nursery burrow, triangles-observed active, squares-observed in another shelter, squares-observed with male(s). dashed line-estimated beginning of stable temperature period. Solid line-first observed with egg or young. Shaded area-estimated interval of egg-laying based on observation of an egg or the weight of young.
One female was extensively studied and mated five times over a 17-day period in which she repeatedly entered short periods of torpor. Twelve days after the first known mating (July 11), while in torpor an embryo was detected in her uterus (and again five days later when fresh sperm was also detected). She was observed to enter a Nursery burrow on August 7, so presumably development had progressed to near the egg-laying stage despite the frequent torpor.
The figure below shows the external temperature record for another female. This female entered the nursery burrow only about 10 days after the last arousal from hibernation. Prior to the last hibernation, there had been a long period of activity, at the beginning of which they assumed a successful mating.
Figure 2 of Morrow and Nicol (2009). Arrow1- presumed time of fertilization; Arrow2- arousal from final hibernation; Arrow3- entry into the nursery burrow.
Rismiller and McKelvey (2000) reported that on Kangaroo Island some females continued to forage while incubating the egg in their pouch while others remained in a burrow until hatching. There does not appear to be detailed records of temperature variation for females reproducing in warmer conditions in which torpor is infrequent. I have found only one, in which three captive females of the northern and western sub-specie were monitored with external (spine-attached) temperature loggers at a zoo in Perth (Ferguson and Turner (2013). Single males were temporarily placed with single females in outdoor enclosures with an artificial burrow and activity was monitored, including inside the burrow by infrared video cameras. Initially the pair was active only in the late afternoon and early evening. When courtship began, activity occurred throughout the night, then returned to the prior behavior after mating. During five pregnancies, females were active for and average 22 days after mating, before remaining in the burrow for an average 12 days prior to egg hatching. The time in the burrow was thus considerably less than in studies in colder regions, where the mother (with young in her pouch) remained in the burrow for some time after the eggs hatched.
The figure at right shows the temperature record for two of the pregnancies in the second year of the three-year study. The shaded box shows the time when the females did not leave the burrow. The enclosure of the female shown in upper half had partial exposure to the sun. In the first year of the study this female was sometimes observed to bask in the sunlight after becoming active. During these times the external monitor would record spikes in temperatures exceeding 30 degrees C. The authors also show data from the same female when such spikes were observed in 18 of 30 days in May. Two such temperature spikes are evident in this female on the days immediately before and after the extended period in the burrow despite it being winter. Heat lamps were installed in the other enclosures without sunlight the next year, but the females only utilized them during the night. No such spikes were observed for the female shown in the lower half.
Figure 5 of Ferguson and Turner (2013)
Lower external temperature variability was shown during the extended burrow period than before or after. The extent that this reflects temperature variability experienced by the embryo/egg is of course unknown. In this study females incubating eggs in the burrow were observed to shiver for short periods of time. Beard et al. (1992) had observed that in mating retreats “activity … could be detected as rapid variations in strength of the radio signal (resulting from the orientation of the transmitter and its attached antenna changing with body movements).” Beard and Grigg (2000) also frequently observed signal variability for females in “plugged” burrows. They suggested that they “were moving or shivering to generate heat required to maintain the higher and more stable than normal body temperatures observed.” They speculated that “a constant, warmer temperature at this stage is necessary to maintain development.” To my knowledge, this is the first statement of the homeothermic hypothesis studied here, with perhaps with a change to “maintain proper development.”
A close examination of all the published internal temperature data suggests three distinct phases of temperature variation during the period in the burrow. In most cases there are at least 5 days with a stable average daily, followed by a period of slowly decreasing temperatures, but still with low variability. There is then a final period, likely following hatching, when there is more daily variation, but still less than the earlier or later active periods. Although considerable uncertainty remains concerning when the stages of developing are occurring in this species, I think the this first stable period likely overlaps all or some of the time from gastrulation to pharyngula (G/P) stages.
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