Placentals
(Under Construction)
Rodentia
McAllan and Geiser (2014) discussed dormouse species in which females have been reported to enter torpor during pregnancy, but it is not clear at what stages of development this occurred.
Lehmer et al. (2003) studied black-tailed prairie dogs in the plains of northwest Colorado. Males and females entered a shallow form of torpor at a similar frequency in early winter. From the period from February 1 through 9, no males or females entered torpor, a period that corresponds to a previously determined period of copulation. Thereafter, only one of three females entered torpor, while 4 of 5 males continued to enter torpor sporadically until late March. Reproductive status of the females was not determined, but the results suggest that pregnant females might remain homeothermic throughout gestation.
Krushchova et al. (2023) studied 68 newly matured male/female pairs of Campbell’s hamsters (Phodopus campbelli) from a long-established colony in Moscow originally obtained from northeast Mongolia. In response to the shortening day length in fall, this species loses weight while growing a thick white winter coat. The pairs were housed in plastic cages with nesting material in a roofed enclosure otherwise exposed to the local weather. Torpor, weight, and reproductive status were followed from September through March and survival of the pairs and offspring were then monitored to the end of that year. Torpor use was very individualistic, from some animals entering torpor frequently to others only once or never. Despite the availability of food, about two-thirds of both males and females entered torpor at least once, with the first occurrences in November, peaking in December, and ending in January. Although sex was not predictive of use of torpor, initial weight and weight loss between September and December were predictive. Lower daily average ambient temperature was also predictive, even though only half as many animals entered torpor in January, even though it was on average colder in January. There was an additional tendency for both members of the pair to enter torpor on the same day. The authors suggest this was due to a reduced temperature in the nest after one of the pair entered torpor that would encourage torpor in the other. Less than 10% of the pairs had bred by the end of December, but this reached about 30, 60, and 80% by the ends of January, February, and March, respectively. Based on the assumption of a gestation length of 24 days and the parturition dates, it was determined that no female and only one male entered torpor during the gestation period. This maintenance of homeothermy, possibility assisted by the coordinated homeothermy of the male, is particularly remarkable for conceptions in January, when the colder ambient temperatures might be expected to result in more use of torpor.
This species can produce several litters in a year and has a short lifespan. By the end of the study (at the end of the following December), 74% of the males and 50% of females were alive. Prior use of torpor was not predictive of survival of the parent or of the total number of pups produced. The results of the study could be interpreted as torpor usage compensating for any detrimental effects from lower body weights prior to reproduction.
In contrast to reproduction starting in winter, immediately after a period when torpor may be used, reproduction starts later in the closely related Djungarian hamster, Phodopus sungorus. Although the two species live at the same latitudes, winters are not as cold in the habitats occupied by the Djungarian hamster, and rain is more plentiful and reliable. These milder conditions may allow this species to not be as “urgent” to begin reproduction as soon as possible. For some juvenile males and females, shorter days in fall not only results growth of the winter coat as in the other specie, but also delays maturation of reproductive organs (Timonin et al. 2006). Other individuals, both males and females, do not undergo the loss of weight and change to the winter coat..
In a laboratory study of newly-born Djungarian hamsters (Przybylska-Piech et al. 2021) on the effect of different periods of acclimatization to a daily light period of 16 hours before transfer to 8 hours of light. Temperature was kept constant throughout the study. About 60% of the animals began to lose weight and then switched to the winter coat immediately after the transfer, about 10% initially gained weight and did not begin to make the switch to the winter phenotype until 2-3 months after the transfer, and about 30% never lost weight and did not switch to the winter coat.
A later study (Prrzbylska-Piech and Jefimow 2022)
Pretzlaff et al. (2014) reported that free-ranging male and non-reproductive female hazel dormice (Muscardius avellanarius) in northern Germany frequently entered torpor from spring to fall, but torpor was not observed in pregnant and lactating animals. However, this study did not exclude the possibility that pregnant females might enter torpor at earlier stages of gestation when pregnancy would not be evident.
Chiroptera
There are many cases of torpor during pregnancy reported for bats in temperate climates. However, in most cases pregnancy was determined by palpation for the fetus (e.g., the lesser long-eared bat (Nictophyilus geoffroyi, Turbill and Geiser 2006) and it is unclear how early in gestation this is possible. In other cases, parturition occurred a short time after the observed torpor (e.g. Hoary bat, (Lasiuris cinerus, Willis et al. 2006), which would have been at a late stage in gestation.
For other species of temperate climate bats, copulation occurs in the fall with birth in the spring or summer following winter hibernation. Sperm is either stored in the female until fertilization after hibernation ends or fertilization occurs immediately after copulation and development halts at the blastocyst stage (prior to gastrulation) and does not resume until hibernation ends (Kawamoto 2003).
In the subtropical fruit bat, Cynopterus sphinx (Banerjee et al. 2007), development is slow for a period from fertilization in November to December (this bat also has another reproductive cycle in the spring/summer when there is no developmental delay). During this time the ambient temperature decreases 13 degrees C and the female enters daytime torpor, during which the average body temperature decreases 5 degrees C, with food intake at night. The lower metabolic rate during daytime contributes to an increase in body weight and fat. In January, although the ambient temperature continues to decrease, torpor ceases, the fat stores are depleted, the body temperature rises 4oC, and development accelerates (starting at the primitive streak stage of gastrulation, which is when the expression of the Hox genes begins).
Racey and Swift (1981) reported that the subtropical bat Pipistrellus pipistrellus would enter torpor after 24 hours starvation beginning 4 or 9 days following the presumed time of fertilization. However, there was no information given on the developmental stage at these times or the effect of starvation and torpor on the offspring.
Eulipotyphia
The European hedgehog, Erinaceus europaeus, remained normothermic during gestation when kept in an outdoor enclosure (Fowler 1988). Almost all males and females entered torpor in mid-summer when exposed to cold without food for 48 hours. However, one female resisted going into torpor during exposure and gave birth 3-6 days later.
Species of the family Tenrecidae are native to Madagascar and have some of the lowest Tb of any mammal. Lovegrove (2000) suggested spiny tenrecs of the sub-family Tenrecinae have some of the lowest basal metabolic rates for animals of their size because they do not need to run fast to escape predators since they can roll up into spiny balls. Reproductive energetics were studied in a lesser Hedgehog tenrec, Echinops telfairi, colony in Aberdeen, Scotland (Poppitt et al. 1994). For males, body temperature (during the daytime non-active phase) was less than 1.5oC above the ambient temperature over a wide range. In contrast, over the range 26-31oC ambient temperature, daytime average body temperature in pregnant females was constant and higher than that of males.
Levesque et al. (2014) studied the thermoregulatory behavior during reproduction of a spiny tenrec, the greater hedgehog tenrec, Setifer setosus. After capture, animals were tagged and body temperatures and respiratory rate measured at temperatures below 25oC and later at a higher temperatures in the thermal neutral zone (the range of ambient temperatures where an approximately constant body temperature is maintained with little change in metabolic rate). Pregnant females and some males were fitted with transponders for subsequent recapture and measurements. Time of parturition was determined by females not moving between burrows.
Below the thermal neutral zone, body temperatures of males and non-pregnant females decreased more than twice as much with decreases in ambient temperature as that of pregnant females, which had much higher resting metabolic rates. Data loggers were implanted in some animals and torpor was only observed once in released pregnant females, 46-49 days prior to parturition. For a gestation time of 61 Days ( ), this likely occurred prior to gastrulation.
For two species of tenrecs, males and non-reproductive females appeared to be poikilothermic in respiratory chambers. However, animals in cages had body temperatures above ambient while all pregnant Dobson’s shrew tenrecs (Nesogale (formerly Microgale) dobsoni, Stephenson and Racey 1993a) and some pregnant large-eared tenrecs (Geogale aurita, Stepenson and Racey 1993b) did not icto
Primates
Use of hibernation and torpor by primates was reviewed by Dausmann and Warnecke (2016). In almost all cases heterothermy is only observed in the cold, dry, and non-reproductive season.
Torpor in the gray mouse lemurs (Microcebus murinus) occurs frequently in the dry season in Madagascar, presumed to be an energy-saving tactic when food is scarce, and not observed during reproduction during the wet season. Canale et al. (2012) used food restriction to see if torpor could be induced during pregnancy and lactation in a captive colony in France. The food restrictions were initiated at various times starting 15 days before the end of the expected 62-day gestation period. Torpor was observed in some of the pregnant females, but not at all for non-pregnant females exposed to the same regimen. It is unknown if similar treatments could induce torpor at earlier stages of development or if this would be compatible with normal development.