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Photoperiod and the Timing of Reproduction in Antechinus Flavipes

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Photoperiod and the Timing of Reproduction in Antechinus Flavipes ARTICLE IN PRESS www.elsevier.de/mambio Original investigation Photoperiod and the timing of reproduction in Antechinus flavipes (Dasyuridae: Marsupialia) By B.M. McAllan and F. Geiser Centre for Physiological and Behavioural Ecology, School of Biological, Biomedical and Molecular Sciences; and Centre for Physiological and Behavioural Ecology, Zoology, University of New England, Armidale, NSW 2351, Australia Receipt of Ms. 25.4.2005 Acceptance of Ms. 17.1.2006 Abstract The effect of an artificial, unchanging photoperiod regime was examined in comparison to a natural photoperiodic regime on the reproductive pattern in Antechinus flavipes, a small dasyurid marsupial which in the wild has a short, highly synchronized mating period. Females held under a photoperiod of LD 12:12 showed delayed sexual maturity and only one individual entered oestrus, about 3 weeks after females under natural photoperiod. Oestrus could be induced in the remaining females by increasing the photoperiod by 1 min/day for at least 3–4 weeks. In contrast to the females, males under artificial and natural photoperiod showed a similar pattern of maturity and decline of reproductive condition and senility. Only some aspects of sexual maturity were delayed and others were unsynchronized in males under LD 12:12 regime compared to the males held under the natural photoperiod. Our study suggests that, especially in females, changing photoperiod is important in synchronizing reproductive events in A. flavipes. r 2006 Deutsche Gesellschaft fu¨r Sa¨ugetierkunde. Published by Elsevier GmbH. All rights reserved. Key words: Antechinus flavipes, marsupial, photoperiod, reproduction Introduction Photoperiod and endogenous circannual seasonally constant conditions of photoper- rhythms are important in regulating repro- iod and temperature, remain in the repro- ductive cycles in many placental mammals ductive state proscribed by the proximate (Bronson 1985; Goldman 2001). Circannual photoperiodic cue, and change reproductive rhythms can be pronounced, with some status only in response to a change in the species demonstrating repeated and approxi- photoperiod (Bronson 1985; Goldman 2001). mately yearly reproductive cycling while held Whereas placental mammals have received under seasonally constant conditions of considerable attention with respect to inter- photoperiod and temperature (e.g., ground actions between photoperiod and reproduc- squirrels and sheep, Bronson 1985; Ko¨rtner tion, few studies have been performed to and Geiser 2000; Goldman 2001). However, determine whether similar control mechan- many other mammals exhibit non-circannual isms exist for marsupials, especially for the seasonality. These species, when held under order Dasyuromorphia (McAllan 2003). 1616-5047/$ - see front matter r 2006 Deutsche Gesellschaft fu¨r Sa¨ugetierkunde. Published by Elsevier GmbH. All rights reserved. doi:10.1016/j.mambio.2006.01.005 Mamm. biol. 71 (2006) 3 Á 129–138 ARTICLE IN PRESS 130 B.M. McAllan, F. Geiser Reproduction in the marsupial genus Ante- study was designed to provide experimental chinus (Dasyuromorphia) is typified by a evidence regarding the extent of the photo- short, highly synchronized mating period, periodic control of reproduction in the the timing of which varies only little from yellow-footed antechinus, A. flavipes. year to year (Dickman 1982; Lee et al. 1982; McAllan et al. 2006). Females are mono- estrous and all males die shortly after mating (Woolley 1966; Wood 1970). While the Material and methods pattern of the reproductive behaviour has Experimental conditions been extensively monitored, little work has been done to establish the mechanisms by Experimental animals consisted of 17 laboratory which reproduction is controlled (Dickman reared A. flavipes, the offspring of pregnant females 1985; Scott 1986; Woolley 1966; Wood 1970; wild caught in the Adelaide area, South Australia (341500S, 1381300 E), and all experiments were McAllan et al. 1991). Most work has focused conducted in Adelaide. They were fed a mixture of on members of the A. stuartii/A. agilis moistened dog or puppy chow and tinned cat food complex with few studies exploring mechan- which was exchanged daily late in the afternoon. isms of regulation of the reproductive cycle in Dry cat chow and water were available ad libitum. other species (Dickman 1985; Scott 1986; All animals were housed under a natural photo- Woolley 1966; Wood 1970; McAllan et al. period of Adelaide while with their mothers or 1991). other juveniles until the beginning of the experi- Dickman (1985), on the basis of experimental ment, when all juveniles were weaned and were evidence, has suggested that photoperiod separated from other individuals. From 23 Febru- may cue an endogenous rhythm in three ary all animals were housed individually in cages (45 Â 30 Â 16 cm) provided with hard wood shav- species of Antechinus. In this study A. stuartii, ings and nesting boxes containing nesting material. A. flavipes, and A. swainsonii were placed Four males and five females were maintained under under LD 12:12 photoperiod at differing natural photoperiod conditions of Adelaide times from late-April to June (when the throughout the experimental period. Four male natural photoperiod is decreasing towards and four females were placed under an unchanging the winter solstice, in late June), which artificial photoperiod of LD 12:12. This photoper- resulted in unsynchronized reproductive ac- iod was chosen as it is the longest photoperiod tivity when compared to animals held under prevailing at the reported mating times in A. the naturally changing cycle, although ex- flavipes (Schmidt and Mason 1973). Females under artificial photoperiod which had not shown signs of perimental animals did reproduce at an oestrus by late September (8 weeks after those approximately similar time of year to those under natural photoperiod exhibited oestrus) were held under the natural photoperiod. Dick- exposed to an increase in photoperiod by 1 min/day man (1985) found that the laboratory condi- starting from the original cycle of LD 12:12. This tions of his study also affected reproductive approximates the change in photoperiod naturally synchrony under both naturally changing experienced by A. flavipes during the mating season and LD 12:12 photoperiod, indicating an (McAllan et al. 2006). effect of social organization. McAllan and Dickman (1986) and McAllan et al. (1991) Females demonstrated that a discretely increasing photoperiod (rate of change of photoperiod) Females were checked once every 1–2 weeks and may synchronize reproduction in A. stuartii. during the mating season every 2–3 days, for the Recently McAllan et al. (2006) developed this presence of epithelial cells, which indicate the onset paradigm further by demonstrating a corre- of oestrus (Selwood 1982; McAllan et al. 1991). Urine samples were taken when possible. When lation between the changing photoperiod and females did not urinate a urogenital sinus smear timing of reproduction for all species of was taken by carefully wiping the urogenital sinus Antechinus, and that most wild populations over a clean slide. Samples were examined for of A. flavipes may be cuing to an increasing the presence of epithelial cells and scored on a rate of change of photoperiod of approxi- scale similar to that of Selwood (1982) and mately 77–97 s per day. Thus, the present McAllan et al. (1991). When individuals gave ARTICLE IN PRESS Photoperiod and the timing of reproduction in Antechinus flavipes 131 birth, urogenital sinus smears were discontinued. trapped and released using Elliot box traps during The pouch change associated with sexual maturity, the breeding season at two sites in South Australia oestrus, and pregnancy or pseudo-pregnancy is an (341320 S, 1381300E; and 351S230E). Females were easily observable phenomenon in Antechinus assessed for reproductive condition, mating activ- (Woolley 1966; Dickman 1985; McAllan et al. ity, and subsequent births, and males were assessed 1991) and the pouch changes associated with the for reproductive maturity and signs of reproductive reproductive sequence were scored following senility, as described above. McAllan et al. (1991). The urogenital sinus of A. flavipes becomes very swollen and flushed during oestrus and this indicator was also included in the Statistical analysis scoring system (see McAllan et al. 1991). Reproductive data were analysed by repeated measures Analysis of Variance, using treatment, and date of measurement as variables for the Males duration of the experiment. All male reproductive Males were checked once every 1–2 weeks. The variables were compared on the same day for each scrotal width was measured with vernier calipers. group in each experiment throughout the monitor- The condition of the pelage, the pigmentation of ing period. In females, the peak of the brief the testes and the maturation of the penis were presence of epithelial cells indicating reproductive monitored essentially as described by Woolley receptivity, may be evident between weekly mea- (1966) and McAllan et al. (1991). The presence of surements of reproductive parameters. Therefore, sperm in the urine (spermatorrhoea), which is an female data for presence of epithelial cells were indicator of sexual maturity in male dasyurids compared on the day of measurement for the (Woolley 2003) was also recorded as was the mating period, at all other times data were change of the size of the urethral bulbs or Cowper’s compared at the once weekly measurement. glands, which are paired sets of glands that lie on Data were also analysed by the time of the year either side of the urogenital sinus; according to that the reproductive event occurred for each Rodger and Hughes (1973) these lie adjacent to the individual by numbering the days throughout the crura of the penis. They enlarge just prior to the year, determining the week number when the event mating period in A. stuartii and A. flavipes and in occurred, and then performing an unpaired t-test A. stuartii increase in response to presence of on the day numbers for each treatment group. In testosterone (Woolley 1966; McAllan et al. 1991; males, this was for the date when variables reached McAllan 1998).
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