Naoki Tomita

Environmental perturbations influence telomere dynamics in long-lived birds in their natural habitat

Telomeres are regarded as markers of biological or cellular ageing because they shorten with the degree of stress exposure. Accordingly, telomere lengths should show different rates of change when animals are faced with different intensities of environmental challenges. However, a relationship between telomere length and the environment has not yet been tested within a natural setting. Here, we report longitudinal telomere dynamics in free-living, black-tailed gulls (Larus crassirostris) through the recapture of birds of a known age over 2–5 consecutive years. The rate of change in telomere lengths differed with respect to year but not sex or age. The years when gulls showed stable telomere lengths or increases in telomere lengths (from 2009 to 2010) and decreases in telomere lengths (from 2010 to 2011) were characterized by El Niño and the Great Japan Earthquake, respectively. Both events are suspected to have had long-lasting effects on food availability and/or weather conditions. Thus, our findings that telomere dynamics in long-lived birds are influenced by dramatic changes in environmental conditions highlight the importance of environmental fluctuations in affecting stress and lifespan.

Within- and among-clutch variation in maternal yolk testosterone level in the Black-tailed Gulls Larus crassirostris

Abstract Mother birds can enhance growth and/or survival of chicks by supplying energetic and hormonal resources to the egg yolk (i.e. maternal effect). In several bird species, mothers supply higher level of testosterone to the eggs laid later within the clutch and enhance the growth of the chick to compensate for the disadvantage of the later hatching. As same as this within-clutch mechanism, mothers breeding later in the season can be expected to supply higher level of testosterone to the clutch. However, among-clutch seasonal variation in yolk testosterone levels has been rarely described. Here, we investigated among-clutch seasonal variation in the yolk testosterone level in Black-tailed Gulls Larus crassirostris, as well as within-clutch variation. Mean yolk testosterone level of eggs laid later within the clutch (“b-eggs”) was significantly higher than that of eggs laid earlier (“a-eggs”). The yolk testosterone levels of both a- and b-eggs of later breeders were significantly higher than those of earlier ones, while this trend was not observed in mean egg mass. Our results indicate that mothers establishing the clutch later in the season would invest more maternal testosterone into the clutch.

Latitudinal Variation in Birth Dates of Northern Fur Seals (Callorhinus ursinus) in Captivity

Seasonality of mammalian reproduction is ultimately related to dietary and climatic factors, and the timing of birth is scheduled to optimize offspring survival (Bronson 1985). Reproductive synchrony also represents a strategy that individuals adopt to maximize reproductive success in the course of sociobiological and ecological processes such as sexual selection and predation (Ims 1990). Pinnipeds (seals, walruses and sea lions; Carnivora, Pinnipedia) are distinct from other mammals in having two different phases in their life cycles: reproduction on land (or on ice) and foraging in water. Reproduction in most pinniped species is characterized by tight synchrony of births which ensures that pups are born at the optimal time of year (Atkinson 1997). Seasonality and synchrony of births in pinnipeds then lead to temporal aggregation of postpartum estrus and copulation (Stirling 1975; Boness 1991). Reproductive cycles of female pinnipeds are characterized by embryonic diapause and delayed implantation, a preadaptive feature shared with ursid and mustelid carnivores (Mead 1989; Boyd 1991). Lengths of postimplantation gestation (active gestation) are relatively constant in most pinnipeds (ca. 8 months), and the period of delay in embryo implantation adjusts the length of the whole gestation period and determines the timing of births (Boyd 1991). The northern fur seal (Callorhinus ursinus), a highly polygynous pinniped species, inhabits the North Pacific Ocean, Bering Sea, Okhotsk Sea, and Japan Sea, and breeds on subpolar and temperate islands during summer (Gentry 1998). Their reproduction is characterized by highly synchronized annual cycles (Trites 1992). Synchronization of estrus is linked to monopolizability of receptive females by adult males in terrestrial breeding areas and thus provides a basis for the development of polygyny in this species (Boness 1991). Temte (1985) compared the mean birth dates of two wild populations in Alaska (57°N) and in California (33°N), and postulated that the mean photoperiod of 12.5 h/day in autumn might act as a cue for the implantation and control the synchronization of annual breeding cycles of female northern fur seals. On the contrary, Spotte and Adams (1981) disagreed with the hypothesis of photoperiodic control of reproduction based on the fact that breeding activity of captive northern fur seals captured in Alaska (57°N) and translocated to Connecticut (41°N) was observed in July and August being unaffected by the difference in photoperiod between the two sites. However, their results were inconclusive because they only examined breeding activity by month and their birth records consisted of seven stillbirths that occurred over a period ranging from February to July. Temte (1993) examined birth data of pinnipeds kept in North America, Korea and New Zealand, and found a significant latitudinal gradient of birth timing in California sea lion (Zalophus californianus) and harbor seal (Phoca vitulina). Temte and Temte (1993) further explained that the latitudinal variation of births dates in California sea lions were a response to a common photoperiod (11.5 h/day) before implantation. But Temte (1993) failed to find a significant latitudinal variation in birth timing for northern fur seals due to the small sample size. In Japan, northern fur seals were kept in five aquaria under special permit for domestic law that regulates the capture and possession of this species. In four of the five aquaria, northern fur seals were kept outdoor and exposed to natural photoperiodic conditions (at least during the period from estrus to implantation). These four aquaria were located in two geographical areas with different latitudes: Honshu area (35°N), and Hokkaido area (42–43°N). In this study, we analyze the birth dates of northern fur seals kept in these aquaria to ascertain

Relationship between Non-Breeding Migratory Movements and Stable Isotopes of Nitrogen and Carbon from Primary Feathers of Black-Tailed Gull Larus crassirostris

Abstract Various seabird foraging strategies during the non-breeding season have recently been revealed by combining the use of bio-logging devices and the study of stable isotopic signatures (δ15N and δ13C) from various tissues. In this study, we used these combined methods to determine the relationships between stable isotopic signatures in Black-tailed Gulls Larus crassirostris primary feathers and the areas in which the feathers are presumed to have been grown. The fifth primary (P5) feathers are replaced during late August, and although the migratory movements for seven of the eight gulls studied during this replacement period differed, the isotopic δ15N and δ13C values were similar. These values indicated that the seven gulls fed on a wide range of prey from krill to demersal fish species. The isotopic values from P5 for the individual gull that moved southward after breeding, were much higher than for the seven other birds. In contrast, all eight gulls showed a relatively narrow distribution during the replacement of their outermost primaries (P10), which were replaced during mid October and November. However, the isotopic values from P10 of the individual that moved southward during replacement of P5 were also much higher. The unique isotopic values of this gull might indicate specialization in anthropogenic food resources or high trophic level resources through the migration period, regardless of location. Contrary to previous studies, our research did not detect links between migratory movements and stable isotopic signatures from feathers in Larus gulls migrating through a relatively narrow range and having considerable individual variation in diet.

Seasonal Changes in Hatching Patterns in Relation to Incubation Behavior of the Black-Tailed Gull (Larus crassirostris)

Abstract We investigated the amount of time Black-tailed Gulls (Larus crassirostris) incubated and its effects on hatching interval within two-egg clutches. Incubation patterns were classified into three categories (rising, steady, or pulsed) related to daily change of incubation rate until clutch completion. Hatching intervals (mean ± SD, 0.95 ± 0.76 days) were significantly shorter than laying intervals (2.56 ± 0.75 days). There was a significant positive relationship between incubation rate on the day when the first egg was laid (day 1) and hatching interval (Spearmans rs  =  0.677, P  =  0.016). The incubation rate on day 1 also increased (Spearmans rs  =  0.521, P  =  0.039) as the breeding season progressed, and hatching interval expanded (Kruskal-Wallis test: &khgr;22  =  8.3, P  =  0.016, range  =  0–2 day). Thus, the amount of time gulls spent incubating on day 1 was important in affecting hatching intervals and suggested that parents partially controlled hatching intervals with seasonal change by timing of the onset of incubation in this species.

Effect of Photoperiod on Gonadal Steroid Hormone Levels and Reproductive Cycles of Northern Fur Seals (Callorhinus ursinus)

The northern fur seal (Callorhinus ursinus) is a migratory marine mammal belonging to the family Otariidae that breeds on the islands in the North Pacific Ocean, Bering Sea, Sea of Okhotsk, and near the coast of California during summer (Peterson 1968; Gentry 1998). Their reproduction is characterized by extreme polygyny and highly synchronized annual cycles that are concentrated around the boreal summer (Peterson 1968; Trites 1992; Gentry 1998). Females arrive at breeding sites in early July, give birth within 36 hours, and then enter estrus and copulate within a few days (Peterson 1968). Although active gestation persists for approximately eight months, the total duration of gestation period is approximately one year because of the embryonic diapause (delayed implantation), which accurately synchronizes the annual reproductive cycle (Craig 1964; Boyd 1991). Males return to the breeding sites approximately one month before females, establish their territories in the breeding area, and maintain breeding activities for approximately two months (Peterson 1968). Photoperiod is commonly cited as the main trigger for the synchronization of the annual reproductive cycles of pinnipeds (Boyd 1991; Atkinson 1997; Boyd et al. 1999), and this theory is supported by several studies. Temte (1985) compared the mean dates of parturition between the two wild populations of northern fur seals in Alaska (57°N) and California (33°N) and suggested that a mean photoperiod of 12.5 h/day in autumn acts as a trigger for the termination of embryonic diapause and initiation of implantation to synchronize parturition (also see Spotte and Adams 1981). Kiyota et al. (2009) also observed a significant latitudinal variation in the parturition of captive northern fur seals in Japan, which supported the theory of photoperiodic control of the reproductive cycle. The effect of photoperiod on reproductive cycles has been only experimentally demonstrated in harbour seals (Phoca vitulina) (Bigg and Fisher 1975). Bigg and Fisher (1975) demonstrated that estrus occurred earlier than usual during extended photoperiods and was delayed during shortened photoperiods. However, Daniel (1981) did not detect any effect of a shortened photoperiod on the rate of blastocyst development in northern fur seals. Boyd (1991) interpreted the finding of Daniel’s study to be the result of the relatively insignificant shortened photoperiod and/or the short study period. Seasonal changes that occurred in the testicular activity of male fur seals in captivity corresponded with those that occurred in males in the wild (Kohyama et al. 1999; Tsubota et al. 2001). These studies indicate that photoperiodic control of the male reproductive cycle is similar to that of female reproductive cycle, but this photoperiodic effect has not been extensively studied (Boyd 1991). Photoperiod has been reported to control the timing of implantation and parturition in pinnipeds (Temte 1985). However, this interpretation has not been applied to the timing of estrous and ovulation of non-pregnant females or the testicular activities of males. Other mammals, such as Siberian hamsters (Phodopus sungorus) and gray mouse lemurs (Microcebus murinus), are defined as long-day breeders because their reproductive activities increase in response to day length as the seasons change from spring to summer (Goldman 1991, 1999; Perret and Aujard 2001). Therefore, we aimed to determine whether the reproductive cycles of both female and male northern fur seals would be altered under experimentally induced conditions of extended photoperiods. Seasonal changes in gonadal steroid hormone levels and body weight were used as indicators of the reproductive cycle indices, because changes in these factors in relation to the reproductive cycle have previously been described (Kiyota et al. 1999; Kohyama et al. 1999). The effects of photoperiod on seasonal changes in reproductive cycles