PHOTOPERIOD DEFINES THE PHENOLOGY OF BIRTH IN CAPTIVE CALIFORNIA SEA LIONS

A population-based analysis was used to evaluate the role of photoperiod in regulating the precise annual birth timing of captive California sea lions. Latitudinal variation of 463 birth dates was explained by a response to a common photoperiod, 11.48 h/d, occurring 242 d pre-partum and immediately before blastocyst implantation. The lengths of the pupping seasons at the 18 largest captive colonies were significantly correlated to those estimated by the photoperiod model. Hence, the phenology of birth in this species is defined by photoperiod.     

An assessment of population size and distribution of harbour seals in the Republic of Ireland during the moult season in August 2003

The status of Ireland's harbour seal Phoca vitulina vitulina population is poorly understood. The most recent national population estimate dates back to the breeding season in 1978 and did not cover the entire coastline. Reliable up-to-date information on the abundance and distribution of harbour seals in Ireland is necessary to assess the conservation status of the species and for the effective identification, management and monitoring of special areas of conservation required for harbour seals under the EU Habitats Directive. To provide comprehensive current information on Ireland's harbour seal population, a geographically extensive survey was conducted along the coastline of the Republic of Ireland during the species' annual moult in August 2003. This complemented a similar survey of Northern Ireland, which was conducted in 2002. Using thermal imaging technology, haul-out groups of harbour seals and grey seals Halichoerus grypus were identified from the air, aerial-counts were obtained and compared with simultaneous ground-count data from selected sites. Harbour seal distribution recorded during the 2003 moult season was concentrated in the south-west, west and north-west of the country. This national survey yielded a minimum population estimate for the Republic of Ireland of 2905 harbour seals, delivering an effective baseline for current and future population research.     

Clines revisited: The timing of pupping in the harbour seal (Phoca vitulina)

The regional variation in the pupping season of the harbour seal ( Phoca vitulina ) was reviewed using the birth periods reported for 65 colony sites distributed over a range from 30.4 to 78.5 North latitude. The birth timing of P. v. vitulina was not related to latitude, but birthing in P. v. concolor along eastern North America exhibited a latitudinal cline. The timing of birth in P. v. richardsi varied in three distinct patterns: (1) a significant unidirectional latitudinal cline extending between Baja California and the west coast of Washington; (2) a cluster comprised of Puget Sound, Washington and Vancouver Island, British Columbia colonies in which birthing occurred an average of 65 days later than on the Washington coast; and (3) a cluster from northern British Columbia and Alaska which did not demonstrate a latitudinal cline. Insufficient data were available for the analysis of P. v. mellonae or P. v. stejnegeri .
We found great regional variation in the timing of birth among all colonies, with mean birth dates occurring as early as 15 March and as late as 3 September. Little variation existed north of 50. To the south of 50, however, most of the variation could be attributed to correlation with latitude or to affiliation with the Puget Sound, Washington-Vancouver Island, British Columbia geographic area.
Clinal variation in pupping could result from: (1) geographic variations in a selective factor with perhaps gene exchange between contiguous populations playing a role in smoothing the variation; or (2) for populations between Mexico and the west coast of Washington, regional variation in a non-selective environmental variable, such as photoperiod.     

Persistence thresholds for phocine distemper virus infection in harbour seal Phoca vitulina metapopulations

1. This paper explores the concept of the critical community size for persistence of infection in wildlife populations. We use as a case study the 1988 epidemic of phocine distemper virus in the North Sea population of harbour seals, Phoca vitulina .
2. We summarize the available data on this epidemic and use it to parameterize a stochastic compartmental model for an infection spreading through a spatial array of patches coupled by nearest-neighbour mixing, with replacement of susceptibles occurring as a discrete annual event.
3. A combination of analytical and simulation techniques is used to show that the high levels of transmission between different seal subpopulations, combined with the small annual birth cohort, act to make persistence of infection impossible in this harbour seal population at realistic population levels. The well known mechanisms by which metapopulation structures may act to promote persistence can be seen to have an effect only at weaker levels of spatial coupling, and higher levels of host recruitment, than those empirically observed.     

PRECISE BIRTH TIMING IN CAPTIVE HARBOR SEALS (PHOCA VITULINA) AND CALIFORNIA SEA LIONS (ZALOPHUS CALIFORNIANUS)

The absolute and relative precision of birth timing was assessed in 27 captive harbor seals and 30 captive California sea lions. Data were obtained from zoos and aquaria and only adult females with at least three live births were selected for analysis. Individuals of both species demonstrated very high absolute precision with narrow ranges of birth dates and small standard deviations of the individual mean birth dates. In addition, with the exception of one sea lion, no temporal trends for earlier or later birthing were found. Whereas marked differences in birth timing were found among individual harbor seals, these relative differences tended to disappear when subspecies affiliation and location were taken into account. Moderate inter-individual differences were also found among the California sea lions, but these differences persisted following the partitioning of adult females by location.
The absolute precision in birth timing strongly suggests that environmental regulation of birth timing occurs via a highly precise cue, such as photoperiod. The relative differences among individuals may indicate that birth timing in pinnipeds has a heritable component, and hence may evolve in response to natural selection, thus allowing adaptation of the pupping season to specific seasonal environments.     

Photoperiod and reproduction in captive female Northern fur seals*

The reproductive cycles of captive female Northern fur seals (Callorhinus ursinus) were unaffected over two consecutive years by a photoperiod that differed substantially from that of the natural range. Breeding was observed in July and August, or at the same time as in the wild. Growth was comparable in captive and wild fetuses, indicating a similar timing of delayed implantation of the blastocysts.     

Cytochrome P450 1A expression and organochlorine contaminants in harbour seals (Phoca vitulina): evaluating a biopsy approach

We previously reported in vivo induction of cytochrome P450 1A (CYP1A) by beta-naphthoflavone in skin and liver biopsies of captive harbour seals (Phoca vitulina richardsi). The present study evaluated CYP1A expression (immunoblot analysis and ethoxyresorufin O-deethylase activity-EROD) in harbour seals using two study designs: i) skin and liver biopsies from 20 harbour seal pups captured from coastal British Columbia (BC, Canada) and temporarily housed in captivity; and ii) skin biopsies from 42 free-ranging harbour seals captured and sampled on-site in multiple locations in BC and Washington State (USA). Toxic Equivalency Quotients (TEQs) were calculated for polychlorinated biphenyl, polychlorinated dibenzo-p-dioxin, and polychlorinated dibenzofuran residues measured in blubber from a subset of study animals (n=30). CYP1A data from the seal pups held temporarily in captivity show that CYP1A protein levels were greater in liver than skin and that CYP1A protein and EROD activity were correlated in skin and liver. However, analysis of free-ranging seals from different sites revealed that blubber organochlorine TEQ values did not correlate with skin CYP1A levels. CYP1A protein levels and EROD activities in skin of seal pups from the BC locations and from Puget Sound were relatively low, possibly reflecting contaminant levels that were not high enough to elicit a response, a small sample size, or methodological limitations. Our results show that CYP1A measurements in skin show promise as a biomarker of contaminant exposure, but that refinements to techniques and a larger sample size are needed.     

Timing of puberty and synchronization of seasonal rhythms by simulated natural photoperiods in female Siberian hamsters

The timing of puberty is a critical life history trait of short-lived species; spring-born individuals mature rapidly and breed in the season of birth, whereas young born in mid- to late summer delay puberty until the next spring. The cues that govern the transition from rapid to delayed maturation in natural populations remain unknown. To identify ecologically relevant photoperiod cues that control timing of puberty, we monitored nine cohorts of female Siberian hamsters (Phodopus sungorus) born every 2 wk from 4 wk before to 12 wk after the summer solstice in a simulated natural photoperiod (SNP). Hamsters born by the summer solstice underwent rapid somatic growth and achieved puberty that summer; among females born 2-4 wk after the solstice, some delayed puberty by many weeks, whereas others manifested early puberty. Hamsters born 6 or more weeks after the solstice generally delayed puberty until the following spring. The transition from accelerated to delayed pubertal development in the SNP occurred at day lengths that induce early puberty when presented as static photoperiods. Despite differences in timing of birth and timing of puberty, fall and subsequent spring seasonal events occurred at similar calendar dates in all cohorts. We found no evidence that prenatal photoperiod history influenced postnatal development of female hamsters. Considered together with a parallel study on males, the present findings point to sex differences in responsiveness to natural photoperiod variations. In both sexes, incrementally changing photoperiods exert a strong organizing effect on seasonal rhythms.     

Separation and characterization of metallothionein in two species of seals by high performance liquid chromatography-atomic absorption spectrophotometry

Metallothionein (MT) was separated from the livers of two species of seals, ribbon seal (Histriophoca fasciata) and harbour seal (Phoca vitulina), by high performance liquid chromatography--atomic absorption spectrophotometry (HPLC-AAS). Both gel permeation and anion-exchange HPLC demonstrated that MT was present as a mixture of at least two isoforms in the livers of both species of seals.     

Latitude of origin influences photoperiodic control of reproduction of deer mice (Peromyscus maniculatus)

Three subspecies of Peromyscus maniculatus originating from different latitudes were maintained from birth in light dark cycles that provided between 10 and 18 h of light per day. At 50 days of age, Chihuahua, Mexico mice (latitude of origin 27 degrees N) and South Dakota, U.S.A. mice (44 degrees N) kept in the 10L:14D photoperiod had reduced gonadal and seminal vesicle weights and a lower spermatogenic index than corresponding mice kept in a 14L:10D photoperiod. Some Chihuahua and South Dakota mice, apparently constituting nonphotoperiodic subpopulations, developed their gonads while kept in the short-day photoperiod. The critical day length for stimulation of sexual maturation was greater for mice from Manitoba, Canada (55 degrees N) than for mice from the lower latitudes. At 70 days of age, testes and seminal vesicle weights, and the spermatogenic index of Manitoba mice in the 14L:10D photoperiod, were lower than those of animals maintained in 16L:8D and 18L:6D photoperiods. Responsiveness to short day lengths was greater among adult South Dakota than adult Chihuahau mice and melatonin treatment significantly reduced testes weights of South Dakota but not of Chihuahua adult mice. Photoperiodic regulation of the reproductive system varies with latitude of origin. Differences in the critical day length necessary for stimulating development of functional reproductive activity and variations in the percent of photoperiodic animals within each subspecies, appear to contribute to latitudinal gradients in reproduction.     

Rookery through rehabilitation: Microbial community assembly in newborn harbour seals after maternal separation

Microbial community assembly remains largely unexplored in marine mammals, despite its potential importance for conservation and management. Here, neonatal microbiota assembly was studied in harbour seals (Phoca vitulina richardii) at a rehabilitation facility soon after maternal separation, through weaning, to the time of release back to their native environment. We found that the gingival and rectal communities of rehabilitated harbour seals were distinct from the microbiotas of formula and pool water, and became increasingly diverse and dissimilar over time, ultimately resembling the gingival and rectal communities of local wild harbour seals. Harbour seal microbiota assembly was compared to that of human infants, revealing the rapid emergence of host specificity and evidence of phylosymbiosis even though these harbour seals had been raised by humans. Early life prophylactic antibiotics were associated with changes in the composition of the harbour seal gingival and rectal communities and surprisingly, with transient increases in alpha diversity, perhaps because of microbiota sharing during close cohabitation with other harbour seals. Antibiotic-associated effects dissipated over time. These results suggest that while early life maternal contact may provide seeding for microbial assembly, co-housing of conspecifics during rehabilitation may help neonatal mammals achieve a healthy host-specific microbiota with features of resilience.     

Photoperiod and delayed implantation in the northern fur seal (Callorhinus ursinus)

An equation for determination of the photoperiod at any given latitude for any given date is presented and used in an analysis of reproductive timing in the northern fur seal in which there is an obligatory delay of implantation. Fur seals breeding on San Miguel Island, California (33 degrees N) displayed a mean date of parturition that was 14 days earlier (P less than 0.001) than that of the parent stock on the Pribilof Islands, Alaska (57 degrees N). Previous studies have shown that changes occur in the corpus luteum, in follicles in the ovary containing the corpus luteum, in concentrations of plasma progesterone and oestradiol-17 beta, and in the uterine lining when there is a mean photoperiod of 12.5 h/day. This photoperiod occurs at both locations at 62 days after the mean dates of parturition, and may act as a cue for the initiation of implantation in these seals.     

The 1988 and 2002 phocine distemper virus epidemics in European harbour seals

We present new and revised data for the phocine distemper virus (PDV) epidemics that resulted in the deaths of more than 23 000 harbour seals Phoca vitulina in 1988 and 30,000 in 2002. On both occasions the epidemics started at the Danish island of Anholt in central Kattegat, and subsequently spread to adjacent colonies in a stepwise fashion. However, this pattern was not maintained throughout the epidemics and new centres of infection appeared far from infected populations on some occasions: in 1988 early positive cases were observed in the Irish Sea, and in 2002 the epidemic appeared in the Dutch Wadden Sea, 6 wk after the initiation of the outbreak at Anholt Island. Since the harbour seal is a rather sedentary species, such 'jumps' in the spread among colonies suggest that another vector species could have been involved. We discussed the role of sympatric species as disease vectors, and suggested that grey seal populations could act as reservoirs for PDV if infection rates in sympatric species are lower than in harbour seals. Alternatively, grey seals could act as subclinical infected carriers of the virus between Arctic and North Sea seal populations. Mixed colonies of grey and harbour seal colonies are found at all locations where the jumps occurred. It seems likely that grey seals, which show long-distance movements, contributed to the spread among regions. The harbour seal populations along the Norwegian coast and in the Baltic escaped both epidemics, which could be due either to genetic differences among harbour seal populations or to immunity. Catastrophic events such as repeated epidemics should be accounted for in future models and management strategies of wildlife populations.     

Circulating levels of oestradiol-17beta during early pregnancy in the Alaskan fur seal showing an oestrogen surge preceding implantation

Circulating levels of estradiol-17beta during early pregnancy in the Alaskan fur seal (Callorhinus ursinus) were studied to determine whether an estrogen surge coincided with the period of blastocyst growth immediately before implantation. Blood samples were obtained from 38 adult female seals during the period of blastocyst dormancy and early postimplantation. An estrogen surge (35 pg/ml) occurred immediately before the time of blastocyst reactivation and accelerated growth leading to implantation. A prolonged period (almost 2 months to return to lowest levels of 11 pg/m1) of high estrogen concentration followed ovulation. A return to high levels was characteristic of postimplantation. It is concluded that the Alaskan fur seal, having obligatory delayed implantation, has an estrogen surge near the end of that delay period.     

Simulated natural day lengths synchronize seasonal rhythms of asynchronously born male Siberian hamsters

Photoperiodism research has relied on static day lengths and abrupt transitions between long and short days to characterize the signals that drive seasonal rhythms. To identify ecologically relevant critical day lengths and to test the extent to which naturally changing day lengths synchronize important developmental events, we monitored nine cohorts of male Siberian hamsters (Phodopus sungorus) born every 2 wk from 4 wk before to 12 wk after the summer solstice in a simulated natural photoperiod (SNP). SNP hamsters born from 4 wk before to 2 wk after the solstice underwent rapid somatic and gonadal growth; among those born 4-6 wk after the solstice, some delayed puberty by many weeks, whereas others manifested early puberty. Hamsters born eight or more weeks after the solstice failed to undergo early testicular development. The transition to delayed development occurred at long day lengths, which induce early puberty when presented as static photoperiods. The first animals to delay puberty may do so predominantly on the basis of postnatal decreases in day length, whereas in later cohorts, a comparison of postnatal day length to gestational day length may contribute to arrested development. Despite differences in timing of birth and timing of puberty, autumn gonadal regression and spring gonadal and somatic growth occurred at similar calendar dates in all cohorts. Incrementally changing photoperiods exert a strong organizing effect on seasonal rhythms by providing hamsters with a richer source of environmental timing cues than are available in simple static day lengths.     

Maximum likelihood population size estimation of harbour seals in the Dutch Wadden Sea based on a mark–recapture experiment

1. The harbour seal population Phoca vitulina in the entire Wadden Sea was severely depleted due to a virus-epizootic during 1988. A comprehensive study on the population biology and activity patterns was subsequently initiated to design a management and conservation plan. The main objective of this study was to estimate harbour seal abundance in the different regions of the Wadden Sea.
2. We investigated the potential of a mark–recapture experiment using VHF radio-tags in combination with repeated aerial surveys to estimate the number of harbour seals in the Dutch part of the Wadden Sea. The number of harbour seals hauled-out and the presence of any radio-tagged seals was monitored during seven aerial surveys of all known haul-out sites in the Dutch Wadden Sea over the 1994 breeding season.
3. A maximum likelihood (ML) estimator was developed to infer the rate of tag-loss and the size of the local prepupping population.
4. The ML estimate of the number of harbour seals in the Dutch Wadden Sea was 1536 (95% confidence limits were 1225 and 2200). The corresponding maximum proportion of seals hauled-out was 68%.
5. The use of VHF radio-tags which can be monitored from the air provides a way of correcting aerial survey counts for the proportion of harbour seals hauled-out during the surveys. Since haul-out behaviour may be influenced by local conditions, such as exposure time of sand banks, we recommend this technique be repeated in other areas of the Wadden Sea rather than using the estimates from the current study in other areas.     

Reversible reproductive control in harbour seals (Phoca vitulina) with a gonadotropin-releasing hormone agonist

Reproductive control in captive pinnipeds is an important management subject for many facilities. To date reproductive control in harbour seals (Phoca vitulina) has been achieved using anti-androgens, progestagen preparations, castration, and physical separation of the sexes. The harbour seal group at the seal station in Friedrichskoog, Germany consists of three mature females (all >10 years), one older mature male (13 years of age in 2000) and one male who reached maturity during the study (3 years of age in 2000). In 2000 the older mature male received for the first time a 3-month depot injection of a gonadotropin-releasing hormone agonist (buserelin acetetate, 9.9 mg) by subcutaneous injection. This male was subsequently given the gonadotropin-releasing hormone agonist in 2001, 2004 and 2005. The younger male reached maturity during the investigation and received burserelin for the first time in 2004 and again in 2005. No pups were born in 2001, 2002, 2005 or 2006. No reproductive control was performed in 2002 and 2003, resulting in three newborns in 2003 and 2004. Serum levels of testosterone were measured by a routine liquid chromatography coupled with mass spectometry. Pre-burserelin testosterone levels varied between 0.02 and 2.18 ng/ml. Post-burserelin levels were under the detection limit except for the first year of the investigation. No behavioural changes such as changes in social ranking and no clinical side effects were observed. This study shows that the gonadotropin-releasing hormone agonist, burserelin acetate, can be used for reversible reproductive control in harbour seals without observed side effects or detrimental behavioural changes.     

Assessing the potential impact of salmon fisheries management on the conservation status of harbour seals (Phoca vitulina) in north-east Scotland

Conservation efforts are often constrained by uncertainty over the factors driving declines in marine mammal populations. In Scotland, there is concern over the potential impact of unrecorded shooting of seals, particularly where this occurs near Special Areas of Conservation. Here, we show that the abundance of harbour seals Phoca vitulina in the Moray Firth, north-east Scotland, declined by 2–5% per annum between 1993 and 2004. Records from local salmon fisheries and aquaculture sites indicated that 66–327 harbour seals were shot each year between 1994 and 2002. Matrix models and estimates of potential biological removal indicate that this level of shooting is sufficient to explain observed declines. Nevertheless, uncertainty over the number and identity of seals shot means that other factors such as changes in food availability may be contributing. Recent conservation measures markedly reduced the recorded levels of shooting in 2003 and 2004. In 2005, a coordinated management plan was developed to protect salmon fisheries interests while minimizing impacts on local seal populations. Comprehensive monitoring of future population trends and improved regulation of culls are now required to provide more robust assessments of the impact of human persecution on harbour seal populations in the Moray Firth and in other parts of the UK.     

Earlier pupping in harbour seals,Phoca vitulina

The annual reproductive cycle of most seal species is characterized by a tight synchrony of births. Typically, timing of birth shows little inter-annual variation. Here, however we show that harbour seals Phoca vitulina from the Wadden Sea (southeast North Sea) have shortened their yearly cycle, moving parturition to earlier dates since the early 1970s. Between 1974 and 2009, the birth date of harbour seals shifted on average by −0.71 d yr⁻¹, three and a half weeks (25 days) earlier, in the Dutch part of the Wadden Sea. Pup counts available for other parts of the Wadden Sea were analysed, showing a similar shift. To elucidate potential mechanism(s) for this shift in pupping phenology, possible changes in population demography, changes in maternal life-history traits and variations in environmental conditions were examined. It was deduced that the most likely mechanism was a shortening of embryonic diapause. We hypothesize that this could have been facilitated by an improved forage base, e.g. increase of small fishes, attributable to overfishing of large predator fishes and size-selective fisheries.     

Photoperiodic regulation of reproductive development in male white-footed mice (Peromyscus leucopus) born at different phases of the breeding season

Male white-footed mice were maintained from birth in chambers equipped with latitudinal timers programmed to simulate the natural progression of daylengths at 42 degrees N latitude. Mice were born into photoperiods starting on 1 April, 15 July, 15 September or 27 October. Testes and seminal vesicles of April- and July-born mice were mature at 60 days of age; puberty was delayed by several months in animals born into the September and October photoperiods but these mice became fecund at about 3.5 months of age, independent of current photoperiod. Therefore, increasing daylengths of late winter do not appear to synchronize the reproductive development of overwintering juveniles born at different times during the previous breeding season.