ANNUAL REPRODUCTIVE CYCLE OF THE FEMALE HAWAIIAN MONK SEAL (MONACHUS SCHAUINSLANDI)

Abstract: The annual reproductive cycle is described for the adult female Hawaiian monk seal ( Monachus schauinslandi ) from data collected at Laysan Island (1982–1991) and Lisianski Island (1982–1983) in the Northwestern Hawaiian Islands. Pupping, lactation, weaning, and molting were directly observed, while mating was rarely observed and was, therefore, inferred from the occurrence of mounting injuries and from adult male and female association patterns. Pooled birth rates during the study period were 0.544 for all adult-sized females and 0.675 for females parous in earlier years. For parturient females, pupping peaked in late March and early April, weaning in May, mounting injuries in May and June, and molting in July. For non-parturient females, the median mounting injury and molting dates occurred 17 and 28 days earlier, respectively. Pupping date set the timing of subsequent events in the annual cycle, but the timing of those events was adjusted by loss of the pup or poor physical condition of the female. Individual pupping patterns varied widely. The mean interval for births in consecutive years was 381 days; females that pupped in consecutive years gave birth later each season. Conversely, females who skipped a year or more gave birth earlier their next pupping season.     

EFFECTS OF RESEARCH HANDLING ON THE ENDANGERED HAWAIIAN MONK SEAL

We examined the effects of research handling on free-ranging endangered Hawaiian monk seals, Monachus schauinslandi , by analyzing differences in subsequent year survival, migration, and condition between handled seals and controls during 1983–1998. Each of 549 handled seals was matched to a control seal of the same age, sex, location, and year. Handling included instrumentation with tel metry devices ( n = 93), blood sampling ( n = 19), and tagging ( n = 437). No significant differences were found between handled seals and their controls in one-year resighting rates, observed migration rates, or condition. Resighting rates of handled and control seals were high (80%-100%). Available sample sizes were sufficient to detect reasonably small (9%-20%) differences in resighting rates had they existed among instrumented or tagged seals and controls (α= 0.05, power = 0.90). Too few seals were captured for blood sampling to detect even large differences in their resighting rates. However, blood samples were drawn from most instrumented seals, and there was no indication that this larger group suffered harmful effects. Duration of restraint during flipper tagging had no effect on subsequent probability of resighting. Our analysis suggests that conservative selection procedures and careful handling techniques have no deleterious effects on Hawaiian monk seals.     

A COPROLOGICAL SURVEY OF HELMINTH PARASITES OF THE HAWAIIAN MONK SEAL FROM THE NORTHWESTERN HAWAIIAN ISLANDS

In conjunction with an Hawaiian monk seal, Monachus schauinslandi , breeding enhancement program, fecal samples were examined for the presence of helminth parasite products (eggs, larvae, and proglottids). Eighty-two samples were examined from four island groups in the northwestern Hawaiian Islands: 38 from Kure Atoll, 32 from French Frigate Shoals, 11 from Laysan Island, and one from Lisianski Island. Identified helminth products include those of Diphyllobothrium sp., D. cameroni, Contracaecum turgidum, Anisakis sp., Corynosoma rauschi , and Trematoda. In addition, eggs from Halarachne laysanae (Atari) were found in 3 samples. Eggs of C. turgidum were present in the highest percentage (>64%) of samples from all locations. Eggs of Anisakis sp. and Trematoda are reported from this host for the first time.     

SURVIVAL RATES FOR THE HAWAIIAN MONK SEAL (MONACHUS SCHAUINSLANDI)

Abstract: Endangered Hawaiian monk seal ( Monachs schauinslandi ) pups at all the major breeding islands in the Northwestern Hawaiian Islands have been tagged since the early 1980s. Pups were double flipper tagged as soon as possible post-weaning. With few exceptions, an extensive tag resighting effort was conducted annually at the same islands. These resighting data were used to estimate seal survival rates from the time of tagging to age one at all locations using the ratio of seals alive in the second year to number of pups tagged. These survival rates among the islands, from weaning to age one, averaged over the years of the study, ranged from 0.80 to 0.90. For young seals over age one, capture-recapture methods were used to calculate survival pooled through several years, and these rates ranged from 0.85 to 0.98. At French Frigate Shoals and Laysan Island, the higher numbers of tagged pups allowed separate estimates of male and female survival to be calculated. These rates suggested that survival of immature females was better than males. Beginning in 1989, survival of immature seals at French Frigate Shoals declined sharply.     

ANALYSIS OF CORPORA LUTEA TO ESTIMATE REPRODUCTIVE CYCLES OF WILD HAWAIIAN MONK SEALS (MONACHUS SCHAUINSLANDI)

Ovaries from 14 female Hawaiian monk seals, O-24 yr of age, collected from the northwestern Hawaiian Islands were analyzed by gross and histological examination for the presence of corpora hemorrhagica (CH), lutea (CL), albicantia (CA), and dominant follicles. Seven seals, 5-24 yr of age, were mature females, and another seven seals, O-5 yr of age, were immature based on the presence or absence of CL and CA in the ovaries. Two 5-yr-old seals did not have CL and CA, but one J-yr-old and both 6-yr-old seals had CL or CA. In addition, the weight of the more active ovary increased at 5 yr of age, indicating that puberty in these female Hawaiian monk seals occurred about 5 yr of age. The total number of CL and CA was significantly correlated to the ovarian weight, but not age of the seals, indicating that visible CA of Hawaiian monk seals probably degenerate within a year. If an ovulation resulted in pregnancy, we assumed that the resulting CL from that pregnancy persisted throughout gestation and regressed approximately 2 yr after ovulation. However, the CL of pregnancy were not easily differentiated from cyclic CL that did not result in pregnancy. Four of seven mature seals were clearly polyestrous from the analyses of their ovaries and reproductive histories. The remaining three seals were pregnant in previous consecutive years, and we could not positively determine whether they were also polyestrous. The ovaries from Hawaiian monk seals had unusually large, rounded granular cells containing the aging pigment, lipofuscin. These cells were located between loose fibrous tissues in all regressing CL and CA but were not present in any CH.     

USE OF DISCOVERY CURVES TO ASSESS ABUNDANCE OF HAWAIIAN MONK SEALS

We investigated the pattern of first sighting of individual seals over the course of a field season, or the "discovery curve," as a means for estimating abundance of the endangered Hawaiian monk seal, Monachus schauinslandi . We empirically derived a criterion to determine whether or not total enumeration had been accomplished at a given site and year. When greater than 100-h field effort was expended without a new individual being identified, we concluded that total enumeration was likely achieved. To evaluate the potential for estimating abundance through extrapolation of nonlinear asymptotic functions fitted to discovery curves, we conducted simulations under a range of capture probability scenarios, including some based on observed individual variability in monk seal sighting frequencies. We demonstrated that if capture heterogeneity existed among individuals, the fitted asymptotes tended to yield biased estimates of abundance. Moreover, the levels of bias and uncertainty tended to increase inversely with the proportion of the population identified. While extrapolation shows little promise for generating unbiased abundance estimates, discovery curves have practical appeal for determining whether total enumeration has been achieved, and for optimizing field effort allocation. This is especially true for relatively small, closed populations of marked individuals.     

BODY SIZE,SURVIVAL, AND DECLINE OF JUVENILE HAWAIIAN MONK SEALS,MONACHUS SCHAUINSLANDI

In the mid 1980s half of the entire Hawaiian monk seal species was located at French Frigate Shoals, and this colony may have reached environmental carrying capacity. Since 1989 this colony has declined by 55%, primarily from poor juvenile survival. Only 8%–25% of weaned pups have survived to age 2 during this period, compared to at least 80% between 1984 and 1987. We characterize (1) this drop in survival, (2) a strong, but variable, correlation between survival and size at weaning, (3) interisland differences in size from weaning to age 2 in 1991 through 1993, and (4) decadal-scale changes in mean measures of size at weaning. We compare observations at French Frigate Shoals with the colony at Laysan Island where abundance is well below historical levels and was therefore expected to be below carrying capacity. At Laysan Island juvenile survival has also been poor (30%-70%), and the size of weaned pups has decreased during the past decade. Our hypothesis is that poor survival may be due to reduced prey availability at both sites, but particularly at French Frigate Shoals. Evidence to support this hypothesis includes a large increase in total abundance at French Frigate Shoals; reduced size of weaned pups; decreased survival, emaciation, and slower growth rates of juvenile seals; and declining primary productivity. Regardless of cause, the immediate consequences at French Frigate Shoals and Laysan Island, and for the species overall, will likely be poor recruitment and productivity. Because the decline is still in progress, the ultimate consequences for the species' viability are of great concern in light of its already low abundance.     

IDENTIFYING DIURNAL FORAGING HABITAT OF ENDANGERED HAWAIIAN MONK SEALS USING A SEAL-MOUNTED VIDEO CAMERA

The Hawaiian monk seal ( Monachus schauinslandi ) is thought to be a foraging generalist, preying on numerous species in diverse habitats of the subtropical Northwestern Hawaiian Islands. At the atoll of French Frigate Shoals, recent evidence of emaciation and low survival in monk seals prompted a search for their specific prey communities and foraging habitat.
A video camera (National Geographic Television's CRITTERCAM) fitted to 24 adult male seals documented benthic and demersal foraging on the deep slopes (50-80 m) of the atoll and neighboring banks. The number of bottom searches for prey was compared by year, time of day, type of bottom, individual seal, and length of bottom time. Analysis of variance identified a significant interaction of seal and bottom type, explaining 65% of the total variance. Seals fed on communities of cryptic fauna (fish and large invertebrates) in transitional "ecotone" regions of low relief where consolidated substrate, rubble, and talus bordered areas of sand. Independent areal surveys of bottom types throughout the atoll and neighboring banks suggest that the type of bottom selected as foraging habitat represents a relatively small percentage of the total benthic area available.     

REPRODUCTIVE CYCLE OF THE FEMALE MEDITERRANEAN MONK SEAL IN THE WESTERN SAHARA

Mediterranean monk seals at Cap Blanc, western Sahara, pup annually throughout the year, although births are more frequent in autumn (October). Consequently, subsequent events of the cycle are not seasonal. This lack of synchronicity in reproduction can be attributed to the subtropical location of the colony and the presence of a semipermanent upwelling in the area. This contrasts with the consistency in the timing of parturition of individual females, which results in an interbirth period of one year, which varies by a maximum of only 15 d. The duration of lactation, which can last up to five months, correlates with that of the interbirth period. The interbirth and "molt-to-parturition" periods are relatively constant, and the only part of the cycle that appears to compensate for variation in lactation length is the "weaning-to-molt" period, which correlates negatively with the duration of lactation. As a result of the long lactation period, esrrus probably does not occur at the end of weaning, as it does in most other phocids.     

CONCENTRATIONS OF ESTRONE SULFATE and PROGESTERONE IN PLASMA and SALIVA, VAGINAL CYTOLOGY, and BIOELECTRIC IMPEDANCE DURING THE ESTROUS CYCLE OF THE HAWAIIAN MONK SEAL (MONACHUS SCHAUNSLAnDI)

Blood and saliva samples, vaginal swabs, and bioelectric impedance measurements were collected 1–3 times per week from a captive adult female Hawaiian monk seal ( Monacbus schauinslandi ) during the spring and summer of 1991. During 1992 saliva only was collected on average 4 times weekly. Concentrations of progesterone and estrone sulfate, and the periodic appearance of cornified epithelial cells from the vagina indicated consecutive estrous cycles ranging 35 ± 3 days in duration. Progesterone concentrations in plasma and saliva had a correlation of 0.868, while estrone sulfate had a correlation of 0.982. Bioimpedance of the whole seal body resulted in a pattern similar to the estrone sulfate concentrations, but shifted forward by 2 d. Bioimpedance of the upper vaginal tissues paralleled the estrone sulfate pattern while the bioimpedance of the lower reproductive tract fluctuated without a distinct pattern. The luteal phase ranged 17–20 d and the follicular phase was 15–18 d in length. These results indicate that: (1) the Hawaiian monk seal, in captivity, is a polyestrous seal, in contrast to other phocid seals that have been studied; (2) salivary concentrations of estrogen and progesterone may provide an accurate, less-invasive method of monitoring reproductive hormones in captive Hawaiian monk seals; and (3) vaginal cytology and bioelectric impedance reflect physiological changes associated with the estrous cycle.     

MORPHOMETRY, HEMATOLOGY, AND SERUM CHEMISTRY IN THE HAWAIIAN MONK SEAL (MONACHUS SCHAUINSLANDI)

We studied morphometric, hematology, and serum chemistry variables in 140 Hawaiian monk seals ( Monachus schauinslandi ) to establish normal baseline values for these variables among free-living seals. We compared seals at French Frigate Shoals (FFS), Midway Atoll (MID), and Pearl and Hermes Reef (PHR) because these subpopulations differ in their rates of population recovery. Dorsal standard length and axillary girth differed significantly between immature (1–4 yr old) and adult (≥5 yr old) seals among sex and island subgroups. Immature seals at FFS were shorter than those at MID and PHR; adult seals at FFS had smaller dorsal standard lengths and axillary girths compared to the other subpopulations. The differences in size were more pronounced among adult females. Significant differences were also found for hematology and serum chemistry variables among seals at FFS, MID, and PHR. Monk seals at FFS had an absolute lymphopenia and eosinopenia compared to those at MID and PHR, compatible with a stress response. Seals at FFS also had lower blood urea nitrogen than seals at PHR, and a lower plasma potassium than seals at MID or PHR. Monk seals had an absolute and relative eosinophilia compared to previously published values. Analysis of subpopulation differences is useful for population health assessment and for long-term monitoring of an endangered species.     

IMPROVED BODY CONDITION OF WEANED HAWAIIAN MONK SEAL PUPS ASSOCIATED WITH EL Niño EVENTS: POTENTIAL BENEFITS TO AN ENDANGERED SPECIES

Efforts to enhance recovery of endangered Hawaiian monk seals ( Monachus schauinslandi ) require an understanding of factors influencing population dynamics. This study examines relationships between body condition and survival of monk seal pups at French Frigate Shoals and Laysan Island and El Niño events. Girth measurements and mass estimates were used as indicators of pup body condition, and survival was evaluated from weaning to age 2. Linear models and logistic regression analysis were used to evaluate El Niño effects. Temporal trends in mean girth, mass, and survival were identified at both study sites. After accounting for temporal trends, girths were 3.7 cm and 2.7 cm greater during El Niño years at French Frigate Shoals and Laysan Island, respectively. Average mass estimates were significantly greater during El Niño years at French Frigate Shoals (2.6 kg increase), but were not significantly different at Laysan Island (1.8 kg increase). Weaned pups born at French Frigate Shoals during El Niño years survived significantly better, but this effect was not detected at Laysan Island. El Niño events probably affect pup condition and survival, but these parameters need to be monitored during future El Niño events to clarify these relationships.     

HAWAIIAN MONK SEALS (MONACHUS SCHAUINSLANDI) FORAGING IN DEEP-WATER CORAL BEDS

Plans to harvest deep-water corals in the remote Northwestern Hawaiian Islands, close to populations of endangered Hawaiian monk seals ( Monachus schauinslandi ), have raised concerns about the seals' use of deep-water habitats. Movements and diving patterns of seals studied at French Frigate Shoals (FFS) Atoll indicated two areas where five males out of 33 instrumented seals dove deep enough (300–500 m) to encounter commercially sought deep-water corals. Submarine surveys conducted at each location found beds of gold ( Gerurdia sp.) and pink ( Corallium sp.) precious coral suggesting an overlap between the foraging habitat of some seals and the target of the coral fishery. Areas adjacent to the coral beds that were visually censused using submersibles showed significantly fewer precious corals. Precious coral beds were not found on previous submarine surveys at other regions around FFS, supporting the notion that seals were selecting the areas with corals as forage habitat. Five male seals were fitted with back-mounted video cameras to document feeding among precious corals. None of the five seals dove deep enough to encounter precious corals (>300 m). However, three of the seals visited beds of black coral ( Cirrhipdhes sp.) at shallower depths (∼ 80 m). One seal was observed revisiting the black coral beds on three successive nights to feed on fish hiding among the coral stems.     

Dramatic shifts in Hawaiian monk seal distribution predicted from divergent regional trends

Total estimated abundance of Hawaiian monk seals was just 1,161 individuals in 2008 and this number is decreasing. Most monk seals reside in the remote Northwestern Hawaiian Islands (NWHI) where the decline is approximately 4%/yr, whereas relatively fewer seals currently occupy the main Hawaiian Islands (MHI). It is widely accepted that the MHI population is increasing, although there are no formal estimates of total abundance, population growth rate or vital rates. This lack of information has hampered efforts to anticipate future scenarios and plan conservation measures. We present the first estimates of MHI monk seal survival and age‐specific reproductive rates. Using these rates, a conservative estimate of current MHI abundance and a previously published stochastic simulation model, we estimate the MHI population growth rate and projected abundance trend. Analogous estimates for the NWHI are derived from a much richer data set. Estimated survival from weaning to age 1 yr is 77% in the MHI, much higher than recent NWHI estimates ranging from 42% to 57%. Moreover, MHI females begin reproducing at a younger age and attain higher birth rates than observed in the NWHI. The estimated MHI intrinsic rate of population growth is 1.07 compared to a 0.89–0.96 range in the NWHI. Assuming an initial abundance of 152 animals in the MHI, projections indicate that if current demographic trends continue, abundance in the NWHI and MHI will equalize in approximately 15 yr. These results underscore the imperative to mitigate the NWHI decline while devoting conservation efforts to foster population growth in the MHI, where documented threats including fishery interactions, direct killing, and disease could rapidly undo the current fragile positive trend.     

FORAGING OF JUVENILE MONK SEALS AT FRENCH FRIGATE SHOALS, HAWAII

Emaciation and poor survivorship of juvenile Hawaiian monk seals at French Frigate Shoals atoll prompted a study of their foraging, using video camera technology ( crittercam ). Nine juveniles between the ages of 1 and 3 yr (six males, three females) were fitted with crittercam to identify their foraging habitat and feeding behavior. All feeding was directed at small (≤ 10 cm), cryptic, benthic prey. Older seals (ages 2 and 3), varied in their foraging intensity with most of their attention directed at shallow atoll depths (10–30 m). In contrast, the three yearlings focused all their feeding in the sand fields (50–100 m) on the atoll's outer slope. Bottom trawls were used to assess the prey abundance of the sand habitat and found 70% of the numerical catch was flounder ( Bothidae ). Extrapolating the yearlings' prey capture rate (0.13/min, derived from the crittercam video) over their total bottom time yielded an estimated 1–1.3 kg/day of flounder. The mean size of flounder (5 ± 1.7 cm) caught in the bottom trawls was close to the size at which larval flounder settle from the plankton (3 cm), suggesting that localized changes in oceanography could directly impact the seals' prey supply. Extensive use of sand communities by young seals may be the strongest link yet identified between juvenile survivorship and oceanographic dynamics.     

PUPPING HABITAT USE IN THE MEDITERRANEAN MONK SEAL: A LONG-TERM STUDY

The Mediterranean monk seal gives birth almost exclusively in coastal caves. Given its critical conservation status, the identification and protection of such sites is important for the survival of the species. From 1990 to 2004 we collected data on physical and environmental variables and monitored pupping events in thirty-four coastal caves in Greece. We modeled the probability of cave occupancy as a function of the properties of each cave. Model selection and model averaging enabled us to rank the variables that influenced use of potential pupping sites. Environmental variables related to cave seclusion, substrate, and degree of protection from wind and wave action were the most important among them. The relative importance and directions of these relationships confirm the long-standing assumption that Mediterranean monk seals require sheltered pupping sites, far from sources of human disturbance and thus are progressively limited to isolated parts of the country's coastline. We used cross-validation to examine the predictive ability of our analysis and quantified the sensitivity of our predictions to the degree of extrapolation. We conclude that, although more data are required, the model is capable of predicting occupancy for caves close to the middle of the environmental space examined in this study.     

DIVING DEVELOPMENT AND BEHAVIOR OF A REHABILITATED MEDITERRANEAN MONK SEAL (MONACHUS MONACHUS)

Among the priority actions identified for saving the critically endangered Mediterranean monk seal are gaining basic biological information on movements and behavior, and rescuing and rehabilitating wounded, stranded, and orphaned pups. On 22 May 2004 a rehabilitated monk seal juvenile was fitted with a satellite tag, released in the National Marine Park of Alonnisos, Northern Sporades, Greece, and monitored for 167 d. Postrelease, the seal remained close to the islands of the park and within the 200-m isobath. Throughout the monitoring period, the seal reduced time hauled out, while 95-percentile dive duration and depth gradually increased. The overall maximum depth of 123 m recorded in this study is the greatest depth ever recorded for the species. These results confirm the effectiveness of the rehabilitation program carried out on the particular animal and provide additional support for the continuation of the rehabilitation program as a conservation measure for the species. We demonstrate that satellite tracking of rehabilitated seals is a valuable research and conservation tool, even for a species that commonly uses shoreline caves for resting, molting, and parturition.     

NEW INFORMATION ON THE NATURAL HISTORY,DISTRIBUTION, AND SKULL SIZE OF THE EXTINCT (?) WEST INDIAN MONK SEAL,MONACHUS TROPICALIS

Our knowledge of the extinct West Indian monk seal, Monachus tropicalis , is scant due to heavy exploitation following European colonization of the New World. We present previously unknown accounts of the species, including unpublished field notes of biologist E. W. Nelson, who observed a small number of wild seals in June of 1900. Records indicate that M. tropicalis may have had a long pupping season, occurred in large groups (up to 100) when abundant, probably ate fish and crustaceans, were preyed upon by sharks, and that young and adult seals may have assorted themselves into different age groups when hauled out. Additional records extend the known range of M. tropicalis to include the north coast of South America as far east as Guyana. We also present previously unavailable measurements from a large series of adult skulls and mandibles ( n = 48). Two cases of histocytosis X, carcinoma, or other disease of the hard palate are documented from among these specimens.     

PUP SURVIVAL IN THE MEDITERRANEAN MONK SEAL (MONACHUS MONACHUS) COLONY AT CABO BLANCO PENINSULA (WESTERN SAHARA-MAURITANIA)

We surveyed pup survival in Mediterranean monk seals ( Monachus monachus ), at Cabo Blanco Peninsula (Western Sahara-Mauritania) colony from May 1993 to December 1997. This species breeds and hauls out on beaches inside two main caves. During the study period we detected a total of 93 pups that died or disappeared. The survival rate of 84 pups through the age of first moult (approximately two months) was 0.47. This value is similar to those reported for other pinnipeds breeding in caves but lower than for those breeding on open beaches. Mortality varied seasonally and appeared to increase as a result of storms, large ocean swells, and high tides. Mother-pup pair separation (and resulting pup starvation) and physical injury caused by impact against the rock walls of the cave and cliffs were established as the causes of most deaths. Beach surface area inside the caves also appeared to be a mediating factor in the effects of sea conditions. High pup mortality may be a limiting growth factor in this population, although cave dwelling protects the population from predators and human disturbance.     

Sighting patterns reveal unobserved pupping events to revise reproductive rate estimates for Hawaiian monk seals in the main Hawaiian Islands

We used sighting reports, including decades of citizen-reported Hawaiian monk seal (Neomonachus schauinslandi) sightings, to describe female breeding biology and reproductive success in the main Hawaiian Islands. We first used this data set to describe the timing of events in the female reproductive cycle. We then conducted an expert review of patterns in sighting histories to detect unobserved pupping events. Finally, we estimated the age-specific reproductive curve for female monk seals in the main Hawaiian Islands. Charting reproductive cycles showed indications of the robust condition of female monk seals in the main Hawaiian Islands; they nursed pups 12% longer than their counterparts in the Northwestern Hawaiian Islands and regained condition to molt more quickly after weaning a pup. By examining sighting histories, we were able to infer 25 unobserved pupping events that had previously gone uncounted. We accounted for additional uncertainty with a randomization procedure. After accounting for unobserved pupping events, the age-specific reproductive rate of main Hawaiian Islands monk seals exceeded 0.70 for prime aged females (8–18 years). This is the highest reproductive rate reported for any of the Hawaiian monk seal breeding sites, illustrating the important role of the main Hawaiian Islands population in Hawaiian monk seal recovery.