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.     

Seasonal testosterone pattern in Hawaiian monk seals (Monachus schauinslandi).

Blood samples from four captive male Hawaiian monk seals were collected at intervals of one month for one year for testosterone assay. Plasma testosterone concentrations, measured by radioimmunoassay, revealed a clear seasonal pattern. The lowest mean testosterone concentration (0.09 +/- 0.04 ng ml-1) occurred in January, and the highest (1.78 +/- 0.40 ng ml-1) in June. The seasonal occurrence of births and of injuries related to mating in wild populations of Hawaiian monk seals showed a distinct association with the period of high testosterone. This study supports other data that indicate that the Hawaiian monk seal is a seasonal breeder and is reproductively active for longer than monachine seals that live in higher latitudes.     

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.     

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.     

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.     

Survey for Selected Pathogens and Evaluation of Disease Risk Factors for Endangered Hawaiian Monk Seals in the Main Hawaiian Islands

A recently reestablished and increasing population of Hawaiian monk seals in the main Hawaiian Islands (MHI) is encouraging for this endangered species. However, seals in the MHI may be exposed to a broad range of human, pet, livestock, and feral animal pathogens. Our objective was to determine the movement and foraging habitats of Hawaiian monk seals in the MHI relative to the potential exposure of seals to infectious diseases in near-shore marine habitats. We captured 18 monk seals in the MHI between January 27, 2004 and November 29, 2005, tested them for various infectious diseases, and then monitored the foraging movements of 11 of them using satellite-linked radio transmitters for the next 32–167 days. All seals tested negative for canine adenovirus, calicivirus, four morbilliviruses, phocine herpes virus, Leptospira sp., and feline and canine heartworm antigen/antibody. Six of the seals tested positive on complement fixation for Chlamydophila abortus (formerly Chlamydia psittaci). Four seals demonstrated positive titers to Sarcocystis neurona, two to Neospora caninum, and two to Toxoplasma gondii. Fecal cultures showed approximately half (n = 6) positive for E. coli 0157, no Salmonella sp., and only one with Campylobacter sp. Satellite monitored seals spent considerable time foraging, traveling, and resting in neritic waters close to human population centers, agricultural activity, and livestock ranges, and sources of land-based water runoff and sewage dispersal. Consequently, Hawaiian monk seals in the MHI may be at risk of exposure to several infectious disease agents associated with terrestrial animals that can contaminate marine habitats from runoff along drainages and that are known to cause disease in marine mammals. Further, some seals overlapped substantially in their use of coastal habitats and several moved among islands while foraging and were seen on beaches near each other. This suggests that diseased seals could infect healthy conspecifics throughout the MHI.     

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.     

Body growth in Hawaiian monk seals

Body length and axillary girth measurements of more than 600 free‐ranging Hawaiian monk seals from 1 to 20 yr old were analyzed. Comparison of fitted von Bertalanffy growth models confirmed there is no evidence of sexual dimorphism in this species. Substantial differences in growth patterns were detected among seven subpopulations representing the species entire geographic range. The age at which seals would be expected to attain a reference length of 180 cm ranged from just over 3 yr up to almost 7 yr at the various sites. Subpopulations exhibiting slower growth have previously been found to also exhibit lower age‐specific reproductive rates. Differences in growth of seals among sites likely indicate varying environmental conditions determining growth during the time periods represented in the sampled data.     

Biogeography and taxonomy of extinct and endangered monk seals illuminated by ancient DNA and skull morphology

Extinctions and declines of large marine vertebrates have major ecological impacts and are of critical concern in marine environments. The Caribbean monk seal, Monachus tropicalis, last definitively reported in 1952, was one of the few marine mammal species to become extinct in historical times. Despite its importance for understanding the evolutionary biogeography of southern phocids, the relationships of M. tropicalis to the two living species of critically endangered monk seals have not been resolved. In this study we present the first molecular data for M. tropicalis, derived from museum skins. Phylogenetic analysis of cytochrome b sequences indicates that M. tropicalis was more closely related to the Hawaiian rather than the Mediterranean monk seal. Divergence time estimation implicates the formation of the Panamanian Isthmus in the speciation of Caribbean and Hawaiian monk seals. Molecular, morphological and temporal divergence between the Mediterranean and “New World monk seals” (Hawaiian and Caribbean) is profound, equivalent to or greater than between sister genera of phocids. As a result, we classify the Caribbean and Hawaiian monk seals together in a newly erected genus, Neomonachus. The two genera of extant monk seals (Monachus and Neomonachus) represent old evolutionary lineages each represented by a single critically endangered species, both warranting continuing and concerted conservation attention and investment if they are to avoid the fate of their Caribbean relative.     

Do monk seals exert top‐down pressure in subphotic ecosystems?

Patterns of subphotic fish assemblages on seamounts in the Northwestern Hawaiian Islands were identified and compared for potential structuring influences, including the bottom-up effects of regional oceanic productivity and top-down predation pressure exerted by visiting monk seals ( Monachus schauinslandi ). Patterns in fish size, density, and biomass were evaluated at the deep extreme (350–500 m) of the seals feeding range to avoid confounding effects of diverse shallow habitats ( e.g. , coral reefs). Fish number and size were used to calculate biomass density of the seamount fish assemblages that were then compared to the independent variables of summit depth, substrate type, relief, oceanic productivity, distance to seal colonies, and seal colony population. Only the variables of distance to seal colony and seal colony population were retained in a multiple regression model that explained 31% of the variance. Despite the presence of obvious regional differences in oceanic productivity, the overall patterns in the subphotic fish assemblages are better explained by the top-down hypothesis of predation pressure from monk seals.     

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.     

Extremely low genetic diversity in the endangered Hawaiian monk seal (Monachus schauinslandi)

Hunted to near extinction in the late 19th century, the endangered and endemic Hawaiian monk seal (Monachus schauinslandi) exhibits low variation at all molecular markers tested to date. Here we confirm extreme paucity of genetic diversity, finding polymorphisms at only 8 of 154 microsatellite loci tested (143 novel species-specific loci, 10 loci from Antarctic seals, and 1 previously characterized locus). This screening revealed unprecedentedly low levels of allelic diversity and heterozygosity (A = 1.1, H(e) = 0.026). Subsequent analyses of 2409 Hawaiian monk seals at the 8 polymorphic loci provide evidence for a bottleneck (P = 0.002), but simulations indicate low genetic diversity (H(e) < 0.09) prior to recorded human influence. There is little indication of contemporary inbreeding (F(IS) = 0.018) or population structure (K = 1 population). Minimal genetic variation did not prevent partial recovery by the late 1950s and may not be driving the current population decline to approximately 1200 seals. Nonetheless, genotyping nearly every individual living during the past 25 years sets a new benchmark for low genetic diversity in an endangered species.     

Hematology and serum chemistry of the young Hawaiian monk seal (Monachus schauinslandi)

Between January 1984 and May 1987, blood samples were collected from 12 young (3- to 6-mo-old) Hawaiian monk seals (Monachus schauinslandi) that were captured in the wild and held in captivity. All samples evaluated were from clinically normal animals. Average hematologic and serum chemistry values were not remarkable for a young diving mammal. The blood and serum analyses performed established reference ranges, which can be used as indicators of health status for this endangered species.     

Movements and home ranges of monk seals in the main Hawaiian Islands

Hawaiian monk seals (Neomonachus schauinslandi) began recolonizing the main Hawaiian Islands (MHI) roughly 20 yr ago. The species’ abundance is still declining, but the subpopulation in the MHI is increasing by 6.5% per year. This difference may be due to differences in prey availability or habitat quality between the northwest (NWHI) and main Hawaiian Islands, which could be reflected in the movements and behavior of the seals. For example, foraging trip durations may be shorter in areas with higher forage quality. From 2007 to 2014 we deployed GPS phone tags on the islands of Molokai (n = 7), Kauai (n = 6), and Oahu (n = 6) to study movements and dive behavior. Foraging trips typically lasted 0.57 d (IQR: 0.34–0.83) and seals traveled 18 km (IQR: 10.2–30.5) per trip. Seals began benthic dives shortly after entering the water, with most dives to depths of 12–32 m. The median 95% and 50% kernel density isopleths for seals in the MHI were 149.2 km² and 23.2 km², respectively. The duration and distance of foraging trips in the MHI were shorter than that observed in other studies from the NWHI, suggesting that foraging habitat is currently better in the MHI.     

Estimating the carrying capacity of French Frigate Shoals for the endangered Hawaiian monk seal using Ecopath with Ecosim

The carrying capacity of the French Frigate Shoals (FFS) region for the endangered Hawaiian monk seal was appraised using an updated version of the original FFS Ecopath model ( Polovina 1984 ). Model parameters were updated using recent literature, and data from surveys of the seal population and its bottom‐associated prey. Together they produced a static mass balance model for 1998 when the prey surveys began. The Ecopath‐estimated monk seal biomass was 0.0045 t/km², which was in close agreement with the biomass calculated from monk seal field beach counts (0.0046 t/km²). Model simulations through time were done in Ecosim using the Ecopath balanced model and included fisheries data time series from 1998 to 2008. Monk seal biomass declined concurrently with decreases in benthic bottomfish biomass, which were influenced by large‐scale changes in the environment of the North Pacific. This model scenario was extended from 2010, when the last permitted fishery in the Northwestern Hawaiian Islands was closed, through to 2040, assuming a constant environmental signal. Model results for this time period did not show a recovery of monk seals that exceeded the initial 1998 model biomass levels, highlighting the importance of including environmental variability in estimates of monk seals recovery at FFS.     

REPRODUCTIVE PATTERNS OF THE HAWAIIAN MONK SEAL

We evaluated reproductive patterns of the Hawaiian monk seal ( Monachus schauinslandi ) using a combination of fitted age-specific reproductive curves and analysis of reproductive patterns of individual females. We review the difficulties inherent in the acquisition and modeling of reproductive data with emphasis on the significance of reproductive senescence to populations with dissimilar age/sex compositions. Validation of the fitted reproductive parameters was accomplished by Monte Carlo sampling of parameter distributions to compare the expected number of pups with the observed production. Although the fitted reproductive functions appear to provide an acceptable fit to the raw reproductive data, we found that the fitted curves did a poor job of predicting the actual pup production in individual years because of high variability among years. To further verify, and elaborate on, the patterns in the pooled (multi-seal, and multi-year) rates, we examined attributes of the reproductive performance of individual seals. The attributes included age of primiparity, reproductive rates computed over several age ranges, and the relationship between reproductive performance and seal longevity. Analysis of individual seal patterns reinforced the conclusion that reproductive senescence is operative in monk seal populations.     

Effects of color banding, radio tagging, and repeated handling on the condition and survival of Lapwing chicks and consequences for estimates of breeding productivity

ABSTRACT.   Color bands and radio tags are widely used to facilitate individual recognition and relocation of precocial chicks in studies of prefledging survival. However, the accuracy of data collected and subsequent estimates of survival rates rely on the assumption that such techniques do not affect the parameters under study. We compared the body condition and survival of color-banded and radio-tagged Lapwing ( Vanellus vanellus ) chicks with noncolor-banded and nonradio-tagged individuals using a 10-year dataset ( N = 3174 chicks, with 205 color banded and 700 radio tagged). Color bands did not adversely affect chicks. However, radio-tagged chicks and their untagged broodmates were handled more frequently because these broods were more readily encountered than those without a tagged member. Chicks disturbed and handled more frequently had lower body condition indices and higher mortality rates. Simulations of the impact of tagging and handling on breeding productivity under two scenarios indicated a 26% reduction in productivity in situations where nest and chick survival rates were low (as in our study), but only a 7% reduction in productivity for a simulated population with the higher levels of nest and chick survival associated with a stable population. The frequent disturbance associated with radio-tracking and recapturing chicks, rather than the attachment of a tag or physical handling of chicks, may affect body condition. Frequent handling and disturbance may affect body condition by reducing foraging time, increasing stress levels, or increasing predation risk. Because our results suggested that the negative impact of handling could last up to a week, we recommend that investigators avoid disturbance of shorebird chicks more frequently than every 8 d.     

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.     

A longitudinal and cross-sectional analysis of total body oxygen store development in nursing harbor seals (<Emphasis Type="Italic">Phoca vitulina</Emphasis>)

This study compared the efficacy of longitudinal and cross-sectional sampling regimes for detecting developmental changes in total body oxygen (TBO₂) stores that accompany behavioral development in free-ranging harbor seal pups. TBO₂ stores were estimated for pup (n = 146) and adult female (n = 20) harbor seals. Age related changes were compared between pups captured repeatedly during the lactation period (longitudinal dataset) and a second group of pups handled only once (cross-sectional dataset). At each handling, hematocrit, hemoglobin, red blood cell count, total plasma volume, blood volume, muscle myoglobin concentration, and blood and muscle oxygen stores were determined. Comparisons across age categories revealed newborn blood oxygen stores were initially elevated, declined to low values by early lactation, and increased through post-weaning. Muscle oxygen stores remained low and constant throughout lactation and only increased significantly post-weaning. Overall TBO₂ stores increased 17% during lactation, and weaned pups had TBO₂ stores that were 55% as large as those of adults. Thus, significant increases in TBO₂ stores must occur after weaning, as pups begin to forage independently. Results from the two sampling schemes did not differ, indicating that the logistically simpler cross-sectional design can be used to monitor physiological development in harbor seals.     

A comparison of four serologic assays in screening for Brucella exposure in Hawaiian monk seals

A survey for Brucella spp. antibodies was undertaken on 164 serum samples from 144 Hawaiian monk seals (Monachus schauinslandi) from the northwestern Hawaiian Islands collected between 1995 and 2002. The buffered antigen plate agglutination test (BPAT), the indirect enzyme immunoassay (I-ELISA), the competitive enzyme immunoassay (C-ELISA), and the fluorescence polarization assay (FPA) were compared with regard to their ability in detecting antibodies to Brucella spp. in the serum samples. Overall, antibodies were detected in 28 (17.1%) animals, using the BPAT test, 25 (15.2%) by the C-ELISA, and 19 (11.6%) in the I-ELISA and the FPA test, using thresholds established for cattle. No evidence of gross pathology consistent with clinical brucellosis was noted in any of the seropositive animals tested. Although further work would be necessary to validate these tests for use with monk seals it appears that both the C-ELISA and the FPA tests would be appropriate as diagnostic screening tests for detection of antibodies to Brucella spp. in this species.