Adaptation of sea turtles to climate warming: Will phenological responses be sufficient to counteract changes in reproductive output?

Sea turtles are vulnerable to climate change since their reproductive output is influenced by incubating temperatures, with warmer temperatures causing lower hatching success and increased feminization of embryos. Their ability to cope with projected increases in ambient temperatures will depend on their capacity to adapt to shifts in climatic regimes. Here, we assessed the extent to which phenological shifts could mitigate impacts from increases in ambient temperatures (from 1.5 to 3°C in air temperatures and from 1.4 to 2.3°C in sea surface temperatures by 2100 at our sites) on four species of sea turtles, under a "middle of the road" scenario (SSP2-4.5). Sand temperatures at sea turtle nesting sites are projected to increase from 0.58 to 4.17°C by 2100 and expected shifts in nesting of 26-43 days earlier will not be sufficient to maintain current incubation temperatures at 7 (29%) of our sites, hatching success rates at 10 (42%) of our sites, with current trends in hatchling sex ratio being able to be maintained at half of the sites. We also calculated the phenological shifts that would be required (both backward for an earlier shift in nesting and forward for a later shift) to keep up with present-day incubation temperatures, hatching success rates, and sex ratios. The required shifts backward in nesting for incubation temperatures ranged from -20 to -191 days, whereas the required shifts forward ranged from +54 to +180 days. However, for half of the sites, no matter the shift the median incubation temperature will always be warmer than the 75th percentile of current ranges. Given that phenological shifts will not be able to ameliorate predicted changes in temperature, hatching success and sex ratio at most sites, turtles may need to use other adaptive responses and/or there is the need to enhance sea turtle resilience to climate warming.

Persistence of maternal antibodies against Mycoplasma agassizii in desert tortoise hatchlings.

OBJECTIVE: To investigate Mycoplasma agassizii-specific maternal antibodies in desert tortoise (Gopherus agassizii) hatchlings. SAMPLE POPULATION: Plasma from 43 captive-reared desert tortoise hatchlings. PROCEDURE: ELISA for M agassizii-specific antibodies was performed. Four hatchlings from 4 clutches of 3 M agassizii-seropositive females with chronic upper respiratory tract disease (URTD) were tested on the day of hatching (set 1), and 20 hatchlings from 4 clutches of 4 M agassizii-seropositive females with URTD and 19 hatchlings from 4 M agassizii-seronegative healthy females were tested at 4, 8, 12, and 29 months old (set 2). Immunoblot analysis was performed to determine immunoglobulin classes in yolk and plasma of hatchlings. To determine infection status of hatchlings, yolk, egg shell membranes (set 1), and nasal lavage fluid (sets 1 and 2) were examined for M agassizii by use of polymerase chain reaction. RESULTS: Yolk and hatchling plasma had significantly lower amounts of specific antibodies than did plasma from adult females. The IgG and IgM antibodies were transferred, but M agassizii-specific antibodies were of the IgG class. Hatchlings were not infected with mycoplasmas. Offspring of sick females had significantly higher specific antibody titers than did offspring of healthy females. Titers were still significantly different in 1-year-old hatchlings. CONCLUSIONS: Desert tortoise females transfer specific IgG and IgM antibodies to their offspring that are still detectable after 1 year. CLINICAL RELEVANCE: Infection with M agassizii may be misdiagnosed in hatchlings with persistent maternal antibodies. Passively acquired antibodies may have a role in pathogenesis of mycoplasma-induced respiratory tract disease and other diseases.

Sex differences in plasma corticosterone in desert tortoises, Gopherus agassizii, during the reproductive cycle.

Blood samples from 30 female and 20 male adult desert tortoises, Gopherus agassizii, were collected at monthly intervals during the annual reproductive cycle (April to October). Plasma corticosterone and the sex steroids in each of the samples were analyzed by radioimmunoassay. Mean corticosterone levels in males were significantly higher than in females (P < 0.001) in every month. Male tortoises showed a marked seasonal pattern in plasma corticosterone with a highly significant peak in July, August, September, and October that corresponded with a similar peak in plasma testosterone. Testosterone and corticosterone in the male showed a highly significant correlation (P < 0.0001). The pattern of corticosterone in the female was less marked, with a significant peak in May during the mating and nesting season, but no association with the peak in estradiol in late summer was apparent. The highest levels of corticosterone in the males were associated with the peak in spermatogenesis and intense male-male combat. These results support similar data from other reptiles that suggest increased glucocorticoid secretion during periods of increased activity and metabolism.

Seasonality of adult male Japanese macaques (Macaca fuscata): androgens and behavior in a confined troop.

Seasonal variations in levels of serum testosterone, dihydrotestosterone (DHT), reproductive behavior, and social behavior were investigated in 12 adult males (5 to 20+ years of age) of the Oregon troop of Japanese macaques (Macaca fuscata). Blood samples were collected at 2- to 4-month intervals, and behaviors were monitored twice weekly over a 15-month period. Significant seasonal variations in levels of testosterone and DHT, and in frequencies of mount series, ejaculations, number of female partners, displays, courtship, and aggression were observed. Seasonal variations in reproductive and social behaviors did not correlate with seasonal variations in androgen levels because seasonal increases in these behaviors followed seasonal increases in the androgens with a 1- to 2-month delay. However, significant correlations between increased androgen levels and the onset of mating activity occur when mean monthly frequencies of mount series are shifted 1 to 2 months earlier to coincide with the rise in serum androgen levels. The frequency of adult male play and male-male mounting increased significantly when androgen levels were low. We suggest that photoperiod changes may function as a proximate cue in male Japanese macaques which induces a state of biological readiness for mating, and the behavioral consequences (i.e., mating) are then dependent upon the presence of receptive females.

The effects of used motor oil, silt, and the water mold Saprolegnia parasitica on the growth and survival of mole salamanders (genus Ambystoma).

Amphibians appear to be declining worldwide. One cause of their decline may be used crankcase oil which leaks from motor vehicles and washes into ponds. Once in ponds, the oil may either be directly toxic to amphibians, or may indirectly affect them by disrupting food chains. The effects of oil may also be compounded by naturally occurring materials in the water column such as silt. Silt may interfere with respiration across gill surfaces. This study examined the effects of oil and silt on the growth and metamorphosis of larval mole salamanders, Ambystoma opacum and A. tigrinum tigrinum. In Experiment One it examined ponds with and without silty water and oil pollution to determine their suitability as habitats for salamander larvae. In Experiment Two it studied the effects of low levels of oil combined with silt on animals raised in the laboratory and fed prey items not raised in oil. In Experiment Three, it explored the effects of oil at an ecosystem level by raising the salamanders in the field in plastic micromesocosms that mimicked small ponds. Finally, in Experiment Four, in the laboratory, it examined the short-term survival of salamanders in high concentrations of oil. This study found that ponds containing oil and silt produce salamanders of reduced size and weight. Furthermore, while salamanders are relatively robust to the short term effects of large concentrations of used motor oil, oil has deleterious effects on the community and therefore exerts an indirect negative effect on salamanders. In the mi- cro-mesocosms containing oil, salamanders were smaller and weighed less than animals not raised in oil. Furthermore, silt results in reduced growth, earlier metamorphosis, and increased susceptibility to the water mold Saprolegnia parasitica.

Estrogen induction of plasma vitellogenin in the Kemp's ridley sea turtle (Lepidochelys kempi).

Estrogen stimulation of the production of teh yolk protein precursor vitellogenin was demonstrated in immature Kemp's ridley sea turtles. 17beta-Estradiol injection elicited an increase in serum estrogen, protein, protein phosphorus, and total calcium within 7 days. Associated with these changes was the appearance of a single, dimethylformamide-precipitable, 205-kDa estradiol-induced serum protein, which became the predominant serum protein identified by polyacrylamide gel electrophoresis. The effects of estradiol injection were maintained for 3 months following termination of estradiol administration, despite a decline in serum estrogen levels. Although studies in other species have indicated that changes in circulating vitellogenin levels can influence thyroid hormone transport, no changes were observed throughout the study in total blood levels of thyroxine or triiodothyronine or protein binding of these hormones. We conclude that in the immature Kemp's ridley estrogen induces the synthesis and secretion of a vitellogenin which resembles that of other reptiles, but which does not influence thyroid hormone transport. The prolonged presence of vitellogenin in the blood may be due to a lack of an active ovarian uptake mechanism in these immature animals.

Seasonality in plasma thyroxine in the desert tortoise, Gopherus agassizii.

To characterize seasonal changes in thyroid function in a terrestrial reptile, thyroid hormones were measured over a period of 2 years in desert tortoises, Gopherus agassizii, maintained at the Desert Tortoise Conservation Center in Las Vegas, Nevada. In all samples, triiodothyronine was nondetectable (less than 0.1 ng/ml). Thyroxine (T(4)) exhibited distinct cycles in both sexes, being lowest during hibernation and rising toward the time of emergence. Females exhibited only one peak in T(4), during the early spring. In males, T(4) levels peaked in early spring and again in late summer. The desert tortoise has distinct activity patterns that include increased feeding, mating, and locomotor activity in the early spring and increased mating and combat in the late summer. In an experiment to determine whether food intake influences T(4), food was withheld for 2 weeks. Compared to continuously fed controls, T(4) declined significantly in unfed tortoises, but increased significantly within 36 h of refeeding, indicating that thyroid activity is responsive to nutrient intake. The second seasonal peak of T(4) only in males suggests that male reproductive activity in late summer is associated with thyroid activation. To evaluate this possibility, adult, subadult, and juvenile males were sampled during the months of the second seasonal peak in T(4). Although all three age groups showed similar foraging and thermoregulatory behaviors, T(4) peaked in July only in the reproductively active adults, which also exhibited significantly higher testosterone levels. Elevated T(4) in desert tortoises is thus associated with periods of increased feeding and reproductive activity, supporting a role for thyroid hormones in these energy-demanding activities.

Seasonal reproductive cycle of the Kemp's ridley sea turtle (Lepidochelys kempi).

The seasonal reproductive cycle of the Kemp's ridley sea turtle (Lepidochelys kempi) was studied under seminatural conditions at the Cayman Turtle Farm, Grand Cayman, British West Indies, from June 1987 to July 1988. Male L. kempi displayed a prenuptial rise in serum testosterone 4 to 5 months prior to the mating period (March). Male testosterone then declined sharply during the mating period. Female L. kempi also displayed a prenuptial rise in serum testosterone, estradiol, and total calcium 4 to 6 months prior to the mating period (March). Female testosterone and estradiol declined during the nesting period (April to July) immediately following the mating period (March). Elevated levels in female estradiol and total calcium corresponded with the period of vitellogenesis as determined from gel electrophoresis and ultrasonography. Serum thyroxine also fluctuated seasonally with elevated levels observed in females associated with the period of vitellogenesis. L. kempi displayed a distinct seasonal reproductive cycle in captivity. Nesting in the captive study group corresponded with nesting in the wild population at Rancho Nuevo, Mexico (April to July). Female endocrine cycles during the nesting period were similar to those observed in the wild population.

Changes in gonadal and adrenal steroid levels in the leatherback sea turtle (Dermochelys coriacea) during the nesting cycle.

The reproductive endocrinology of nesting leatherback turtles (Dermochelys coriacea) was studied during the 1996-1997 and 1997-1998 nesting seasons at Los Baulas National Park, Playa Grande, Costa Rica. Blood samples were collected from nesting females throughout the season. Females were observed to nest up to 10 times during the nesting season. Plasma steroids were measured by radioimmunoassay and total plasma calcium was measured by flame atomic absorption spectrophotometry. Plasma testosterone and plasma estradiol levels declined throughout the nesting cycle of the female. Testosterone declined from a mean of 10.18 +/- 0.77 ng/ml at the beginning of the nesting cycle to 1.73 +/- 0.34 ng/ml at the end of the nesting cycle. Estradiol declined in a similar manner, ranging from a mean of 190.95 +/- 16.80 pg/ml at the beginning of the nesting cycle to 76.52 +/- 12.66 pg/ml at the end of the nesting cycle. Plasma progesterone and total calcium levels were relatively constant throughout the nesting cycle. Lack of fluctuation of total calcium levels, ranging from a mean high of 97.46 +/- 11.37 microg/ml to a mean low of 64.85 +/- 11.20 microg/ml, further suggests that vitellogenesis is complete prior to the arrival of the female at the nesting beach. Clutch size (both yolked and yolkless eggs) did not vary over the course of the nesting cycle.