Elevated Calf Mortality and Long-Term Responses of Wild Bottlenose Dolphins to Extreme Climate Events: Impacts of Foraging Specialization and Provisioning
Title: Elevated Calf Mortality and Long-Term Responses of Wild Bottlenose Dolphins to Extreme Climate Events: Impacts of Foraging Specialization and Provisioning
As demands for wildlife tourism increase, provisioning has become a popular means of providing up-close viewing to the public. At Monkey Mia, Shark Bay, Australia, up to five adult female Indo-Pacific bottlenose dolphins ( Tursiops aduncus ) visit a 100 m stretch of beach daily to receive fish handouts. In 2011, a severe marine heatwave (MHW) devastated seagrass and fish populations in Shark Bay. Offspring survival declined precipitously among seagrass specialists (dolphins that forage disproportionately in seagrass habitat). As all provisioned dolphins at the site are seagrass specialists, we examined how provisioned and non-provisioned seagrass specialists responded to the MHW. Using 27 years of data we compare habitat use, home range size, calf mortality, and predation risk between provisioned and non-provisioned females and their offspring before and after the MHW. Our results show that provisioned females have extremely small home ranges compared to non-provisioned females, a pattern attributable to their efforts to remain near the site of fish handouts. However, weaned offspring (juveniles) born to provisioned females who are not provisioned themselves also had much smaller home ranges, suggesting a persistent maternal effect on their behavior. After the MHW, adult females increased their use of seagrass habitats, but not their home range size. Provisioned females had significantly lower calf mortality than non-provisioned females, a pattern most evident pre-MHW, and, in the first 5 years after the MHW (peri-MHW, 2011–2015), calf mortality did not significantly increase for either group. However, the ecosystem did not recover, and post-MHW (2016–2020), calf mortality was substantially higher, regardless of provisioning status. With few survivors, the impact of the MHW on juvenile mortality post-weaning is not known. However, over three decades, juvenile mortality among offspring of provisioned vs. non-provisioned females did not statistically differ. Thus, the survival benefits accrued to calves in the provisioned group likely cease after weaning. Finally, although shark attack rates on seagrass specialists did not change over time, elevated predation on calves cannot be ruled out as a cause of death post-MHW. We discuss our results as they relate to anthropogenic influences on dolphin behavioral plasticity and responses to extreme climate events. more »« less
Greenwald, Alexandra M.; Burns, Gregory R.; Eerkens, Jelmer W.; Bartelink, Eric J.; Leventhal, Alan; Arellano, Monica V.(
, American Journal of Biological Anthropology)
AbstractObjectives
The mortuary record at Middle Period siteKalawwasa Rummeytak(CA‐SCL‐134) (2600‐1225 cal BP) in California's southern Santa Clara Valley shows pronounced wealth inequality;Olivellashell bead wealth, as well as other grave goods, are concentrated in the burials of several older adult females. The concentration of wealth among women, along with regional strontium isotopic evidence of male‐biased residential shifts in early adulthood, suggests a matrilineal kinship system that practiced matrilocal post‐marital residence patterns. We suggest local resource enhancement effects incentivized keeping women in their natal communities and investing more in female offspring.
Materials and Methods
With the consent of, and in collaboration with, the Muwekma Ohlone Tribe of the San Francisco Bay Area, this paper employs isotopic analysis (δ15N andδ13C,86Sr/87Sr) to examine duration of exclusive breastfeeding, weaning age (complete cessation of breastmilk consumption), early childhood diet, and lifetime residential mobility of individuals interred atKalawwasa Rummeytakto test the assumption that the site inhabitants favored matrilocality and that female offspring received greater levels of investment in groups with female wealth/status attainment. First molars, third molars, and bone was sampled from 22 individuals.
Results
The average weaning age for females atKalawwasa Rummeytakis 36.3 months ± 9.7 (1 SD), or just over 3 years. The average weaning age for males is 31.2 ± 7.9 months (1 SD), or about 2.6 years. Infants at the site were provisioned with supplemental foods dominated by C3plants and terrestrial herbivores, as well as anadromous fish. After weaning, individuals consumed a diet dominated by acorns, C3plants, and terrestrial herbivores, with periodic inclusion of anadromous fish. 30% of the sampled population of females exhibit local first molar87Sr/86Sr values, suggesting thatKalawwasa Rummeytakis their natal community. None of the males interred at the site are locals.
Discussion
Despite the small sample size often unavoidable in archaeological contexts, we find possible female‐biased parental investment strategies. Cessation of breastfeeding (weaning) was, on average, 5 months earlier for males compared to females. There are no differences between females and males in the consumption of supplemental or post‐weaning foods. Strontium data suggest a flexible postmarital residence system that favored matrilocality. This may have incentivized greater investment in female offspring.
Dittus, Wolfgang; Baker, Anne(
, American Journal of Primatology)
Abstract
Weaning age in primates has been challenging to measure and new methods, involving molecular biomarkers in feces, tissue, or teeth have contributed to a solution. Here, we used a direct approach by briefly anesthetizing 442 female toque macaques (Macaca sinica) of Sri Lanka (over a 17‐year period) and manually testing their mammary tissue for the presence or absence of milk. Milk tests were related to known offspring ages and maternal care behaviors and indicated that older infants suckled milk well past the weaning age of 7 months that is often reported for food‐provisioned primates. Mothers strongly rejected their infants' nursing attempts in two phases, the first at 7 months as an honest signal “giving notice” promoting a shift to greater independence from milk to solid food, and when “shutting down” at final weaning after 12–18 months. The shift to supplementary lactation coincided also with the cessation of mothers carrying their infants and a resumption of cycling. All infants up to 7.2 months suckled milk, 91% of them did up to 18 months, this continued for 42% of infants beyond 18 months, and normally none received milk after 22 months. Lactation extended into 2.2% of cycling and 10.7% of pregnant females (up to 50% of gestation). The interbirth interval was prolonged by factors predicted to draw on female metabolic energy reserves and included the duration of lactation, growth among primiparas, and dietary limitations. The last also increased menarche. Females offset the metabolic costs of lactation with increased foraging and catabolism, but infants died when lactation costs seemingly compromised maternal condition. The prolonged lactation and slowed reproduction are considered adaptations to promote infant survival and growth in an environment where the natural food supply limits population growth and competition for food and water impacts the mortality of the youngest the most.
Badger, Janelle J.; Bowen, W. Don; den Heyer, Cornelia E.; Breed, Greg A.(
, Ecology and Evolution)
Abstract
An individual's size in early stages of life may be an important source of individual variation in lifetime reproductive performance, as size effects on ontogenetic development can have cascading physiological and behavioral consequences throughout life. Here, we explored how size‐at‐young influences subsequent reproductive performance in gray seals (Halichoerus grypus) using repeated encounter and reproductive data on a marked sample of 363 females that were measured for length after weaning, at ~4 weeks of age, and eventually recruited to the Sable Island breeding colony. Two reproductive traits were considered: provisioning performance (mass of weaned offspring), modeled using linear mixed effects models; and reproductive frequency (rate at which a female returns to breed), modeled using mixed effects multistate mark–recapture models. Mothers with the longest weaning lengths produced pups 8 kg heavier and were 20% more likely to breed in a given year than mothers with the shortest lengths. Correlation in body lengths between weaning and adult life stages, however, is weak: Longer pups do not grow to be longer than average adults. Thus, covariation between weaning length and future reproductive performance appears to be a carry‐over effect, where the size advantages afforded in early juvenile stages may allow enhanced long‐term performance in adulthood.
Chamorro, Jannine D.; McDonald, Adriane M.; Hofmann, Gretchen E.(
, Frontiers in Marine Science)
Kelp forests of the California Current System have experienced prolonged marine heatwave (MHW) events that overlap in time with the phenology of life history events (e.g., gametogenesis and spawning) of many benthic marine invertebrates. To study the effect of thermal stress from MHWs during gametogenesis in the purple sea urchin ( Strongylocentrotus purpuratus ) and further, whether MHWs might induce transgenerational plasticity (TGP) in thermal tolerance of progeny, adult urchins were acclimated to two conditions in the laboratory – a MHW temperature of 18°C and a non-MHW temperature of 13°C. Following a four-month long acclimation period (October–January), adults were spawned and offspring from each parental condition were reared at MHW (18°C) and non-MHW temperatures (13°C), creating a total of four embryo treatment groups. To assess transgenerational effects for each of the four groups, we measured thermal tolerance of hatched blastula embryos in acute thermal tolerance trials. Embryos from MHW-acclimated females were more thermally tolerant with higher LT 50 values as compared to progeny from non-MHW-acclimated females. Additionally, there was an effect of female acclimation state on offspring body size at two stages of embryonic development - early gastrulae and prism, an early stage echinopluteus larvae. To assess maternal provisioning as means to also alter embryo performance, we assessed gamete traits from the differentially acclimated females, by measuring size and biochemical composition of eggs. MHW-acclimated females had eggs with higher protein concentrations, while egg size and lipid content showed no differences. Our results indicate that TGP plays a role in altering the performance of progeny as a function of the thermal history of the female, especially when thermal stress coincides with gametogenesis. In addition, the data on egg provisioning show that maternal experience can influence embryo traits via egg protein content. Although this is a laboratory-based study, the results suggest that TGP may play a role in the resistance and tolerance of S. purpuratus early stages in the natural kelp forest setting.
Doremus, Matthew R.; Stouthamer, Corinne M.; Kelly, Suzanne E.; Schmitz-Esser, Stephan; Hunter, Martha S.(
, Frontiers in Microbiology)
null
(Ed.)
Arthropods harbor heritable intracellular symbionts that may manipulate host reproduction to favor symbiont transmission. In cytoplasmic incompatibility (CI), the symbiont sabotages the reproduction of infected males such that high levels of offspring mortality result when they mate with uninfected females. In crosses with infected males and infected females, however (the “rescue” cross), normal numbers of offspring are produced. A common CI-inducing symbiont, Cardinium hertigii , causes variable levels of CI mortality in the parasitoid wasp, Encarsia suzannae. Previous work correlated CI-induced mortality with male development time in this system, although the timing of Cardinium CI-induction and the relationship between development time and CI mortality was not well understood. Here, using a combination of crosses, manipulation of development time, and fluorescence microscopy, we identify the localization and the timing of the CI-induction step in the Cardinium-E. suzannae system. Antibiotic treatment of adult Cardinium -infected males did not reduce the mortality associated with the CI phenotype, suggesting that CI-alteration occurs prior to adulthood. Our results suggest that the alteration step occurs during the pupal period, and is limited by the duration of pupal development: 1) Encarsia produces most sperm prior to adulthood, 2) FISH localization of Cardinium in testes showed an association with sperm nuclei throughout spermatogenesis but not with mature sperm, and 3) two methods of prolonging the pupal period (cool temperatures and the juvenile hormone analog methoprene) both caused greater CI mortality, suggesting the degree of alteration is limited by the duration of the pupal stage. Based on these results, we compare two models for potential mechanisms of Cardinium sperm modification in the context of what is known about analogous mechanisms of Wolbachia , a more extensively studied CI-inducing symbiont.
Mann, Janet, Foroughirad, Vivienne, McEntee, Molly H., Miketa, Madison L., Evans, Taylor C., Karniski, Caitlin, Krzyszczyk, Ewa, Patterson, Eric M., Strohman, John C., and Wallen, Megan M. Elevated Calf Mortality and Long-Term Responses of Wild Bottlenose Dolphins to Extreme Climate Events: Impacts of Foraging Specialization and Provisioning. Retrieved from https://par.nsf.gov/biblio/10293580. Frontiers in Marine Science 8. Web. doi:10.3389/fmars.2021.617550.
Mann, Janet, Foroughirad, Vivienne, McEntee, Molly H., Miketa, Madison L., Evans, Taylor C., Karniski, Caitlin, Krzyszczyk, Ewa, Patterson, Eric M., Strohman, John C., & Wallen, Megan M. Elevated Calf Mortality and Long-Term Responses of Wild Bottlenose Dolphins to Extreme Climate Events: Impacts of Foraging Specialization and Provisioning. Frontiers in Marine Science, 8 (). Retrieved from https://par.nsf.gov/biblio/10293580. https://doi.org/10.3389/fmars.2021.617550
Mann, Janet, Foroughirad, Vivienne, McEntee, Molly H., Miketa, Madison L., Evans, Taylor C., Karniski, Caitlin, Krzyszczyk, Ewa, Patterson, Eric M., Strohman, John C., and Wallen, Megan M.
"Elevated Calf Mortality and Long-Term Responses of Wild Bottlenose Dolphins to Extreme Climate Events: Impacts of Foraging Specialization and Provisioning". Frontiers in Marine Science 8 (). Country unknown/Code not available. https://doi.org/10.3389/fmars.2021.617550.https://par.nsf.gov/biblio/10293580.
@article{osti_10293580,
place = {Country unknown/Code not available},
title = {Elevated Calf Mortality and Long-Term Responses of Wild Bottlenose Dolphins to Extreme Climate Events: Impacts of Foraging Specialization and Provisioning},
url = {https://par.nsf.gov/biblio/10293580},
DOI = {10.3389/fmars.2021.617550},
abstractNote = {As demands for wildlife tourism increase, provisioning has become a popular means of providing up-close viewing to the public. At Monkey Mia, Shark Bay, Australia, up to five adult female Indo-Pacific bottlenose dolphins ( Tursiops aduncus ) visit a 100 m stretch of beach daily to receive fish handouts. In 2011, a severe marine heatwave (MHW) devastated seagrass and fish populations in Shark Bay. Offspring survival declined precipitously among seagrass specialists (dolphins that forage disproportionately in seagrass habitat). As all provisioned dolphins at the site are seagrass specialists, we examined how provisioned and non-provisioned seagrass specialists responded to the MHW. Using 27 years of data we compare habitat use, home range size, calf mortality, and predation risk between provisioned and non-provisioned females and their offspring before and after the MHW. Our results show that provisioned females have extremely small home ranges compared to non-provisioned females, a pattern attributable to their efforts to remain near the site of fish handouts. However, weaned offspring (juveniles) born to provisioned females who are not provisioned themselves also had much smaller home ranges, suggesting a persistent maternal effect on their behavior. After the MHW, adult females increased their use of seagrass habitats, but not their home range size. Provisioned females had significantly lower calf mortality than non-provisioned females, a pattern most evident pre-MHW, and, in the first 5 years after the MHW (peri-MHW, 2011–2015), calf mortality did not significantly increase for either group. However, the ecosystem did not recover, and post-MHW (2016–2020), calf mortality was substantially higher, regardless of provisioning status. With few survivors, the impact of the MHW on juvenile mortality post-weaning is not known. However, over three decades, juvenile mortality among offspring of provisioned vs. non-provisioned females did not statistically differ. Thus, the survival benefits accrued to calves in the provisioned group likely cease after weaning. Finally, although shark attack rates on seagrass specialists did not change over time, elevated predation on calves cannot be ruled out as a cause of death post-MHW. We discuss our results as they relate to anthropogenic influences on dolphin behavioral plasticity and responses to extreme climate events.},
journal = {Frontiers in Marine Science},
volume = {8},
author = {Mann, Janet and Foroughirad, Vivienne and McEntee, Molly H. and Miketa, Madison L. and Evans, Taylor C. and Karniski, Caitlin and Krzyszczyk, Ewa and Patterson, Eric M. and Strohman, John C. and Wallen, Megan M.},
editor = {null}
}
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