Accurate epigenetic aging in bottlenose dolphins (Tursiops truncatus), an essential step in the conservation of at-risk dolphins

Funding: This research was funded by SERDP grant RC20-C2-1097 awarded to Peter Tyack and Prescott Award NA20NMF4390132 awarded to Ashley Barratclough.Epigenetics, specifically DNA methylation, allows for the estimation of animal age from blood or remotely sampled skin. This multi-tissue epigenetic age estimation clock uses 110 longitudinal samples from 34 Navy bottlenose dolphins (Tursiops truncatus), identifying 195 cytosine-phosphate-guanine sites associated with chronological aging via cross-validation with one individual left out in each fold (R2 = 0.95). With a median absolute error of 2.5 years, this clock improves age estimation capacity in wild dolphins, helping conservation efforts and enabling a better understanding of population demographicsPublisher PDFPeer reviewe

An expert-based system to predict population survival rate from health data

This work was supported by the Office of Naval Research Marine Mammal Biology Program [grant number N00014-17-1-2868].Timely detection and understanding of causes for population decline are essential for effective wildlife management and conservation. Assessing trends in population size has been the standard approach but we propose that monitoring population health could prove more effective. We collated data from seven bottlenose dolphin (Tursiops truncatus) populations in southeastern U.S. to develop the Veterinary Expert System for Outcome Prediction (VESOP), which estimates survival probability using a suite of health measures identified by experts as indices for inflammatory, metabolic, pulmonary, and neuroendocrine systems. VESOP was implemented using logistic regression within a Bayesian analysis framework, and parameters were fit using records from five of the sites that had a robust stranding network and frequent photographic identification (photo-ID) surveys to document definitive survival outcomes. We also conducted capture-mark-recapture (CMR) analyses of photo-ID data to obtain separate estimates of population survival rates for comparison with VESOP survival estimates. VESOP analyses found multiple measures of health, particularly markers of inflammation, were predictive of 1- and 2-year individual survival. The highest mortality risk one year following health assessment related to low alkaline phosphatase, with an odds ratio of 10.2 (95% CI 3.41-26.8), while 2-year mortality was most influenced by elevated globulin (9.60; 95% CI 3.88-22.4); both are markers of inflammation. The VESOP model predicted population-level survival rates that correlated with estimated survival rates from CMR analyses for the same populations (1-year Pearson's r = 0.99; p = 1.52e-05, 2-year r = 0.94; p = 0.001). While our proposed approach will not detect acute mortality threats that are largely independent of animal health, such as harmful algal blooms, it is applicable for detecting chronic health conditions that increase mortality risk. Random sampling of the population is important and advancement in remote sampling methods could facilitate more random selection of subjects, obtainment of larger sample sizes, and extension of the approach to other wildlife species.Publisher PDFPeer reviewe

Modeling population effects of the Deepwater Horizon oil spill on a long-lived species

This research was enabled partly by a grant from The Gulf of Mexico Research Initiative (GOMRI).The 2010 Deepwater Horizon (DWH) oil spill exposed common bottlenose dolphins (Tursiops truncatus) in Barataria Bay, Louisiana to heavy oiling that caused increased mortality and chronic disease and impaired reproduction in surviving dolphins. We conducted photographic surveys and veterinary assessments in the decade following the spill. We assigned a prognostic score (good, fair, guarded, poor, or grave) for each dolphin to provide a single integrated indicator of overall health, and we examined temporal trends in prognostic scores. We used expert elicitation to quantify the implications of trends for the proportion of the dolphins that would recover within their lifetime. We integrated expert elicitation, along with other new information, in a population dynamics model to predict the effects of observed health trends on demography. We compared the resulting population trajectory with that predicted under baseline (no spill) conditions. Disease conditions persisted and have recently worsened in dolphins that were presumably exposed to DWH oil: 78% of those assessed in 2018 had a guarded, poor, or grave prognosis. Dolphins born after the spill were in better health. We estimated that the population declined by 45% (95% CI 14–74) relative to baseline and will take 35 years (95% CI 18–67) to recover to 95% of baseline numbers. The sum of annual differences between baseline and injured population sizes (i.e., the lost cetacean years) was 30,993 (95% CI 6607–94,148). The population is currently at a minimum point in its recovery trajectory and is vulnerable to emerging threats, including planned ecosystem restoration efforts that are likely to be detrimental to the dolphins’ survival. Our modeling framework demonstrates an approach for integrating different sources and types of data, highlights the utility of expert elicitation for indeterminable input parameters, and emphasizes the importance of considering and monitoring long-term health of long-lived species subject to environmental disasters. Article impact statement: Oil spills can have long-term consequences for the health of long-lived species; thus, effective restoration and monitoring are needed.Publisher PDFPeer reviewe

Radiographic assessment of pectoral flipper bone maturation in bottlenose dolphins (Tursiops truncatus), as a novel technique to accurately estimate chronological age.

Accurate age estimation in wildlife conservation is an important diagnostic tool in the interpretation of biological data, necropsy examination, reproductive status and population demographics. The most frequently utilized methods to age bottlenose dolphins (Tursiops truncatus) include tooth extraction; counting dental growth layer groups and dental radiography. These methods are inaccurate in dolphins > 13 years old, due to overlapping of the growth layer groups in dolphins and worn teeth. Establishing a non-invasive method of accurately aging bottlenose dolphins across the entire age range is important to long term conservation efforts to understand health status, lifespan, reproduction and survivability. A database of 126 radiographs from 94 dolphins of known chronological age was utilized to establish the stages of skeletal ossification over time. A numerical score from -1 to 8 was assigned to 16 anatomic locations on the pectoral radiograph, to create a formula to estimate age. The most informative areas to evaluate morphologically were the metaphyseal regions of the radius and ulna, and the proximal and distal epiphysis of metacarpals II and III. Third order polynomial regression calculated separate age predictor formulas for male and female dolphins, with females reaching sexual maturity earlier than males. Completion of epiphyseal closure of the long bones correlated with average sexual maturity. Managed care dolphin ages could be properly estimated with decreasing precision from within 3 months in animals 30 years old. This diagnostic tool could also be applied to diagnose atypical ossification patterns consistent with nutritional, developmental or growth abnormalities, and identifying subclinical health issues. In conclusion, knowledge of the lifespan and the onset of sexual maturity for each species will allow this model to be applied to other cetaceans, facilitating age estimation via pectoral radiography in future research

Age and Sexual Maturity Estimation of Stranded Striped Dolphins, Stenella coeruleoalba, Infected with Brucella ceti

Age parameters in cetaceans allow examining conservation and studying individuals with growth affection. The age and sexual maturity of 51 stranded Stenella coeruleoalba striped dolphins from the Eastern Tropical Pacific (ETP) of Costa Rica, most suffering brucellosis (95.6%), were assessed. In order to ascertain the dolphins’ ages, we measured the length and growth of dentin-layer group counts (GLGs) and assessed flipper bone radiography without (FBSA) and with a formula (FBF). Sexual maturity was determined through gonadal histology and sexual hormone serum levels. Compared with a model based on S. coeruleoalba ages estimations in other latitudes, the striped dolphin studied displayed deficient growth parameters, with considerable variability in length, teeth, and flippers bone development. Close to 43% (n = 15) of GLGs’ measurements were below the body length average ranges for the predicted age, suggesting developmental abnormalities. Likewise, 34.4% and 31.2% of the dolphins assessed by FBSA and FBF were also below the body length based on age prediction curves, also indicating developmental abnormalities. This information is supported by the poor correlation between GLGs, FBSA, and FBF. Inconsistencies between sexually mature males and females related to GLGs, FBSA, and FBF were evident. Although the different oceanic settings of the ETP, such as contamination, food access, diseases, and other parameters, may influence size variation, our data also suggest that long-lasting debilitating brucellosis may account for detrimental growth in the ETP striped dolphins. Our study highlights the possible deleterious consequences of chronic infectious diseases in the cetacean populations already confronting distressful conditions

Age and Sexual Maturity Estimation of Stranded Striped Dolphins, Stenella coeruleoalba, Infected with Brucella ceti

Age parameters in cetaceans allow examining conservation and studying individuals with growth affection. The age and sexual maturity of 51 stranded Stenella coeruleoalba striped dolphins from the Eastern Tropical Pacific (ETP) of Costa Rica, most suffering brucellosis (95.6%), were assessed. In order to ascertain the dolphins’ ages, we measured the length and growth of dentin-layer group counts (GLGs) and assessed flipper bone radiography without (FBSA) and with a formula (FBF). Sexual maturity was determined through gonadal histology and sexual hormone serum levels. Compared with a model based on S. coeruleoalba ages estimations in other latitudes, the striped dolphin studied displayed deficient growth parameters, with considerable variability in length, teeth, and flippers bone development. Close to 43% (n = 15) of GLGs’ measurements were below the body length average ranges for the predicted age, suggesting developmental abnormalities. Likewise, 34.4% and 31.2% of the dolphins assessed by FBSA and FBF were also below the body length based on age prediction curves, also indicating developmental abnormalities. This information is supported by the poor correlation between GLGs, FBSA, and FBF. Inconsistencies between sexually mature males and females related to GLGs, FBSA, and FBF were evident. Although the different oceanic settings of the ETP, such as contamination, food access, diseases, and other parameters, may influence size variation, our data also suggest that long-lasting debilitating brucellosis may account for detrimental growth in the ETP striped dolphins. Our study highlights the possible deleterious consequences of chronic infectious diseases in the cetacean populations already confronting distressful conditions.Los parámetros de edad en cetáceos permiten examinar la conservación y estudiar individuos con afección al crecimiento. Se evaluaron la edad y la madurez sexual de 51 delfines listados Stenella coeruleoalba varados del Pacífico Tropical Oriental (PTO) de Costa Rica, la mayoría con brucelosis (95,6%), fueron evaluados. Para determinar la edad de los delfines, se midió la longitud y el crecimiento de los grupos de capas dentarias (GLG) y se evaluó la radiografía ósea de las aletas sin (FBSA) y con fórmula (FBF). La madurez sexual se determinó mediante la histología gonadal y los niveles séricos de hormonas sexuales. En comparación con un modelo basado en estimaciones de las edades de S. coeruleoalba en otras latitudes, el delfín listado delfín estudiado mostró parámetros de crecimiento deficientes, con una variabilidad considerable en longitud, dientes y desarrollo óseo de las aletas. Cerca del 43% (n = 15) de las medidas de los GLGs estaban por debajo de los rangos medios de longitud corporal para la edad predicha. rangos de longitud media para la edad prevista, lo que sugiere anomalías de desarrollo. Asimismo 34,4% y 31,2% de los delfines evaluados por FBSA y FBF estaban también por debajo de la longitud corporal basada en las curvas de predicción de edad, indicando también anormalidades del desarrollo. curvas de predicción de edad, indicando también anormalidades de desarrollo. Esta información es apoyada por la pobre correlación entre GLGs, FBSA, y FBF. Las incoherencias entre machos sexualmente maduros entre machos y hembras sexualmente maduros. Aunque los diferentes entornos oceánicos la contaminación, el acceso a los alimentos, las enfermedades y otros parámetros, pueden influir en la en la variación del tamaño, nuestros datos también sugieren que la brucelosis debilitante de larga duración puede explicar el crecimiento perjudicial en el delfín listado del POT. crecimiento perjudicial en los delfines listados del POT. Nuestro estudio destaca las posibles consecuencias perjudiciales de enfermedades infecciosas crónicas en las poblaciones de cetáceos que ya se enfrentan a condiciones angustiosasUniversidad Nacional, Costa RicaEscuela de Medicina Veterinari