The environment as a driver of immune and endocrine responses in dolphins (Tursiops truncatus)

Abstract

Immune and endocrine responses play a critical role in allowing animals to adjust to environmental perturbations. We measured immune and endocrine related markers in multiple samples from individuals from two managed-care care dolphin groups (n = 82 samples from 17 dolphins and single samples collected from two wild dolphin populations: Indian River Lagoon, (IRL) FL (n = 26); and Charleston, (CHS) SC (n = 19). The immune systems of wild dolphins were more upregulated than those of managed-care-dolphins as shown by higher concentrations of IgG and increases in lysozyme, NK cell function, pathogen antibody titers and leukocyte cytokine transcript levels. Collectively, managed-care care dolphins had significantly lower levels of transcripts encoding pro-inflammatory cytokine TNF, anti-viral MX1 and INFα and regulatory IL-10. IL-2Rα and CD69, markers of lymphocyte activation, were both lower in managed-care care dolphins. IL-4, a cytokine associated with TH2 activity, was lower in managed-care care dolphins compared to the free-ranging dolphins. Differences in immune parameters appear to reflect the environmental conditions under which these four dolphin populations live which vary widely in temperature, nutrition, veterinary care, pathogen/contaminant exposures, etc. Many of the differences found were consistent with reduced pathogenic antigenic stimulation in managed-care care dolphins compared to wild dolphins. Managed-care care dolphins had relatively low TH2 lymphocyte activity and fewer circulating eosinophils compared to wild dolphins. Both of these immunologic parameters are associated with exposure to helminth parasites which is uncommon in managed-care care dolphins. Less consistent trends were observed in a suite of hormones but significant differences were found for cortisol, ACTH, total T4, free T3, and epinephrine. While the underlying mechanisms are likely multiple and complex, the marked differences observed in the immune and endocrine systems of wild and managed-care care dolphins appear to be shaped by their environment.

Fig 1. Gene transcript levels of measured cytokines from managed-care (Navy, Georgia Aquarium (GA)) and wild populations (Indian River Lagoon (IRL), FL, Charleston (CHS), SC), adjusted for age and sex, using a general linear model.

Statistical differences between groups were found for the following five cytokines TNF, INFα, IL-4, IL-10, IRL2Rα (see Table 5 for statistical differences). Generally, higher transcript levels were found in wild dolphins versus one or both managed-care groups (note, the smaller the normalized value, the more a gene is transcribed, the larger the normalized value, the less a gene is transcribed).

Fig 2. Means and standard deviation of antibody titers to marine bacteria from managed-care (Navy, Georgia Aquarium (GA)) and wild populations (Indian River Lagoon (IRL), FL, Charleston (CHS), SC), adjusted for age and sex, using a general linear model.

For all antibodies, significantly higher titers were found in wild dolphins compared to one or more of the managed dolphin groups (see Table 5 for statistical differences). No differences were observed between the two managed-care dolphin groups with their antibody titers to V. cholera and M. marinarum but differences occurred in the other three organisms (E. rhusiopathiae, V. parahaemolyticus, E.coli).