Wholistic assessment of immune effects of environmental disruptions: A case study using fence lizards and invasive fire ants
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- Author:
- Tylan, Catherine
- Graduate Program:
- Biology
- Degree:
- Doctor of Philosophy
- Document Type:
- Dissertation
- Date of Defense:
- March 05, 2021
- Committee Members:
- Tracy Langkilde, Dissertation Advisor/Co-Advisor
James Harold Marden, Committee Chair/Co-Chair
David Hughes, Committee Member
Susannah French, Special Member
Sonia Angele Cavigelli, Outside Member
Elizabeth Ann Mcgraw, Program Head/Chair - Keywords:
- fence lizard
fire ant
ecoimmunology
stress
glucocorticoids
immunity - Abstract:
- Environmental disruptions of native ecosystems are increasingly common, with stressors such as the introduction of invasive animals and climate change attracting particular attention. Such disruptions to an animal’s environment and associated physiological stress may have potent behavioral, morphological, and physiological sequelae. Such sequelae may be beneficial, adapting the animal to the disturbed environment, but may also render them more susceptible to further perturbations or even result in the eventual extinction of the populations or more rarely species. We need to understand how environmental disruptions affect native animals, in order to appropriately steward and preserve native ecosystems. A particularly important physiological alteration which may occur in native animals exposed to environmental disruptions is changes to their immune function. Such immune changes may directly impact their ability to respond to disruptions such as the presence of invasive animals, and can also affect their ability to deal with and recover from subsequent or co-occurring environmental stressors such as pathogens and wounding. My dissertation research focused on the effects of an invasive insect, the red imported fire ant (Solenopsis invicta), on the immune system of a native animal, the eastern fence lizard (Sceloporus undulatus). These lizards are found throughout the southeastern United States, and in the southern portion of their range have coexisted with invasive fire ants for decades. Fire ants and fence lizards encounter one-another frequently, and both serve as both predator and prey for the other, resulting in interactions that are sublethal but stressful for the lizards. Lizards have a number of morphological, behavioral, and physiological modifications associated with the presence of fire ants, including elevated plasma corticosterone (CORT) concentrations. CORT, the primary glucocorticoid in lizards, is a stress-relevant hormone commonly elevated in animals dealing with stressful stimuli. Immunosuppression is a common sequela of chronically elevated CORT, and this, combined with the immunological potency of fire ant venom, suggests that the presence of fire ants could cause immunological changes in this native lizard. In order to appropriately assess lizard immunity, I compiled a suite of immune tests that can be performed on a lizard to obtain a broad picture of how immunity is affected by fire ants by testing as many branches of the immune system as possible. As part of my initial work developing some of these tests I explored the use of a common test of cell-mediated immune function, the phytohemagglutinin (PHA) skin test. I found that different formulations of PHA assessed different immune responses, and that the PHA-P formulation was a relatively specific assessment of lymphocytic immunity. As baseline concentrations of CORT are known to affect immune function and other parameters, I next quantified the time required to obtain baseline plasma CORT concentrations in several reptile species, including the eastern fence lizard. The blood sampling needed to measure CORT can itself elevate CORT concentrations, so there is a limited time period in which to obtain a blood sample after disturbing an animal before plasma CORT starts increasing due to handling stress. Blood obtained within 3 min of disturbance is commonly considered to indicate baseline concentrations of CORT, but this is based primarily on studies of mammals and birds. Reptiles, as ectotherms, are metabolically different, and this may affect the timing of their release of CORT into the blood. I found that the “3 min rule” was broadly applicable in reptiles, but may need to be shorter in some species (rattlesnakes, rock iguanas), depending on the purpose of the study, or unnecessarily limiting in others (cottonmouths, fence lizards). In addition to the effect of time since disturbance, I also theorized that temperature could affect plasma CORT concentrations, and therefore immune function. Working with an undergraduate researcher, we found that temperature affected CORT release in fence lizards, with lizards kept at lower temperatures showing lower plasma CORT concentrations. While this effect did not appear to be relevant in lizards captured in the field, lizards kept at room temperature failed to show an increase in CORT due to a standardized restraint stressor. Thus, it is important to ensure that lizards be allowed to thermoregulate or otherwise maintain their body temperature when performing laboratory studies in order to observe appropriate physiological stress responses. By applying these methods of assessing immune function and plasma CORT, I then tested the effect of fire ant invasion on immune function. I assessed a broad suite of immune measures in lizards from fire ant invaded (“invaded”) areas and lizards from areas not yet invaded by fire ants (“uninvaded”), and found that some immune measures were lower in invaded areas (lymphocytic cell-mediated immunity, complement), some measures were the same in both areas (phagocyte respiratory burst, natural antibodies), and some were higher in invaded areas (anti-fire ant IgM, basophils). The immune alterations seen in the invaded areas appear to be tailored to the specific stressor of fire ants, rather than being broadly immunosuppressed due to stress, with the immune measures which were higher in invaded areas being particularly important to resisting envenomation when stung. Additionally, in work performed by an undergraduate researcher I advised, we found that in postpartum female lizards kept in captivity (as opposed to captured in the field) lizards from invaded areas had lower lymphocytic cell-mediated immunity as compared to lizards from uninvaded areas. We also found that exogenous CORT reduced the lymphocytic cell-mediated immune function of lizards from uninvaded areas, but not of lizards from fire ant invaded areas, indicating that previous history of exposure to fire ants has also altered their immune response to CORT. Finally, in order to determine how much of the immune alterations in fence lizards associated with existing in fire ant invaded areas were due directly to fire ant exposure, I exposed fence lizards from an uninvaded area to fire ants over the course of three weeks in captivity. Mimicking routes of potential venom exposure in nature, I assigned lizards to one of 3 groups: fed deceased fire ants, stung by fire ants, and feeding and handling controls only. Lizards were then tested for a broad suite of immune measures: all of the immune measures which were increased in lizards fed fire ants were enhanced relative to the lizards stung by fire ants, which may indicate that fire ant consumption can bolster immune measures needed to combat later envenomation. Interpreted together, the wholistic assessment of immunity in lizards in the field and exposed to fire ants in captivity provide a more nuanced picture of how invasive fire ants may affect the immune system of the native eastern fence lizard. This can provide a helpful base of understanding of what pathogens and environmental challenges may be of most concern in managing these populations. Additionally, the information from this system may serve as a starting point for understanding how fire ants and other invasive species affect the immune system of other animals, both wild and domestic, and provides potential research routes for how to help them manage the deleterious effects due to alterations in immune function associated with invasive species.
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