Lynn B. Martin

The Fungicide Chlorothalonil Is Nonlinearly Associated with Corticosterone Levels, Immunity, and Mortality in Amphibians

Background: Contaminants have been implicated in declines of amphibians, a taxon with vital systems similar to those of humans. However, many chemicals have not been thoroughly tested on amphibians or do not directly kill them. Objective: Our goal in this study was to quantify amphibian responses to chlorothalonil, the most commonly used synthetic fungicide in the United States. Methods: We reared Rana sphenocephala (southern leopard frog) and Osteopilus septentrionalis (Cuban treefrog) in outdoor mesocosms with or without 1 time (1×) and 2 times (2×) the expected environmental concentration (EEC) of chlorothalonil (~ 164 μg/L). We also conducted two dose–response experiments on O. septentrionalis, Hyla squirella (squirrel treefrog), Hyla cinerea (green treefrog), and R. sphenocephala and evaluated the effects of chlorothalonil on the stress hormone corticosterone. Results: For both species in the mesocosm experiment, the 1× and 2× EEC treatments were associated with > 87% and 100% mortality, respectively. In the laboratory experiments, the approximate EEC caused 100% mortality of all species within 24 hr; 82 μg/L killed 100% of R. sphenocephala, and 0.0164 μg/L caused significant tadpole mortality of R. sphenocephala and H. cinerea. Three species 
showed a nonmonotonic dose response, with low and high concentrations causing significantly greater mortality than did intermediate concentrations or control treatments. For O. septentrionalis, corticosterone exhibited a similar nonmonotonic dose response and chlorothalonil concentration was inversely associated with liver tissue and immune cell densities (< 16.4 μg/L). Conclusions: Chlorothalonil killed nearly every amphibian at the approximate EEC; at concentrations to which humans are commonly exposed, it increased mortality and was associated with elevated corticosterone levels and changes in immune cells. Future studies should directly quantify the effects of chlorothalonil on amphibian populations and human health.

Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs?

The activation of an immune response is beneficial for organisms but may also have costs that affect fitness. Documented immune costs include those associated with acquisition of special nutrients, as well as immunopathology or autoimmunity. Here, we test whether an experimental induction of the immune system with a non–pathological stimulant can elevate energy turnover in passerine birds. We injected phytohaemagglutinin (PHA), a commonly used mitogen that activates the cell–mediated immune response, into the wing web of house sparrows, Passer domesticus. We then examined energetic costs resulting from this immune activity and related those costs to other physiological activities. We found that PHA injection significantly elevated resting metabolic rate (RMR) of challenged sparrows relative to saline controls. We calculated the total cost of this immune activity to be ca. 4.20 kJ per day (29% RMR), which is equivalent to the cost of production of half of an egg (8.23 kJ egg−1) in this species. We suggest that immune activity in wild passerines increases energy expenditure, which in turn may influence important life–history characteristics such as clutch size, timing of breeding or the scheduling of moult.

Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs

Animals living in temporally dynamic environments experience variation in resource availability, climate and threat of infection over the course of the year. Thus, to survive and reproduce successfully, these organisms must allocate resources among competing physiological systems in such a way as to maximize fitness in changing environments. Here, we review evidence supporting the hypothesis that physiological trade-offs, particularly those between the reproductive and immune systems, mediate part of the seasonal changes detected in the immune defences of many vertebrates. Abundant recent work has detected significant energetic and nutritional costs of immune defence. Sometimes these physiological costs are sufficiently large to affect fitness (e.g. reproductive output, growth or survival), indicating that selection for appropriate allocation strategies probably occurred in the past. Because hormones often orchestrate allocations among physiological systems, the endocrine mediators of seasonal changes in immune activity are discussed. Many hormones, including melatonin, glucocorticoids and androgens have extensive and consistent effects on the immune system, and they change in systematic fashions over the year. Finally, a modified framework within which to conduct future studies in ecological immunology is proposed, viz. a heightened appreciation of the complex but intelligible nature of the vertebrate immune system. Although other factors besides trade-offs undoubtedly influence seasonal variation in immune defence in animals, a growing literature supports a role for physiological trade-offs and the fitness consequences they sometimes produce.

Stress and immunity in wild vertebrates: Timing is everything

Stress has profound effects on vertebrate immunity, but most studies have considered stress-immune interactions in terms of wild animals enduring demanding, but predictable activities (e.g., immune alterations during breeding). A growing biomedical literature, however, indicates that stress may not be obligatorily immunosuppressive; in response to transient, unpredictable stressors, immune activity can be enhanced, especially in body areas requiring immune protection. Also, immune sensitivity to stressors is not fixed throughout life; oftentimes, glucocorticoid (GC) insensitivity can be induced. Further GC sensitivity can be programmed early in life; greater exposure to stressors prior to maturity heightens GC effects on immunity in adulthood. In the present paper, I review the cellular and molecular mechanisms that link stress responses to immune adjustments over short time scales in domesticated species then I attempt to place stress-immune interactions in a naturalistic, organismal context. When, how and why stressors affect immunity in wild animals remains practically unstudied.

Parasites as predators: unifying natural enemy ecology

Parasitism and predation have long been considered analogous interactions. Yet by and large, ecologists continue to study parasite-host and predator-prey ecology separately. Here we discuss strengths and shortcomings of the parasite-as-predator analogy and its potential to provide new insights into both fields. Developments in predator-prey ecology, such as temporal risk allocation and associational resistance, can drive new hypotheses for parasite-host systems. Concepts developed in parasite-host ecology, such as threshold host densities and phylodynamics, might provide new ideas for predator-prey ecology. Topics such as trait-mediated indirect effects and enemy-mediated facilitation provide opportunities for the two fields to work together. We suggest that greater unification of predator-prey and parasite-host ecology would foster advances in both fields.

The effects of anthropogenic global changes on immune functions and disease resistance.

Humans are changing the environmental conditions of our planet, and animal immune functions are being affected by these modifications. For instance, a diversity of chemical contaminants is entering ecosystems and modifying immune functions directly or indirectly through altered host–parasite interactions. Also, global temperature changes have caused outbreaks of disease that have decimated and even extirpated some host species, outcomes partially driven via immune alterations. Finally, some invasive species are immunologically distinct or impose stress on native species, factors that may facilitate the establishment of nonnative hosts as well as parasite transmission to native species. Here, we summarize the known and likely effects of pollutants, nonnative species introductions, and increases in ambient temperature on host immune functions and infections. We then identify future directions for research given our sparse knowledge of immune variation in natural populations. In sum, we advocate integrative, multidisciplinary work at diverse spatial and temporal scales to assess and prevent anthropogenic global changes from further compromising animal immune functions.

IMMUNE DEFENSE AND REPRODUCTIVE PACE OF LIFE IN PEROMYSCUS MICE

Immune activity is variable within and among vertebrates despite the potentially large fitness costs of pathogens to their hosts. From the perspective of life history theory, immunological variability may be the consequence of counterbalancing investments in immune defense against other expensive physiological processes, namely, reproduction. In the present study, we tested the hypothesis that immune defense among captive-bred, disease-free Peromyscus mice would be influenced by their reproductive life history strategies. Specifically, we expected that small species that reproduce prolifically and mature rapidly (i.e., fast pace of life) would favor inexpensive, nonspecific immune defenses to promote reproductive proclivity. Alternatively, we expected that large species that mature slowly and invest modestly in reproduction over multiple events (i.e., slow pace of life) would favor developmentally expensive, specific immune defenses and avoid cheap, nonspecific ones because such defenses are predisposed to self-damage. We found that species exhibited either strong ability to kill (gram-negative) bacteria, a developmentally inexpensive defense, or strong ability to produce antibodies against a novel protein, a developmentally expensive defense, but not both. Cell-mediated inflammation also varied significantly among species, but in a unique fashion relative to bacteria killing or antibody production; wound healing was comparatively similar among species. These results indicate that Peromyscus species use immune strategies that are constrained to a dominant axis, but this axis is not determined solely by reproductive pace of life. Further comparisons, ideally with broader phylogenetic coverage, could identify what ecological and evolutionary forces produce the pattern we detected. Importantly, our study indicates that species may not be differentially immunocompetent; rather, they use unique defense strategies to prevent infection.

Investment in immune defense is linked to pace of life in house sparrows

The evidence for a relationship between life history and immune defense is equivocal, although the basic premise is intuitively appealing: animals that live short lives and reproduce early and rapidly should not waste resources on defenses they might never use. One possible reason for a lack of strong support for this hypothesis could be the inherent complexity of the vertebrate immune system. Indeed, different components of the vertebrate immune system vary in their relative costs and benefits, and therefore only some defenses may complement variation in species’ life history. To address this hypothesis, we compared multiple types of immune activity between two populations of house sparrows (Passer domesticus) with distinct life histories, one from Colon, Panama, which lay small clutches over an extended breeding season (i.e., slow-living) and the other from Princeton, New Jersey, which lay larger clutches in a smaller window of time (i.e., fast-living). We expected (a) that more costly types of immune defenses would be stronger in the slow-living sparrows and (2) that the slow-living sparrows would show a greater increase in whole-body energy expenditure after immune challenge compared to their fast-living counterparts. We found that secondary antibody response to a novel antigen was more rapid and energetic investment in immune activity was greater in slow-living sparrows. However, cell-mediated immune activity was more robust in fast-living sparrows, and other measures of defense were not different between populations. These results provide partial support for a relationship between life history and immune defense in this species, but they also indicate that this relationship is not clear-cut. Further study is necessary to identify the influence of other factors, particular pathogen environment during development, on the architecture of the immune system of wild animals.

Responding to inflammatory challenges is less costly for a successful avian invader, the house sparrow (Passer domesticus), than its less-invasive congener

When introduced into new regions, invading organisms leave many native pathogens behind and also encounter evolutionarily novel disease threats. In the presence of predominantly novel pathogens that have not co-evolved to avoid inducing a strong host immune response, costly and potentially dangerous defenses such as the systemic inflammatory response could become more harmful than protective to the host. We therefore hypothesized that introduced populations exhibiting dampened inflammatory responses will tend to be more invasive. To provide initial data to assess this hypothesis, we measured metabolic, locomotor, and reproductive responses to inflammatory challenges in North American populations of the highly invasive house sparrow (Passer domesticus) and its less-invasive relative, the tree sparrow (Passer montanus). In the house sparrow, there was no effect of phytohemagglutinin (PHA) challenge on metabolic rate, and there were no detectable differences in locomotor activity between lipopolysaccharide (LPS)-injected birds and saline-injected controls. In contrast, tree sparrows injected with PHA had metabolic rates 20–25% lower than controls, and LPS injection resulted in a 35% drop in locomotor activity. In a common garden captive breeding experiment, there was no effect of killed-bacteria injections on reproduction in the house sparrow, while tree sparrows challenged with bacteria decreased egg production by 40% compared to saline-injected controls. These results provide some of the first data correlating variation in immune defenses with invasion success in introduced-vertebrate populations.

Physiological regulatory networks: ecological roles and evolutionary constraints

Ecological and evolutionary physiology has traditionally focused on one aspect of physiology at a time. Here, we discuss the implications of considering physiological regulatory networks (PRNs) as integrated wholes, a perspective that reveals novel roles for physiology in organismal ecology and evolution. For example, evolutionary response to changes in resource abundance might be constrained by the role of dietary micronutrients in immune response regulation, given a particular pathogen environment. Because many physiological components impact more than one process, organismal homeostasis is maintained, individual fitness is determined and evolutionary change is constrained (or facilitated) by interactions within PRNs. We discuss how PRN structure and its system-level properties could determine both individual performance and patterns of physiological evolution.