Kevin D. Matson

Disease ecology in the Galapagos Hawk (Buteo galapagoensis): host genetic diversity, parasite load and natural antibodies

An increased susceptibility to disease is one hypothesis explaining how inbreeding hastens extinction in island endemics and threatened species. Experimental studies show that disease resistance declines as inbreeding increases, but data from in situ wildlife systems are scarce. Genetic diversity increases with island size across the entire range of an extremely inbred Galápagos endemic bird, providing the context for a natural experiment examining the effects of inbreeding on disease susceptibility. Extremely inbred populations of Galápagos hawks had higher parasite abundances than relatively outbred populations. We found a significant island effect on constitutively produced natural antibody (NAb) levels and inbred populations generally harboured lower average and less variable NAb levels than relatively outbred populations. Furthermore, NAb levels explained abundance of amblyceran lice, which encounter the host immune system. This is the first study linking inbreeding, innate immunity and parasite load in an endemic, in situ wildlife population and provides a clear framework for assessment of disease risk in a Galápagos endemic.

Capture stress and the bactericidal competence of blood and plasma in five species of tropical birds

In wild birds, relatively little is known about intra‐ or interspecific variation in immunological capabilities, and even less is known about the effects of stress on immune function. Immunological assays adaptable to field settings and suitable for a wide variety of taxa will prove most useful for addressing these issues. We describe a novel application of an in vitro technique that measures the intrinsic bacteria‐killing abilities of blood. We assessed the capacities of whole blood and plasma from free‐living individuals of five tropical bird species to kill a nonpathogenic strain of E. coli before and after the birds experienced an acute stress. Killing invasive bacteria is a fundamental immune function, and the bacteria‐killing assay measures constitutive, innate immunity integrated across circulating cell and protein components. Killing ability varied significantly across species, with common ground doves exhibiting the lowest levels and blue‐crowned motmots exhibiting the highest levels. Across species, plasma killed bacteria as effectively as whole blood, and higher concentrations of plasma killed significantly better. One hour of acute stress reduced killing ability by up to 40%. This assay is expected to be useful in evolutionary and ecological studies dealing with physiological and immunological differences in birds.

No simple answers for ecological immunology: relationships among immune indices at the individual level break down at the species level in waterfowl

Understanding immune function in the context of other life-history traits is crucial to understand the evolution of life histories, at both the individual and species levels. As the interest in assessing immune function for these comparative purposes grows, an important question remains unanswered: can immune function be broadly characterized using one or two simple measures? Often, interpretation of individual assays is ambiguous and relationships among different measures of immune function remain poorly understood. Thus, we employed five protocols to measure 13 variables of immune function in ten species of waterfowl (Anseriformes). All assays were based on a single blood sample subdivided into leukocyte (blood smear) and plasma (frozen until analysis) components. All assays were run using samples from every individual, and a nested analysis was used to partition variation/covariation at the levels of species and individuals within species. We detected positive correlations between functionally related measures of immunity within species, but these were absent from comparisons between species. A canonical correlation analysis revealed no significant relationships between the plasma and leukocyte assays at the levels of both individual and species, suggesting that these measures of immunity are neither competitive nor synergistic. We conclude that one measure of each assay type may be required to maximally characterize immune function in studies of a single species, while the same is not true in studies among species.

Seasonal Redistribution of Immune Function in a Migrant Shorebird: Annual-Cycle Effects Override Adjustments to Thermal Regime

Throughout the annual cycle, demands on competing physiological systems change, and animals must allocate resources to maximize fitness. Immune function is one such system and is important for survival. Yet detailed empirical data tracking immune function over the entire annual cycle are lacking for most wild animals. We measured constitutive immune indices once a month for a year on captive red knots (Calidris canutus). We also examined temperature as an environmental contributor to immune variation by manipulating ambient temperature to vary energy expenditure. To identify relationships among immune indices, we performed principal‐component analysis. We found significant repeatability in immune indices over the annual cycle and covariation of immune indices within and among individuals. This covariation suggests immune strategies as individual traits among individuals and the use of different immune strategies during different annual‐cycle stages within individuals. Over the annual cycle, both higher‐cost phagocyte‐based immunity and lower‐cost lymphocyte‐based immunity were high during mass change, but there was a clear shift toward lower‐cost lymphocyte‐based immunity during peak molt. Experimental manipulation of temperature had little effect on annual variation in immune function. This suggests that other environmental factors, such as food availability and disease, should also be examined in the future.

Nutrition of Birds in the Order Psittaciformes: A Review

Abstract Over 350 species of birds make up the order Psittaciformes; many of these are maintained in captive environments. Malnutrition is commonly diagnosed in captive psittacine birds; therefore, providing nutritionally adequate diets must be a primary concern. This review integrates quantitative information on the dietary habits and nutritional requirements of psittacine birds to facilitate the formulation and evaluation of diets for birds in captivity. Initially, characterization of the diet and feeding strategy of a particular species in the wild can provide insight into appropriate diet choices in captivity. Knowledge of the gastrointestinal anatomy and physiology can be used to elucidate the capacity of that species to utilize various feedstuffs. For example, the presence of a highly muscularized gizzard may allow a bird to utilize a seed-based diet, whereas a species possessing a small gizzard may be unable to process such a diet. Finally, nutrient requirements determined in a particular species or a related species (eg, similar digestive physiology and feeding strategy) may be applied to create a nutritionally adequate diet. Understanding the factors involved in selecting appropriate diets enables aviculturists, veterinarians, and nutritionists to maintain and propagate these birds with increased success.

Variation in the innate and acquired arms of the immune system among five shorebird species.

SUMMARY To contribute to an understanding of the evolutionary processes that shape variation in immune responses, we compared several components of the innate and acquired arms of the immune system in five related, but ecologically diverse, migratory shorebirds (ruff Philomachus pugnax L., ruddy turnstone Arenaria interpres L., bar-tailed godwit Limosa lapponica L., sanderling Calidris alba Pallas and red knot C. canutus L.). We used a hemolysis-hemagglutination assay in free-living shorebirds to assess two of the innate components (natural antibodies and complement-mediated lysis), and a modified quantitative enzyme-linked immunosorbent assay in birds held in captivity to assess the acquired component (humoral antibodies against tetanus and diphtheria toxoid) of immunity. Ruddy turnstones showed the highest levels of both innate and acquired immune responses. We suggest that turnstones could have evolved strong immune responses because they scavenge among rotting organic material on the seashore, where they might be exposed to a particularly broad range of pathogens. Although ruffs stand out among shorebirds in having a high prevalence of avian malaria, they do not exhibit higher immune response levels. Our results indicate that relationships between immune response and infection are not likely to follow a broad general pattern, but instead depend on type of parasite exposure, among other factors.

Effects of immune supplementation and immune challenge on oxidative status and physiology in a model bird: implications for ecologists

SUMMARY One route to gain insight into the causes and consequences of ecological differentiation is to understand the underlying physiological mechanisms. We explored the relationships between immunological and oxidative status and investigated how birds cope physiologically with the effects of immune-derived oxidative damage. We successively implemented two experimental manipulations to alter physiological status in a model bird species: the homing pigeon (Columba livia). The first manipulation, an immune supplementation, was achieved by oral administration of lysozyme, a naturally occurring and non-specific antimicrobial enzyme. The second manipulation, an immune challenge, took the form of an injection with lipopolysaccharide, a bacterial endotoxin. Between groups of lysozyme-treated and control birds, we compared lipopolysaccharide-induced changes in reactive oxygen metabolites, total antioxidant capacity, haptoglobin, oxygen consumption, body mass and cloacal temperature. Lysozyme supplementation intensified the lipopolysaccharide-induced inflammatory response and generated short-term oxidative and metabolic costs. We identified significant interactions between immune supplementation and immune challenge in terms of reactive oxygen metabolites, haptoglobin and oxygen consumption. Our study provides alternative interpretations of differences in oxidative and immunological indices and demonstrates that these indices can also fluctuate and interact across very short time scales, reflecting something akin to current ‘health status’ or ‘physiological condition’. These ephemeral effects highlight the need to broadly consider current physiological condition when drawing conclusions that relate physiology to ecology and evolution.

Are there differences in immune function between continental and insular birds

Generally, immune system architecture varies with different environments, which presumably reflect different pathogen pressures. Specifically, populations from relatively disease-free, oceanic islands are expected to exhibit reorganized immune systems, which might be characterized by attenuated responses, given the costs of immune function. Some insular animals exhibit an ‘island syndrome,’ including increased susceptibility to disease, and some insular populations have declined when they failed to resist infection by introduced pathogens. I measured eight indices of immune function (haemolysis, haemagglutination, concentration of haptoglobin and concentration of five leukocyte types) in 15 phylogenetically matched pairs of bird populations from North America and from the islands of Hawaii, Bermuda and the Galápagos. Immune responses were not attenuated in insular birds, and several indices, including the concentration of plasma haptoglobin, were elevated. Thus, I find no support for the specific hypothesis that depauperate parasite communities and the costs of immune defences select for reduced immune function. Instead, I suggest that life on islands leads to an apparent reorganization of immune function, which is defined by increases in defences that are innate and inducible. These increases might signal that systems of acquired humoral immunity and immunological memory are less important or dysfunctional in island populations.

Immune function in a free-living bird varies over the annual cycle, but seasonal patterns differ between years

A central hypothesis of eco-immunology proposes trade-offs between immune defences and competing physiological and behavioural processes, leading to immunological variation within and among annual-cycle stages, as has been revealed for some species. However, few studies have simultaneously investigated patterns of multiple immune indices over the entire annual cycle in free-living birds, and none has investigated the consistency of seasonal patterns across multiple years. We quantified lysis, agglutination, haptoglobin, leukocyte profiles, and body mass in free-living skylarks (Alauda arvensis) through two complete annual cycles and within and between four breeding seasons. The skylarks’ annual cycle is characterised by annually repeated changes in energy and time budgets, social structure and diet. If trade-offs relating to these cyclic changes shape evolution, predictable intra-annual immune patterns may result. Alternatively, intra-annual immune patterns may vary among years if fluctuating environmental changes affect the cost–benefit balances of immune function. We found significant variation in immune indices and body mass across the annual cycle, and these patterns differed between years. Immune parameters differed between four breeding seasons, and in all years, lysis and agglutination increased as the season progressed independent of average levels. Population-level patterns (intra-annual, inter-annual, within breeding season) were consistent with within-individual patterns based on repeated measurements. We found little evidence for sex differences, and only haptoglobin was correlated (negatively) with body mass. We conclude that immune modulation is not simply a pre-programmed phenomenon that reflects predictable ecological changes. Instead, fluctuating environmental conditions that vary among years likely contribute to the immunological variation that we observed.

Baseline haptoglobin concentrations are repeatable and predictive of certain aspects of a subsequent experimentally-induced inflammatory response

Ecologists sometimes assume immunological indices reflect fundamental attributes of individuals-an important assumption if an index is to be interpreted in an evolutionary context since among-individual variation drives natural selection. Yet the extent to which individuals vary over different timescales is poorly understood. Haptoglobin, an acute phase protein, is an interesting parameter for studying variability as it is easily quantified and concentrations vary widely due to the molecules role in inflammation, infection and trauma. We quantified haptoglobin in pigeon plasma samples collected over fourteen months and calculated repeatability to evaluate if haptoglobin concentration is a distinctive trait of individuals. We also explored the capacity of baseline haptoglobin concentrations to predict an array of physiological changes associated with a subsequent experimentally-induced inflammatory response. Maximum repeatability, which occurred over a short mid-winter interval, equaled 0.57. Baseline haptoglobin concentrations predicted response haptoglobin concentrations better than any other endotoxin-induced change. Overall, we identified several strengths and limitations of baseline [Hp] quantification. Acknowledging these qualities should lead to more refined conclusions in studies of the ecology and evolution of immune function.