Proceedings of The Royal Society B: Biological Sciences, 2006
Understanding immune function in the context of other life-history traits is crucial to understan... more 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
Little is known about avian taste perception and how taste affects food choice. We designed a stu... more Little is known about avian taste perception and how taste affects food choice. We designed a study to determine the concentrations of aqueous solutions of common chemical taste stimuli that result in altered consumption patterns. Using two-choice taste-preference tests, we studied the taste thresholds of caged cockatiels (Nymphicus hollandicus) for aqueous solutions of potassium chloride, a phosphate buffer (to test pH), fructose, and glucose. First, the preferred and nonpreferred bottle locations were determined for each bird. Then, depending on the compound, the test solutions were placed in bottles in either the preferred or the nonpreferred locations and water was placed in the opposite bottle. Four parameters were measured at the end of 3-day test periods (total consumption, consumption from water side, consumption from test solution side, and proportion of nonpreferred side consumption to total consumption). Experiments were repeated with increasing concentrations of test fla...
Introduction: All bird eggs are exposed to microbes in the environment, which if transmitted to t... more Introduction: All bird eggs are exposed to microbes in the environment, which if transmitted to the developing embryo, could cause hatching failure. However, the risk of trans-shell infection varies with environmental conditions and is higher for eggs laid in wetter environments. This might relate to generally higher microbial abundances and diversity in more humid environments, including on the surface of eggshells, as well as the need for moisture to facilitate microbial penetration of the eggshell. To protect against microbial infection, the albumen of avian eggs contains antimicrobial proteins, including lysozyme and ovotransferrin. We tested whether lysozyme and ovotransferrin activities varied in eggs of larks (Alaudidae) living along an arid-mesic gradient of environmental aridity, which we used as a proxy for risk of trans-shell infection. Results: Contrary to expectations, lysozyme activity was highest in eggs from hotter, more arid locations, where we predicted the risk of trans-shell infection would be lower. Ovotransferrin concentrations did not vary with climatic factors. Temperature was a much better predictor of antimicrobial protein activity than precipitation, a result inconsistent with studies stressing the importance of moisture for trans-shell infection.
Wildlife pathogens can alter host fitness. Low pathogenic avian influenza virus (LPAIV) infection... more Wildlife pathogens can alter host fitness. Low pathogenic avian influenza virus (LPAIV) infection is thought to have negligible impacts on wild birds; however, effects of infection in free-living birds are largely unstudied. We investigated the extent to which LPAIV infection and shedding were associated with body condition and immune status in free-living mallards (Anas platyrhynchos), a partially migratory key LPAIV host species. We sampled mallards throughout the species' annual autumn LPAIV infection peak, and we classified individuals according to age, sex, and migratory strategy (based on stable hydrogen isotope analysis) when analyzing data on body mass and five indices of immune status. Body mass was similar for LPAIV-infected and noninfected birds. The degree of virus shedding from the cloaca and oropharynx was not associated with body mass. LPAIV infection and shedding were not associated with natural antibody (NAbs) and complement titers (first lines of defense against infections), concentrations of the acute phase protein haptoglobin (Hp), ratios of heterophils to lymphocytes (H:L ratio), and avian influenza virus (AIV)-specific antibody concentrations. NAbs titers were higher in LPAIV-infected males and local (i.e., short distance) migrants than in infected females and distant (i.e., long distance) migrants. Hp concentrations were higher in LPAIV-infected juveniles and females compared to infected adults and males. NAbs, complement, and Hp levels were lower in LPAIV-infected mallards in early autumn. Our study demonstrates weak associations between infection with and shedding of LPAIV and the body condition and immune status of free-living mallards. These results may support the role of mallards as asymptomatic carriers of LPAIV and raise questions about possible coevolution between virus and host.
To contribute to an understanding of the evolutionary processes that shape variation in immune re... more 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
In wild birds, relatively little is known about intra- or inter- specific variation in immunologi... more In wild birds, relatively little is known about intra- or inter- specific variation in immunological capabilities, and even less is known about the effects of stress on immune function. Im- munological 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
Developmental and Comparative Immunology - DEVELOP COMP IMMUNOL, 2005
Methods to assess immunocompetence requiring only a single sample are useful in comparative studi... more Methods to assess immunocompetence requiring only a single sample are useful in comparative studies where practical considerations prevent holding or recapturing individuals. The assay for natural antibody-mediated complement activation and red blood cell agglutination described here, requiring ∼100μl of blood, is highly repeatable. The effects of complement deactivation, 2-mercaptoethanol (2-ME), age, and lipopolysaccharide (LPS)-induced sickness response were examined to validate comparisons among diverse avian species. Complement deactivation by heating significantly reduces lysis and treatment with 2-ME reduces both lysis and agglutination. Lysis and agglutination both increase with age in chickens; LPS treatment does not influence these variables in 11-week-old chickens. In a comparison of 11 species, both lysis (0.0–5.3 titers) and agglutination (1.8–8.0 titers) vary significantly among species. Accordingly, this assay can be used to compare constitutive innate humoral immunit...
Journal of Avian Medicine and Surgery - J AVIAN MED SURG, 2001
... Journal of Avian Medicine and Surgery 15(4):257-275. 2001 doi: 10.1647/1082-6742(2001) 015[02... more ... Journal of Avian Medicine and Surgery 15(4):257-275. 2001 doi: 10.1647/1082-6742(2001) 015[0257:NOBITO]2.0.CO;2. Nutrition of Birds in the Order Psittaciformes: A Review. Elizabeth A. KoutsosMS, Kevin D. MatsonMS, Kirk C. KlasingMS, PhD. ...
Little is known about avian taste perception and how taste affects food choice. We designed a stu... more Little is known about avian taste perception and how taste affects food choice. We designed a study to determine the concentrations of aqueous solutions of common chemical taste stimuli that result in altered consumption patterns. Using twochoice taste-preference tests, we studied the taste thresholds of caged cockatiels (Nymphicus hollandicus) for aqueous solutions of potassium chloride, a phosphate buffer (to test pH), fructose, and glucose. First, the preferred and nonpreferred bottle locations were determined for each bird. Then, depending on the compound, the test solutions were placed in bottles in either the preferred or the nonpreferred locations and water was placed in the opposite bottle. Four parameters were measured at the end of 3-day test periods (total consumption, consumption from water side, consumption from test solution side, and proportion of nonpreferred side consumption to total consumption). Experiments were repeated with increasing concentrations of test flavors until intake variables were significantly affected (P < 0.05). Cockatiels distinguished (P < 0.05) between purified water and 0.16 mol L -1 potassium chloride, 0.40 mol L -1 fructose, or 0.16 mol L -1 glucose. The test birds did not distinguish between water and 0.05 mol L -1 mono-and dibasic sodium phosphate buffer solution at any tested pH within the range of 4.9-7.7. When these findings are compared to previous experiments with the same birds, it becomes clear that the gustatory reactions of cockatiels for two different stimuli (e.g., NaCl and KCl) from the same general taste category (salt, sweet, sour) can vary widely. This variation in the responses to related stimuli could be the result of a number of factors including anion effects (for salts and acids) as well as nongustatory physiological processes (e.g., as renal control of blood osmolarity).
Throughout the annual cycle, demands on competing physiological systems change, and animals must ... more 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
Proceedings of the Royal Society B: Biological Sciences, 2006
Generally, immune system architecture varies with different environments, which presumably reflec... more 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.
Proceedings of the Royal Society B: Biological Sciences, 2006
Understanding immune function in the context of other life-history traits is crucial to understan... more 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.
Proceedings of the Royal Society B: Biological Sciences, 2006
An increased susceptibility to disease is one hypothesis explaining how inbreeding hastens extinc... more 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.
A central hypothesis of ecological immunology is that immune defences are traded off against comp... more A central hypothesis of ecological immunology is that immune defences are traded off against competing physiological and behavioural processes. During energetically demanding periods, birds are predicted to switch from expensive inflammatory responses to less costly immune responses. Acute phase responses (APRs) are a particularly costly form of immune defence, and, hence, seasonal modulations in APRs are expected. Yet, hypotheses about APR modulation remain untested in freeliving organisms throughout a complete annual cycle. We studied seasonal modulations in the APRs and in the energy budgets of skylarks Alauda arvensis, a partial migrant bird from temperate zones that experiences substantial ecological changes during its annual cycle. We characterized throughout the annual cycle changes in their energy budgets by measuring basal metabolic rate (BMR) and body mass. We quantified APRs by measuring the effects of a lipopolysaccharide injection on metabolic rate, body mass, body temperature, and concentrations of glucose and ketone. Body mass and BMR were lowest during breeding, highest during winter and intermediate during spring migration, moult and autumn migration. Despite this variation in energy budgets, the magnitude of the APR, as measured by all variables, was similar in all annual cycle stages. Thus, while we find evidence that some annual cycle stages are relatively more energetically constrained, we find no support for the hypothesis that during these annual cycle stages birds compromise an immune defence that is itself energetically costly. We suggest that the ability to mount an APR may be so essential to survival in every annual cycle stage that skylarks do not trade off this costly form of defence with other annual cycle demands.
The immune system is a complex collection of interrelated and overlapping solutions to the proble... more The immune system is a complex collection of interrelated and overlapping solutions to the problem of disease. To deal with this complexity, researchers have devised multiple ways to measure immune function and to analyze the resulting data. In this way both organisms and researchers employ many tactics to solve a complex problem. One challenge facing ecological immunologists is the question of how these many dimensions of immune function can be synthesized to facilitate meaningful interpretations and conclusions. We tackle this challenge by employing and comparing several statistical methods, which we used to test assumptions about how multiple aspects of immune function are related at different organizational levels. We analyzed three distinct datasets that characterized 1) species, 2) subspecies, and 3) among-and within-individual level differences in the relationships among multiple immune indices. Specifically, we used common principal components analysis (CPCA) and two simpler approaches, pair-wise correlations and correlation circles. We also provide a simple example of how these techniques could be used to analyze data from multiple studies. Our findings lead to several general conclusions. First, relationships among indices of immune function may be consistent among some organizational groups (e.g. months over the annual cycle) but not others (e.g. species); therefore any assumption of consistency requires testing before further analyses. Second, simple statistical techniques used in conjunction with more complex multivariate methods give a clearer and more robust picture of immune function than using complex statistics alone. Moreover, these simpler approaches have potential for analyzing comparable data from multiple studies, especially as the field of ecological immunology moves towards greater methodological standardization.
Island organisms face a range of extrinsic threats to their characteristically small populations.... more Island organisms face a range of extrinsic threats to their characteristically small populations. Certain biological differences between island and continental organisms have the potential to exacerbate these threats. Understanding how island birds differ from their continental relatives may provide insight into population viability and serve as a predictive tool for conservation efforts. We compared an eastern bluebird population in Ohio with a threatened population in Bermuda in terms of the birds' development, morphology, immunology, and reproduction. These comparisons revealed that island nestlings had shorter wings and island adults had longer wings than their continental analogs. Island nestlings also had shorter tarsi than continental nestlings at day 8 posthatch, but this difference was absent at day 15 and in adults. Adults weighed less in Bermuda than in Ohio, and both nestlings and adults in Bermuda exhibited higher levels of two immunological indexes (concentrations of an acute-phase protein and titers of nonspecific antibodies). Clutch sizes and hatch rates did not differ between the island and continental populations; however, as the breeding season progressed, brood sizes declined in Bermuda, whereas no such decline occurred in Ohio. Despite these differences and differences in nestling development, island and continental parents fed their nestlings at equal rates. Overall, our results suggest that the Bermuda phenotype may be ad-justed to certain aspects of the island environment but not to others. Efforts to conserve the bluebirds of Bermuda may be improved by focusing on the intraseasonal patterns in nestling mortality and, more generally, the survival probabilities of different age classes.
Using a simple technique for assessing constitutive innate immune function recently adapted for u... more Using a simple technique for assessing constitutive innate immune function recently adapted for use in wild populations, we characterize changes in avian immune system development by repeated measurements of individuals over the period of nestling growth in a wild population of Leach's Storm-Petrels ( Oceanodroma leucorhoa ). 2. We measured levels of natural antibodies (NAb) during the early, middle and late phases of storm-petrel development and related these levels and NAb rate of change to mass and wing length growth. We used natural variation in nestling growth to assess the influence of nutritional status on the development of innate immunity. 3. NAb levels increased over the first 50 days of chick development; however, rate of increase was inversely proportional to wing growth. 4. Initial titre levels were inversely proportional to rate of change in NAb levels over the first 50 days of immune development. This suggests that individuals with low initial NAb levels accelerate immune development to reach adult levels, whereas individuals with high initial levels do not. 5. As in previous studies, our results demonstrate an inverse relationship between growth rate and development of components of the avian immune system. While such a relationship is consistent with the idea that immune function development involves trade-offs, the processes involved are more complex than simple energy allocation.
. The taste thresholds of caged cockatiels Nymphicus hollandicus for aqueous solutions of sodium ... more . The taste thresholds of caged cockatiels Nymphicus hollandicus for aqueous solutions of sodium chloride, citric acid, and sucrose were studied using two-choice taste-preference tests. The effects of location on the threshold were tested by putting the flavored solution in either the Ž . preferred or non-preferred locations i.e. sides of cages and offering water in the opposite Ž location. Four parameters total consumption, consumption from preferred side, consumption from . non-preferred side, and proportion of test solution consumed were measured at the end of 3-day test periods. Experiments were repeated with increasing concentrations of test flavors until intake Ž . variables were significantly p -0.05 affected. The results showed that birds distinguished Ž .
The rejection thresholds of caged cockatiels (Nymphicus hollandicus) were tested to determine the... more The rejection thresholds of caged cockatiels (Nymphicus hollandicus) were tested to determine their sensitivity to plant secondary compounds. Both alkaloids and tannins were tested using a two-bottle method in which purified water was always available in one bottle and an aqueous test solution was available in the other bottle. After each 3-day experimental period, three consumption parameters were recorded (test solution-side consumption, water-side consumption, and a ratio of test solution-side consumption to total consumption). Repeated test periods were conducted with increasingly concentrated test solutions of each compound until one or more consumption parameters were significantly (P < 0.05) affected. The results demonstrate that cockatiels prefer purified water to 100 mol l −1 quinine, 1000 mol l −1 gramine, 500 mol l −1 hydrolysable tannin, and 10,000 mol l −1 condensed tannin. These thresholds for secondary compounds were determined at concentrations that were 16-3900-times more dilute than the thresholds detected for salts and sugars. Moreover, in contrast to the generalization that taste acuity is poorer in birds than in mammals, the data demonstrate that the granivorous cockatiels actually reject quinine at lower concentrations than phytophagic mammals. These findings support the hypothesis that cockatiels use taste to detect, monitor, and possibly avoid intake of potentially toxic compounds.
Proceedings of The Royal Society B: Biological Sciences, 2006
Understanding immune function in the context of other life-history traits is crucial to understan... more 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
Little is known about avian taste perception and how taste affects food choice. We designed a stu... more Little is known about avian taste perception and how taste affects food choice. We designed a study to determine the concentrations of aqueous solutions of common chemical taste stimuli that result in altered consumption patterns. Using two-choice taste-preference tests, we studied the taste thresholds of caged cockatiels (Nymphicus hollandicus) for aqueous solutions of potassium chloride, a phosphate buffer (to test pH), fructose, and glucose. First, the preferred and nonpreferred bottle locations were determined for each bird. Then, depending on the compound, the test solutions were placed in bottles in either the preferred or the nonpreferred locations and water was placed in the opposite bottle. Four parameters were measured at the end of 3-day test periods (total consumption, consumption from water side, consumption from test solution side, and proportion of nonpreferred side consumption to total consumption). Experiments were repeated with increasing concentrations of test fla...
Introduction: All bird eggs are exposed to microbes in the environment, which if transmitted to t... more Introduction: All bird eggs are exposed to microbes in the environment, which if transmitted to the developing embryo, could cause hatching failure. However, the risk of trans-shell infection varies with environmental conditions and is higher for eggs laid in wetter environments. This might relate to generally higher microbial abundances and diversity in more humid environments, including on the surface of eggshells, as well as the need for moisture to facilitate microbial penetration of the eggshell. To protect against microbial infection, the albumen of avian eggs contains antimicrobial proteins, including lysozyme and ovotransferrin. We tested whether lysozyme and ovotransferrin activities varied in eggs of larks (Alaudidae) living along an arid-mesic gradient of environmental aridity, which we used as a proxy for risk of trans-shell infection. Results: Contrary to expectations, lysozyme activity was highest in eggs from hotter, more arid locations, where we predicted the risk of trans-shell infection would be lower. Ovotransferrin concentrations did not vary with climatic factors. Temperature was a much better predictor of antimicrobial protein activity than precipitation, a result inconsistent with studies stressing the importance of moisture for trans-shell infection.
Wildlife pathogens can alter host fitness. Low pathogenic avian influenza virus (LPAIV) infection... more Wildlife pathogens can alter host fitness. Low pathogenic avian influenza virus (LPAIV) infection is thought to have negligible impacts on wild birds; however, effects of infection in free-living birds are largely unstudied. We investigated the extent to which LPAIV infection and shedding were associated with body condition and immune status in free-living mallards (Anas platyrhynchos), a partially migratory key LPAIV host species. We sampled mallards throughout the species' annual autumn LPAIV infection peak, and we classified individuals according to age, sex, and migratory strategy (based on stable hydrogen isotope analysis) when analyzing data on body mass and five indices of immune status. Body mass was similar for LPAIV-infected and noninfected birds. The degree of virus shedding from the cloaca and oropharynx was not associated with body mass. LPAIV infection and shedding were not associated with natural antibody (NAbs) and complement titers (first lines of defense against infections), concentrations of the acute phase protein haptoglobin (Hp), ratios of heterophils to lymphocytes (H:L ratio), and avian influenza virus (AIV)-specific antibody concentrations. NAbs titers were higher in LPAIV-infected males and local (i.e., short distance) migrants than in infected females and distant (i.e., long distance) migrants. Hp concentrations were higher in LPAIV-infected juveniles and females compared to infected adults and males. NAbs, complement, and Hp levels were lower in LPAIV-infected mallards in early autumn. Our study demonstrates weak associations between infection with and shedding of LPAIV and the body condition and immune status of free-living mallards. These results may support the role of mallards as asymptomatic carriers of LPAIV and raise questions about possible coevolution between virus and host.
To contribute to an understanding of the evolutionary processes that shape variation in immune re... more 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
In wild birds, relatively little is known about intra- or inter- specific variation in immunologi... more In wild birds, relatively little is known about intra- or inter- specific variation in immunological capabilities, and even less is known about the effects of stress on immune function. Im- munological 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
Developmental and Comparative Immunology - DEVELOP COMP IMMUNOL, 2005
Methods to assess immunocompetence requiring only a single sample are useful in comparative studi... more Methods to assess immunocompetence requiring only a single sample are useful in comparative studies where practical considerations prevent holding or recapturing individuals. The assay for natural antibody-mediated complement activation and red blood cell agglutination described here, requiring ∼100μl of blood, is highly repeatable. The effects of complement deactivation, 2-mercaptoethanol (2-ME), age, and lipopolysaccharide (LPS)-induced sickness response were examined to validate comparisons among diverse avian species. Complement deactivation by heating significantly reduces lysis and treatment with 2-ME reduces both lysis and agglutination. Lysis and agglutination both increase with age in chickens; LPS treatment does not influence these variables in 11-week-old chickens. In a comparison of 11 species, both lysis (0.0–5.3 titers) and agglutination (1.8–8.0 titers) vary significantly among species. Accordingly, this assay can be used to compare constitutive innate humoral immunit...
Journal of Avian Medicine and Surgery - J AVIAN MED SURG, 2001
... Journal of Avian Medicine and Surgery 15(4):257-275. 2001 doi: 10.1647/1082-6742(2001) 015[02... more ... Journal of Avian Medicine and Surgery 15(4):257-275. 2001 doi: 10.1647/1082-6742(2001) 015[0257:NOBITO]2.0.CO;2. Nutrition of Birds in the Order Psittaciformes: A Review. Elizabeth A. KoutsosMS, Kevin D. MatsonMS, Kirk C. KlasingMS, PhD. ...
Little is known about avian taste perception and how taste affects food choice. We designed a stu... more Little is known about avian taste perception and how taste affects food choice. We designed a study to determine the concentrations of aqueous solutions of common chemical taste stimuli that result in altered consumption patterns. Using twochoice taste-preference tests, we studied the taste thresholds of caged cockatiels (Nymphicus hollandicus) for aqueous solutions of potassium chloride, a phosphate buffer (to test pH), fructose, and glucose. First, the preferred and nonpreferred bottle locations were determined for each bird. Then, depending on the compound, the test solutions were placed in bottles in either the preferred or the nonpreferred locations and water was placed in the opposite bottle. Four parameters were measured at the end of 3-day test periods (total consumption, consumption from water side, consumption from test solution side, and proportion of nonpreferred side consumption to total consumption). Experiments were repeated with increasing concentrations of test flavors until intake variables were significantly affected (P < 0.05). Cockatiels distinguished (P < 0.05) between purified water and 0.16 mol L -1 potassium chloride, 0.40 mol L -1 fructose, or 0.16 mol L -1 glucose. The test birds did not distinguish between water and 0.05 mol L -1 mono-and dibasic sodium phosphate buffer solution at any tested pH within the range of 4.9-7.7. When these findings are compared to previous experiments with the same birds, it becomes clear that the gustatory reactions of cockatiels for two different stimuli (e.g., NaCl and KCl) from the same general taste category (salt, sweet, sour) can vary widely. This variation in the responses to related stimuli could be the result of a number of factors including anion effects (for salts and acids) as well as nongustatory physiological processes (e.g., as renal control of blood osmolarity).
Throughout the annual cycle, demands on competing physiological systems change, and animals must ... more 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
Proceedings of the Royal Society B: Biological Sciences, 2006
Generally, immune system architecture varies with different environments, which presumably reflec... more 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.
Proceedings of the Royal Society B: Biological Sciences, 2006
Understanding immune function in the context of other life-history traits is crucial to understan... more 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.
Proceedings of the Royal Society B: Biological Sciences, 2006
An increased susceptibility to disease is one hypothesis explaining how inbreeding hastens extinc... more 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.
A central hypothesis of ecological immunology is that immune defences are traded off against comp... more A central hypothesis of ecological immunology is that immune defences are traded off against competing physiological and behavioural processes. During energetically demanding periods, birds are predicted to switch from expensive inflammatory responses to less costly immune responses. Acute phase responses (APRs) are a particularly costly form of immune defence, and, hence, seasonal modulations in APRs are expected. Yet, hypotheses about APR modulation remain untested in freeliving organisms throughout a complete annual cycle. We studied seasonal modulations in the APRs and in the energy budgets of skylarks Alauda arvensis, a partial migrant bird from temperate zones that experiences substantial ecological changes during its annual cycle. We characterized throughout the annual cycle changes in their energy budgets by measuring basal metabolic rate (BMR) and body mass. We quantified APRs by measuring the effects of a lipopolysaccharide injection on metabolic rate, body mass, body temperature, and concentrations of glucose and ketone. Body mass and BMR were lowest during breeding, highest during winter and intermediate during spring migration, moult and autumn migration. Despite this variation in energy budgets, the magnitude of the APR, as measured by all variables, was similar in all annual cycle stages. Thus, while we find evidence that some annual cycle stages are relatively more energetically constrained, we find no support for the hypothesis that during these annual cycle stages birds compromise an immune defence that is itself energetically costly. We suggest that the ability to mount an APR may be so essential to survival in every annual cycle stage that skylarks do not trade off this costly form of defence with other annual cycle demands.
The immune system is a complex collection of interrelated and overlapping solutions to the proble... more The immune system is a complex collection of interrelated and overlapping solutions to the problem of disease. To deal with this complexity, researchers have devised multiple ways to measure immune function and to analyze the resulting data. In this way both organisms and researchers employ many tactics to solve a complex problem. One challenge facing ecological immunologists is the question of how these many dimensions of immune function can be synthesized to facilitate meaningful interpretations and conclusions. We tackle this challenge by employing and comparing several statistical methods, which we used to test assumptions about how multiple aspects of immune function are related at different organizational levels. We analyzed three distinct datasets that characterized 1) species, 2) subspecies, and 3) among-and within-individual level differences in the relationships among multiple immune indices. Specifically, we used common principal components analysis (CPCA) and two simpler approaches, pair-wise correlations and correlation circles. We also provide a simple example of how these techniques could be used to analyze data from multiple studies. Our findings lead to several general conclusions. First, relationships among indices of immune function may be consistent among some organizational groups (e.g. months over the annual cycle) but not others (e.g. species); therefore any assumption of consistency requires testing before further analyses. Second, simple statistical techniques used in conjunction with more complex multivariate methods give a clearer and more robust picture of immune function than using complex statistics alone. Moreover, these simpler approaches have potential for analyzing comparable data from multiple studies, especially as the field of ecological immunology moves towards greater methodological standardization.
Island organisms face a range of extrinsic threats to their characteristically small populations.... more Island organisms face a range of extrinsic threats to their characteristically small populations. Certain biological differences between island and continental organisms have the potential to exacerbate these threats. Understanding how island birds differ from their continental relatives may provide insight into population viability and serve as a predictive tool for conservation efforts. We compared an eastern bluebird population in Ohio with a threatened population in Bermuda in terms of the birds' development, morphology, immunology, and reproduction. These comparisons revealed that island nestlings had shorter wings and island adults had longer wings than their continental analogs. Island nestlings also had shorter tarsi than continental nestlings at day 8 posthatch, but this difference was absent at day 15 and in adults. Adults weighed less in Bermuda than in Ohio, and both nestlings and adults in Bermuda exhibited higher levels of two immunological indexes (concentrations of an acute-phase protein and titers of nonspecific antibodies). Clutch sizes and hatch rates did not differ between the island and continental populations; however, as the breeding season progressed, brood sizes declined in Bermuda, whereas no such decline occurred in Ohio. Despite these differences and differences in nestling development, island and continental parents fed their nestlings at equal rates. Overall, our results suggest that the Bermuda phenotype may be ad-justed to certain aspects of the island environment but not to others. Efforts to conserve the bluebirds of Bermuda may be improved by focusing on the intraseasonal patterns in nestling mortality and, more generally, the survival probabilities of different age classes.
Using a simple technique for assessing constitutive innate immune function recently adapted for u... more Using a simple technique for assessing constitutive innate immune function recently adapted for use in wild populations, we characterize changes in avian immune system development by repeated measurements of individuals over the period of nestling growth in a wild population of Leach's Storm-Petrels ( Oceanodroma leucorhoa ). 2. We measured levels of natural antibodies (NAb) during the early, middle and late phases of storm-petrel development and related these levels and NAb rate of change to mass and wing length growth. We used natural variation in nestling growth to assess the influence of nutritional status on the development of innate immunity. 3. NAb levels increased over the first 50 days of chick development; however, rate of increase was inversely proportional to wing growth. 4. Initial titre levels were inversely proportional to rate of change in NAb levels over the first 50 days of immune development. This suggests that individuals with low initial NAb levels accelerate immune development to reach adult levels, whereas individuals with high initial levels do not. 5. As in previous studies, our results demonstrate an inverse relationship between growth rate and development of components of the avian immune system. While such a relationship is consistent with the idea that immune function development involves trade-offs, the processes involved are more complex than simple energy allocation.
. The taste thresholds of caged cockatiels Nymphicus hollandicus for aqueous solutions of sodium ... more . The taste thresholds of caged cockatiels Nymphicus hollandicus for aqueous solutions of sodium chloride, citric acid, and sucrose were studied using two-choice taste-preference tests. The effects of location on the threshold were tested by putting the flavored solution in either the Ž . preferred or non-preferred locations i.e. sides of cages and offering water in the opposite Ž location. Four parameters total consumption, consumption from preferred side, consumption from . non-preferred side, and proportion of test solution consumed were measured at the end of 3-day test periods. Experiments were repeated with increasing concentrations of test flavors until intake Ž . variables were significantly p -0.05 affected. The results showed that birds distinguished Ž .
The rejection thresholds of caged cockatiels (Nymphicus hollandicus) were tested to determine the... more The rejection thresholds of caged cockatiels (Nymphicus hollandicus) were tested to determine their sensitivity to plant secondary compounds. Both alkaloids and tannins were tested using a two-bottle method in which purified water was always available in one bottle and an aqueous test solution was available in the other bottle. After each 3-day experimental period, three consumption parameters were recorded (test solution-side consumption, water-side consumption, and a ratio of test solution-side consumption to total consumption). Repeated test periods were conducted with increasingly concentrated test solutions of each compound until one or more consumption parameters were significantly (P < 0.05) affected. The results demonstrate that cockatiels prefer purified water to 100 mol l −1 quinine, 1000 mol l −1 gramine, 500 mol l −1 hydrolysable tannin, and 10,000 mol l −1 condensed tannin. These thresholds for secondary compounds were determined at concentrations that were 16-3900-times more dilute than the thresholds detected for salts and sugars. Moreover, in contrast to the generalization that taste acuity is poorer in birds than in mammals, the data demonstrate that the granivorous cockatiels actually reject quinine at lower concentrations than phytophagic mammals. These findings support the hypothesis that cockatiels use taste to detect, monitor, and possibly avoid intake of potentially toxic compounds.
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Papers by Kevin Matson