12 research outputs found
Avian life in a seasonally arid tropical environment: Adaptations and mechanisms in breeding, moult and immune function
There is a growing appreciation of the diversity and uniqueness of tropical organisms, but evidence about the selection pressures that shape this diversity remains sketchy. In this thesis, I investigated how variation in life history traits arises from tropical environmental seasonality, starting with exploration of the annual cycle of the Common Bulbul Pycnonotus barbatus in Nigeria. This revealed that breeding was not seasonal, but moult was timed almost entirely to the wet season with only few individuals moulting into the dry season, suggesting that breeding and to a lesser extent moult, are decoupled from season, allowing me to test how breeding and moult affect immune function independent of seasonal conditions. On testing this, I found that season explained variation in immune function better than breeding or moult, but unexpectedly, immune indices were higher in the dry season and during breeding, contrary to expectations that infection risk is higher in the wet season, and that breeding constrains resources for immune function. Furthermore, I compared immune indices along the cool-wet to hot-dry environmental gradient in Nigeria and found that immune indices were rather similar. I then tested the effect of diet alteration on immune function, body mass and moult of bulbuls in captivity and found that bulbuls fed on fruits had better immune function, body mass and moult than those fed on invertebrates. These findings together suggest environmental conditions affect immune function more directly than via resource allocation trade-offs, but that variation in immune function does not follow simple environmental productivity pattern
Body reserves in intra-African migrants
Avian migration has been shown to be a life history strategy for surviving environmental resource variability, but it requires increased body reserves for long distance flight. Fat reserves make excellent energy stores for barrier crossing, whereas proteins generate less energy for the same mass of fat but provide water during breakdown which may become especially useful when birds become water stressed. Intra-African migrants are probably unlikely to have to cross barriers equivalent to the Sahara and the Mediterranean and so may have different patterns of mass reserves reflecting the utility of metabolizing fat versus protein in hot, tropical environments. We examined differences in proportions of body mass gain, pectoral muscle score and fat score between intra African migrants, Palearctic migrants and resident African species. We tested whether intra-African migrants show a distinct seasonal peak in mass gain corresponding to expected peak migration period in a manner similar to Palearctic migrants, but maintain larger muscle tissues, because Palearctic migrants are more constrained by a need to heavily up regulate fat in addition to fat free reserves before migration due to the energy requirements of crossing the barrier of the Sahara. We found that intra-African migrants had a peak seasonal mass gain similar to Palearctics whereas African residents did not, and that Palearctics increased fat reserves with pectoral muscle reserves, so that they had much higher fat scores for any given level of pectoral muscle compared to intra-African migrants or resident species. Our results suggest that barrier crossing leads to a distinct increase in fat reserves rather than migration per se, and suggests that intra-African migrants are more similar in their reserve management to African residents. Mass gain devoid of visible fat accumulation in intra-African migrants may therefore suggest absence of barriers during migrationPeer reviewe
Avian life in a seasonally arid tropical environment:Adaptations and mechanisms in breeding, moult and immune function
There is a growing appreciation of the diversity and uniqueness of tropical organisms, but evidence about the selection pressures that shape this diversity remains sketchy. In this thesis, I investigated how variation in life history traits arises from tropical environmental seasonality, starting with exploration of the annual cycle of the Common Bulbul Pycnonotus barbatus in Nigeria. This revealed that breeding was not seasonal, but moult was timed almost entirely to the wet season with only few individuals moulting into the dry season, suggesting that breeding and to a lesser extent moult, are decoupled from season, allowing me to test how breeding and moult affect immune function independent of seasonal conditions. On testing this, I found that season explained variation in immune function better than breeding or moult, but unexpectedly, immune indices were higher in the dry season and during breeding, contrary to expectations that infection risk is higher in the wet season, and that breeding constrains resources for immune function. Furthermore, I compared immune indices along the cool-wet to hot-dry environmental gradient in Nigeria and found that immune indices were rather similar. I then tested the effect of diet alteration on immune function, body mass and moult of bulbuls in captivity and found that bulbuls fed on fruits had better immune function, body mass and moult than those fed on invertebrates. These findings together suggest environmental conditions affect immune function more directly than via resource allocation trade-offs, but that variation in immune function does not follow simple environmental productivity pattern
Avian life in a seasonally arid tropical environment:Adaptations and mechanisms in breeding, moult and immune function
There is a growing appreciation of the diversity and uniqueness of tropical organisms, but evidence about the selection pressures that shape this diversity remains sketchy. In this thesis, I investigated how variation in life history traits arises from tropical environmental seasonality, starting with exploration of the annual cycle of the Common Bulbul Pycnonotus barbatus in Nigeria. This revealed that breeding was not seasonal, but moult was timed almost entirely to the wet season with only few individuals moulting into the dry season, suggesting that breeding and to a lesser extent moult, are decoupled from season, allowing me to test how breeding and moult affect immune function independent of seasonal conditions. On testing this, I found that season explained variation in immune function better than breeding or moult, but unexpectedly, immune indices were higher in the dry season and during breeding, contrary to expectations that infection risk is higher in the wet season, and that breeding constrains resources for immune function. Furthermore, I compared immune indices along the cool-wet to hot-dry environmental gradient in Nigeria and found that immune indices were rather similar. I then tested the effect of diet alteration on immune function, body mass and moult of bulbuls in captivity and found that bulbuls fed on fruits had better immune function, body mass and moult than those fed on invertebrates. These findings together suggest environmental conditions affect immune function more directly than via resource allocation trade-offs, but that variation in immune function does not follow simple environmental productivity pattern
Local timing of rainfall predicts the timing of moult within a single locality and the progress of moult among localities that vary in the onset of the wet season in a year-round breeding tropical songbird
Funding: C.J.N. was supported by a studentship funded by the Leventis Conservation Foundation through the University of St. Andrews, UK and an Ubbo Emmius grant of the University of Groningen.Rainfall seasonality is likely an important cue for timing key annual cycle events like moult in birds living in seasonally arid environments, but its precise effect is difficult to establish because seasonal rainfall may affect other covarying annual events such as breeding in the same way. In central Nigeria, however, Common Bulbuls Pycnonotus barbatus moult in the wet season but only show weak breeding seasonality. This suggests that moult is more sensitive to rainfall than breeding, but a similar outcome is possible if moult is simply periodic. We tested the relationship between rainfall and moult in Common Bulbuls at a single location over 18 years: on average moult started 5th May (± 41 days: 25th March–15th June), being on average later than the onset of the rains which is usually mid-April. The likelihood of finding a moulting Common bulbul was best predicted by rainfall 9–15 weeks before moult was scored. We then tested the generality of this across populations: the progress of moult should, therefore, correlate with the average timing of the wet season along a spatial environmental gradient where the rains start at different times each year south-to-north of Nigeria. To test this, we modelled moult progress just before the rains across 15 localities 6°–13° N as a function of the onset of the wet season among localities. As predicted, moult progressed further in localities with earlier wet seasons, confirming that the onset of moult is timed to the onset of the wet season in each locality despite weak breeding seasonality in the Common Bulbul. This strategy may evolve to maintain optimal annual cycle routine in seasonal environments where breeding is prone to unpredictable local perturbations like nest predation. It may, however, be less obvious in temperate systems where all annual cycle stages are seasonally constrained, but it may help with explaining the high frequency of breeding–moult overlaps in tropical birds.Peer reviewe
Geographic variation in baseline innate immune function does not follow variation in aridity along a tropical environmental gradient
C.J.N. was supported by a studentship funded by the Leventis Conservation Foundation through the University of St. Andrews, UK and an Ubbo Emmius grant of the University of Groningen. B.I.T. was supported by the Netherlands Organisation for Scientific Research (NWO-Vidi 864.10.012). This is publication number 141 of the A.P. Leventis Ornithological Research Institute, Nigeria and chapter 7 of the thesis ‘Avian life in a seasonally arid tropical environment: adaptations and mechanisms in breeding, molt and immune function’91, submitted for the award of a doctorate degree by the University of Groningen, the Netherlands and University of St. Andrews, UK.Geographic variation in aridity determines environmental productivity patterns, including large-scale variability in pathogens, vectors and associated diseases. If disease risk decreases with increasing aridity and is matched by immune defense, we predict a decrease in innate immune function along a gradient of increasing aridity from the cool-wet forest to the hot-dry Sahel, from south to north in Nigeria. We sampled blood and measured five innate immune indices from 286 Common Bulbuls Pycnonotus barbatus between 6 and 13°N. We sampled in the dry season; we resampled the first location (Jos) also as the last sample location to test temporal change in immune function. Immune indices did not decrease with aridity. One immune index, nitric oxide concentration showed a weak quadratic pattern. In Jos, ovotransferrin concentration, haemagglutination and haemolysis titres increased 12 weeks into the dry season, contrary to expectations that immune indices should decrease with increased dryness. In this tropical system, innate immune function does not decrease with increasing aridity but temporal factors within a location may influence immune function more strongly than spatial variation in aridity, suggesting that immune variation does not follow a simple environmental productivity pattern. Consequently, caution should probably be exercised in predicting effects of climate variability on immune function or disease risk.Peer reviewe
Temperature and aridity determine body size conformity to Bergmann’s rule independent of latitudinal differences in a tropical environment
C.J.N. was supported by a studentship funded by the Leventis Conservation Foundation through the University of St. Andrews, UK.Bergmann’s rule, defined as the tendency for endotherms to be larger in colder environments, is a biophysical generalization of body size variation that is frequently tested along latitudinal gradients, even though latitude is only a proxy for temperature variation. We test whether variation in temperature and aridity determine avian body size conformity to Bergmann’s rule independent of latitude differences, using the ubiquitous Common Bulbul Pycnonotus barbatus, along a West African environmental gradient. We trapped 538 birds in 22 locations between latitudes 6 and 13°N in Nigeria, and estimated average body surface area to mass ratio per location. We then modelled body surface to mass ratio using general linear models, with latitude, altitude and one of 19 bioclimatic variables extracted from http://www.worldclim.org/bioclim as predictors. We sequentially dropped latitude and altitude from each model to obtain the R2 of the resultant models. Finally, we compared the R2 of univariate models, where bioclimatic variables predicted body surface area to mass ratio significantly (14 out of 19), to multivariate models including latitude, altitude and a bioclimatic variable, using the Wilcoxon matched pairs test. We found that multivariate models did not perform better than univariate models with only bioclimatic variables. Six temperature and eight precipitation variables significantly predicted variation in body surface area to mass ratio between locations; in fact, 50% (seven out of 14) of these better explained variation in body surface area to mass ratio than the multivariate models. Birds showed a larger body surface area relative to body mass ratio in hotter environments independent of latitude or altitude, which conforms to Bergmann’s rule. Yet, a combination of morphometric analyses and controlled temperature-exposure experiments is required to prove the proposed relationship between relative body surface area and thermoregulation in endotherms.Peer reviewe
Data for: Innate immune function and antioxidant capacity of nestlings of an African raptor co-vary with the level of urbanization around breeding territories
Urban areas provide breeding habitats for many species. However, animals raised in urban environments face challenges such as altered food availability and quality, pollution, and pathogens assemblages. These challenges can affect physiological processes like immune function and antioxidant defences which are important for fitness.
Here, we explore how levels of urbanisation influence innate immune function, immune response to a mimicked bacterial infection and antioxidant capacity of nestling Black Sparrowhawks Accipiter melanoleucus in South Africa. We also explore the effect of timing of breeding and rainfall on physiology since both can influence the environmental condition under which nestlings are raised. Finally, because urbanisation can influence immune function indirectly, we use path analyses to explore direct and indirect associations between urbanisation, immune function, and oxidative stress.
We obtained measures of innate immunity (haptoglobin, lysis, agglutination and bactericidal capacity), indices of antioxidant capacity (total non-enzymatic antioxidant capacity (tAOX), and total glutathione from nestlings from 2015 - 2019. In addition, in 2018 and 2019, we mimicked a bacterial infection by injecting nestlings with lipopolysaccharide and quantified their immune response.
Increased urban cover was associated with an increase in lysis and a decrease in tAOX, but not with any of the other physiological parameters. Furthermore, except for agglutination, no physiological parameters were associated with the timing of breeding. Lysis and bactericidal capacity, however, varied consistently with the annual rainfall pattern. Immune response to a mimicked a bacterial infection decreased with urban cover but not with the timing of breeding nor rainfall. Our path analyses suggested indirect associations between urban cover and some immune indices via tAOX but not via the timing of breeding.
Our results show that early-life development in an urban environment is associated with variation in immune and antioxidant functions. The direct association between urbanisation and antioxidant capacity and their impact on immune function is likely an important factor mediating the impact of urbanisation on urban-dwelling animals. Future studies should explore how these results are linked to fitness and whether the responses are adaptive for urban-dwelling species.Funding provided by: National Research Foundation, South Africa*Crossref Funder Registry ID: Award Number:Field data including morphometric measurements, sampling history and individual identifiers of nestling of Black Sparrowhawk Accipiter melanoleucus, measures of immune function and antioxidant capacity generated from laboratory analyses of plasma and whole blood, estimation of cover around breeding territories using landcover images, and Cape Town rainfall data collected from the South African Weather Services. All data compiled in Office Microsoft Excel spreadsheets
A fruit diet rather than invertebrate diet maintains a robust innate immunity in an omnivorous tropical songbird
Diet alteration may lead to nutrient limitations even in the absence of food limitation, and this may affect physiological functions, including immunity. Nutrient limitations may also affect the maintenance of body mass and key life-history events that may affect immune function. Yet, variation in immune function is largely attributed to energetic trade-offs rather than specific nutrient constraints. To test the effect of diet on life-history traits, we tested how diet composition affects innate immune function, body mass and moult separately and in combination with each other, and then used path analyses to generate hypotheses about the mechanistic connections between immunity and body mass under different diet compositions. We performed a balanced parallel and crossover design experiment with omnivorous common bulbuls Pycnonotus barbatus in out-door aviaries in Nigeria. We fed 40 wild-caught bulbuls ad libitum on fruits or invertebrates for 24 weeks, switching half of each group between treatments after 12 weeks. We assessed innate immune indices (haptoglobin, nitric oxide and ovotransferrin concentrations, and haemagglutination and haemolysis titres), body mass and primary moult, fortnightly. We simplified immune indices into three principal components (PCs), but we explored mechanistic connections between diet, body mass and each immune index separately. Fruit-fed bulbuls had higher body mass, earlier moult and showed higher values for two of the three immune PCs compared to invertebrate-fed bulbuls. These effects were reversed when we switched bulbuls between treatments after 12 weeks. Exploring the correlations between immune function, body mass and moult, showed that an increase in immune function was associated with a decrease in body mass and delayed moult in invertebrate-fed bulbuls, while fruit-fed bulbuls maintained body mass despite variation in immune function. Path analyses indicated that diet composition was most likely to affect body mass and immune indices directly and independently from each other. Only haptoglobin concentration was indirectly linked to diet composition via body mass. We demonstrated a causal effect of diet composition on innate immune function, body mass and moult: bulbuls were in a better condition when fed on fruits than invertebrates, confirming that innate immunity is nutrient specific. Our results are unique because they show a reversible effect of diet composition on wild adult birds whose immune systems are presumably fully developed and adapted to wild conditions-demonstrating a short-term consequence of diet alteration on life-history traits.</p
Innate immune function and antioxidant capacity of nestlings of an African raptor covary with the level of urbanisation around breeding territories [Elektronisk resurs]
Urban areas provide breeding habitats for many species. However, animals raised in urban environments face challenges such as altered food availability and quality, pollution and pathogen assemblages. These challenges can affect physiological processes such as immune function and antioxidant defences which are important for fitness. Here, we explore how levels of urbanisation influence innate immune function, immune response to a mimicked bacterial infection and antioxidant capacity of nestling Black Sparrowhawks Accipiter melanoleucus in South Africa. We also explore the effect of timing of breeding and rainfall on physiology since both can influence the environmental condition under which nestlings are raised. Finally, because urbanisation can influence immune function indirectly, we use path analyses to explore direct and indirect associations between urbanisation, immune function and oxidative stress. We obtained measures of innate immunity (haptoglobin, lysis, agglutination, bactericidal capacity), indices of antioxidant capacity (total non-enzymatic antioxidant capacity (tAOX) and total glutathione from nestlings from 2015 to 2019. In addition, in 2018 and 2019, we mimicked a bacterial infection by injecting nestlings with lipopolysaccharide and quantified their immune response. Increased urban cover was associated with an increase in lysis and a decrease in tAOX, but not with any of the other physiological parameters. Furthermore, except for agglutination, no physiological parameters were associated with the timing of breeding. Lysis and bactericidal capacity, however, varied consistently with the annual rainfall pattern. Immune response to a mimicked a bacterial infection decreased with urban cover but not with the timing of breeding nor rainfall. Our path analyses suggested indirect associations between urban cover and some immune indices via tAOX but not via the timing of breeding. Our results show that early-life development in an urban environment is associated with variation in immune and antioxidantfunctions. The direct association between urbanisation and antioxidant capacity and their impact on immune function is likely an important factor mediating the impact of urbanisation on urban-dwelling animals. Future studies should explore how these results are linked to fitness and whether the responses are adaptive for urban-dwelling species
