Implications of climate change on the reproductive success of the Southern Yellow-billed Hornbill, Tockus leucomelas

The effects of environmental warming on the reproductive performance of birds are most easily studied in desert habitats where birds already experience air temperatures (Tₐs) close to their upper thermal tolerance. Many desert birds coincide breeding with periods of food availability triggered by rainfall during the summer season. Daily maximum air temperatures (ₘₐₓ) during the Kalahari summer season frequently reach the lower forties (°C) and recent years have been characterised by reduced rainfall and increased Tₐ. Breeding Southern Yellow-billed Hornbills (Tockus leucomelas) could be particularly vulnerable to high Tₐ due to their breeding strategy whereby the females are confined to the nest cavity for most of the nesting period. During this time their male partners are solely responsible for food provisioning, which imposes a considerable energetic demand. In this thesis, I investigated the extent to which Tₐ affects the ability and willingness of breeding males to provision their female partners and offspring. And consequently, the extent to which male investment and the thermal environment affect female body mass (Mb) and chick development rates in Southern Yellowbilled Hornbills in the Kalahari. During three consecutive hornbill breeding seasons (October - March, between 2012 and 2015), I collected life history data during 50 breeding attempts by 32 hornbill pairs. At the study site, Southern Yellow-billed Hornbills readily breed in artificial nest boxes and this allowed me to assess the internal nest climate using temperature and relative humidity loggers which were placed in most of the nests. The male hornbills in the study population were semi-habituated which facilitated behavioural observations. Weather data were recorded at an on-site weather station. Morphometric data from females and chicks were collected on a daily basis at selected nests and perch scales installed at nest entrances recorded Mb data of the provisioning males. From chick hatching to chick fledging, I observed the behaviour of the males during 30-min focal follows and focussed on foraging behaviour, prey allocation decisions (nest versus self), microsite use and thermoregulatory behaviour. Male hornbills spent more than half of their time panting at Tₐs above 34.5 °C. Days on which this threshold temperature was exceeded were therefore described as 'hot days'. The male hornbills experienced trade-offs on hot days between foraging efficiency and panting behaviour, indicating that the additional cost of thermoregulation and high Tₐ affected foraging success (Chapter 2). Males would always provision larger prey items to the nest and consumed the smaller prey items themselves. As Tₐ increased, the males increased their foraging effort, but caught fewer and smaller prey items overall, reducing the total biomass they provisioned to the nest as well as the biomass they consumed. As a result, males were unable to maintain their Mb on days when Tₐ exceeded 37.9 °C (Chapter 3). A similar effect of hot days on Mb maintenance was observed in females and chicks within the nest. Independent of chick age, females departed the nest when their Mb reached a lower limit of 189.3 ± SD 18.1 g. The females would then aid the males in nest provisioning, however the negative effect of increasing ₘₐₓ on provisioning rate was still evident; i.e. females were not able to compensate for reduced male provisioning rates on hot days. High Tₐs during the nesting period resulted in smaller and lighter fledglings and overall reduced the probability of a successful nesting attempt (Chapter 4). A thermal imaging experiment revealed that the large beak of hornbills (both males and females) plays an important role in non-evaporative heat loss. Hornbills were observed to dissipate up to 19.9 % of the total non-evaporative body heat loss via the beak. This water-saving mechanism can be highly advantageous to hornbills living in arid regions where water availability is limited (Chapter 5). Lastly, a comparison of the results of the current study with those of a study on the same hornbill population carried out between 2008 and 2011 revealed that mean ₘₐₓ as well as rainfall during the nesting period had an important impact on overall hornbill reproductive effort and success (Chapter 6). Long-lived species are expected to prioritise future reproductive opportunities over current broods. However, the predicted scenario for the Kalahari is that high Tₐs become more extreme and periods of drought become more frequent. Therefore, I predict an increased risk of breeding failure among Southern Yellow-billed Hornbills in the future which could affect the persistence of this population

Collapse of breeding success in desert-dwelling hornbills evident within a single decade

Rapid anthropogenic climate change potentially severely reduces avian breeding success. While the consequences of high temperatures and drought are reasonably well-studied within single breeding seasons, their impacts over decadal time scales are less clear. We assessed the effects of air temperature (Tair) and drought on the breeding output of southern yellow-billed hornbills (Tockus leucomelas; hornbills) in the Kalahari Desert over a decade (2008–2019). We aimed to document trends in breeding performance in an arid-zone bird during a time of rapid global warming and identify potential drivers of variation in breeding performance. The breeding output of our study population collapsed during the monitoring period. Comparing the first three seasons (2008–2011) of monitoring to the last three seasons (2016–2019), the mean percentage of nest boxes that were occupied declined from 52% to 12%, nest success from 58% to 17%, and mean fledglings produced per breeding attempt from 1.1 to 0.4. Breeding output was negatively correlated with increasing days on which Tmax (mean maximum daily Tair) exceeded the threshold Tair at which male hornbills show a 50% likelihood of engaging in heat dissipation behavior [i.e., panting (Tthresh; Tair = 34.5◦C)] and the occurrence of drought within the breeding season, as well as later dates for entry into the nest cavity (i.e., nest initiation) and fewer days post-hatch, spent incarcerated in the nest by the female parent. The apparent effects of high Tair were present even in non-drought years; of the 115 breeding attempts that were recorded, all 18 attempts that had ≥ 72% days during the attempt on which Tmax > Tthresh failed (equivalent to Tmax during the attempt ≥ 35.7◦C). This suggests that global warming was likely the primary driver of the recent, rapid breeding success collapse. Based on current warming trends, the Tmax threshold of 35.7◦C, above which no successful breeding attempts were recorded, will be exceeded during the entire hornbill breeding season by approximately 2027 at our study site. Therefore, our findings support the prediction that climate change may drive rapid declines and cause local extinctions despite the absence of direct lethal effects of extreme heat events.The DST-NRF Center of Excellence at the FitzPatrick Institute, Natural Environment Research Council, and the National Research Foundation of South Africa.http://frontiersin.org/Ecology_and_Evolutiondm2022Zoology and Entomolog

Seasonal Metabolic Variation in Two Populations of an Afrotropical Euplectid Bird

Many birds exhibit seasonal phenotypic flexibility in basal metabolic rate (BMR) and summit metabolism (Msum), but very little information is available for species from subtropical latitudes or for conspecific populations from sites that vary in climate. We measured body mass (Mb), BMR, and Msum in summer and winter in two populations of the southern red bishop Euplectes orix, a passerine that is widespread in southern Africa. One population occurs at a comparatively warmer coastal site (mean daily minimum air temperature [Ta] inmidwinter, 8.3 C) and the other at a colder inland site (mean daily minimum Ta in midwinter, 2.8 C). Bishops from both populations significantly increased Mb in winter. However, seasonal metabolic adjustments differed considerably between the populations. The inland population significantly increased BMR by approximately 58%, mass-specific BMR by approximately 31%, and Msum by approximately 15% in winter, although massspecific Msum did not change significantly. In contrast, the coastal population showed no significant seasonal change in BMR and significant winter reductions in mass-specific BMR (∼15%), Msum (∼8%), and mass-specific Msum (∼15%). The interpopulation differences in the magnitude and direction of seasonal mass-specific BMR changes are qualitatively consistent with global patterns, although the increase shown by the inland population is larger than expected. Our data reveal that avian seasonal metabolic adjustments can vary greatly within subtropical species depending on the climatic conditions experienced by the birds, and our findings reiterate the need to better understand metabolic flexibility in species that inhabit lower latitudes.The National Research Foundation (NRF) to N.M. and A.E.M.http://www.journals.uchicago.edu/toc/pbz/currentam2013ab201

How hornbills handle heat: sex-specific thermoregulation in the southern yellow-billed hornbill

At a global scale, thermal physiology is correlated with climatic variables such as temperature and aridity. There is also evidence that thermoregulatory traits vary with fine-scale microclimate, but this has received less attention in endotherms. Here, we test the hypothesis that avian thermoregulation varies with microclimate and behavioural constraints in a non-passerine bird. Male and female southern yellow-billed hornbills (Tockus leucomelas) experience markedly different microclimates while breeding, with the female sealing herself into a tree cavity and moulting all her flight feathers during the breeding attempt, becoming entirely reliant on the male for provisioning. We examined interactions between resting metabolic rate (RMR), evaporative water loss (EWL) and core body temperature (Tb) at air temperatures (Ta) between 30°C and 52°C in male and female hornbills, and quantified evaporative cooling efficiencies and heat tolerance limits. At thermoneutral Ta, neither RMR, EWL nor Tb differed between sexes. At Ta >40°C, however, RMR and EWL of females were significantly lower than those of males, by ∼13% and ∼17%, respectively, despite similar relationships between Tb and Ta, maximum ratio of evaporative heat loss to metabolic heat production and heat tolerance limits (∼50°C). These sex-specific differences in hornbill thermoregulation support the hypothesis that avian thermal physiology can vary within species in response to fine-scale microclimatic factors. In addition, Q10 for RMR varied substantially, with Q10 ≤2 in some individuals, supporting recent arguments that active metabolic suppression may be an underappreciated aspect of endotherm thermoregulation in the heat. 40°C, however, RMR and EWL of females were significantly lower than those of males, by ∼13% and ∼17%, respectively, despite similar relationships between Tb and Ta, maximum ratio of evaporative heat loss to metabolic heat production and heat tolerance limits (∼50°C). These sex-specific differences in hornbill thermoregulation support the hypothesis that avian thermal physiology can vary within species in response to fine-scale microclimatic factors. In addition, Q10 for RMR varied substantially, with Q10 ≤2 in some individuals, supporting recent arguments that active metabolic suppression may be an underappreciated aspect of endotherm thermoregulation in the heat

How hornbills handle heat: sex-specific thermoregulation in the southern yellow-billed hornbill

At a global scale, thermal physiology is correlated with climatic variables such as temperature and aridity. There is also evidence that thermoregulatory traits vary with fine-scale microclimate, but this has received less attention in endotherms. Here, we test the hypothesis that avian thermoregulation varies with microclimate and behavioural constraints in a non-passerine bird. Male and female southern yellow-billed hornbills (Tockus leucomelas) experience markedly different microclimates while breeding, with the female sealing herself into a tree cavity and moulting all her flight feathers during the breeding attempt, becoming entirely reliant on the male for provisioning. We examined interactions between resting metabolic rate (RMR), evaporative water loss (EWL) and core body temperature (Tb) at air temperatures (Ta) between 30°C and 52°C in male and female hornbills, and quantified evaporative cooling efficiencies and heat tolerance limits. At thermoneutral Ta, neither RMR, EWL nor Tb differed between sexes. At Ta >40°C, however, RMR and EWL of females were significantly lower than those of males, by ∼13% and ∼17%, respectively, despite similar relationships between Tb and Ta, maximum ratio of evaporative heat loss to metabolic heat production and heat tolerance limits (∼50°C). These sex-specific differences in hornbill thermoregulation support the hypothesis that avian thermal physiology can vary within species in response to fine-scale microclimatic factors. In addition, Q10 for RMR varied substantially, with Q10 ≤2 in some individuals, supporting recent arguments that active metabolic suppression may be an underappreciated aspect of endotherm thermoregulation in the heat

High PD-1 expression on regulatory and effector T-cells in lung cancer draining lymph nodes

The treatment of advanced nonsmall cell lung cancer (NSCLC) with PD-1/PD-L1 immune checkpoint inhibitors has improved clinical outcome for a proportion of patients. The current challenge is to find better biomarkers than PD-L1 immunohistochemistry (IHC) that will identify patients likely to benefit from this therapy. In this exploratory study we assessed the differences in T-cell subsets and PD-1 expression levels on T-cells in tumour-draining lymph nodes (TDLNs) and peripheral blood mononuclear cells (PBMCs). To evaluate this, flow cytometric analyses were performed on endobronchial ultrasound-guided (EBUS) fine-needle aspirates (FNA) from TDLNs of patients with NSCLC, and the results were compared to paired PBMC samples. For a select number of patients, we were also able to obtain cells from a non-TDLN (NTDLN) sample. Our data show that the frequency of PD-1+ CD4+ and CD8+ T-cells, as well as the PD-1 expression level on activated regulatory T (aTreg) and CD4+ and CD8+ T-cells, are higher in TDLNs than in PBMCs and, in a small sub-analysis, NTDLNs. These elevated PD-1 expression levels in TDLNs may reflect tumour-specific T-cell priming and conditioning, and may serve as a predictive or early-response biomarker during PD-1 checkpoint blockade

Comparative phenotypic and functional analysis of migratory dendritic cell subsets from human oral mucosa and skin

Antigen exposure to oral mucosa is generally thought to lead to immune tolerance induction. However, very little is known about the subset composition and function of dendritic cells (DC) migrating from human oral mucosa. Here we show that migratory DC from healthy human gingival explants consist of the same phenotypic subsets in the same frequency distribution as DC migrating from human skin. The gingival CD1a+ Langerhans cell and interstitial DC subsets lacked CXCR4 expression in contrast to their cutaneous counterparts, pointing to different migration mechanisms, consistent with previous observations in constructed skin and gingival equivalents. Remarkably, without any exogenous conditioning, gingival explants released higher levels of inflammatory cytokines than human skin explants, resulting in higher DC migration rates and a superior ability of migrated DC to prime allogeneic T cells and to induce type-1 effector T cell differentiation. From these observations we conclude that rather than an intrinsic ability to induce T cell tolerance, DC migrating from oral mucosa may have a propensity to induce effector T cell immunity and maintain a high state of alert against possible pathogenic intruders in the steady state. These findings may have implications for oral immunization strategies