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Birds undergo pronounced physiological changes during the reproduction, which may be linked to
their parental efforts. Examining these changes may supply information about the birds’ energy expenditure during the particular phases of breeding and help to understand birds’ decisions about their subsequent parental investments. In this study, we meas...
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... great many methods for correcting body mass for body size have been put forward (e.g. Albrecht et al. 1993; García-Berthou 2001; Schulte-Holstedde et al. 2005;Peig and Green 2009). Since there is no agreement about which one performs this correction in the most efficient way, we tested four different methods, all with overall head-bill length as surrogate measure of body size. We used this length as it is considered to be a representative measure- ment of the little auk's structural size (Jakubas and Wo- jczulanis 2007). Firstly, we corrected the body mass with the body condition index (BCI) sensu Albrecht et al. (1993). We computed it using the formula: BCI = M/L, where M is the body mass and L is the linear body mea- surement of an individual (Albrecht et al. 1993). Secondly, we corrected body mass using the residuals of a simple linear regression of body mass and linear body measure- ments following the recommendations of Schulte-Hol- stedde et al. (2005). Thirdly, we performed analysis of covariance (ANCOVA) with the linear body measurement being a covariate (García-Berthou 2001). Finally, we cal- culated the scaled mass index proposed by Peig and Green (2009). All these methods delivered qualitatively similar results in terms of the seasonal changes but differed in efficiency of the body mass to body size correction, which, in turn, affected the sex difference issue. Here, we present the results obtained using the method of Peig and Green (2009), which efficiently corrected body mass for body size. The results of the analyses performed with the other methods of body mass correction are given in the Sup- plementary material ...
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... this study, we investigated the seasonal dynamics of some physiological variables and their mutual relationships in a small (140-180 g) seabird, the little auk (Alle alle) ( Fig. 1), which nests in rock crevices on mountain slopes in the severe Arctic environment. The species is believed to have the highest mass-specific metabolic rate of all sea- birds ( Gabrielsen et al. 1991;Konarzewski et al. 1993). To satiate such high energy demands during the breeding season, these birds need to forage on specific, energy-rich prey which they obtain at distant foraging grounds (median 30-60 km, but sometimes up to 150 km from the breeding colony; Jakubas et al. 2012Jakubas et al. , 2013). Such reproductive de- mands are expected to affect the birds' body condition. Both parents share to an equal extent the 28-day incubation (Wojczulanis-Jakubas et al. 2009a), brood the chick (for the first few days after hatching) and deliver food to it with similar frequency ( Harding et al. 2004;WojczulanisJakubas et al. 2012). Only at the end of the chick rearing period (ca 26 d, Wojczulanis-Jakubas and Jakubas 2012) does the female desert the brood, while the male continues feeding and escorts the fledgling during its first flight to sea. It has been hypothesised that female brood desertion is related to her deteriorating body condition ( Harding et al. 2004). But how that could be the case, given the equal male and female contribution to parental care up to the moment of desertion, is unclear. It is possible that the costs of specific parental activities are different for males and females owing to the basic anatomical, physiological and behavioural differences between the sexes (e.g. Elliot et al. 2010). Although this issue has already been addressed, a limited range of physiological variables, never covering the whole breeding season, were examined ( Jakubas et al. 2008;; Wojczulanis- Jakubas and Jakubas ...
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Sex-biased mortality can occur in birds during development, for example due to sexual differences in energy requirement and/or environmental sensitivity, or the effects of sex hormones or sex differences in the expression of mutations linked to sex chromosomes. The extent of sex-bias in mortality may also be related to environmental conditions that...
Citations
... Residuals indices may have limitations compared to other metrics, mainly when comparing birds from different populations (Labocha and Hayes 2012). However, we consider it adequate for our purpose, since we are comparing individuals of the same species from the same location, as performed elsewhere (Andersson et al. 2002;Giraudeau et al. 2013Giraudeau et al. , 2014Wojczulanis-Jakubas et al. 2015;Salleh Hudin et al. 2016;Nip et al. 2018;da Silva Rodrigues et al. 2021). ...
Haemosporidian parasites, including Plasmodium, Haemoproteus, and Leucocytozoon genera, are vector-borne protists causing malaria-like diseases in birds. Juveniles are often more susceptible to infections, potentially becoming reservoirs within bird communities. However, we still understand little about other factors that may increase host susceptibility to haemosporidian parasites, mainly in terms of stress and overall health condition. Therefore, here, we investigated the complex interplay between haemosporidian parasites, plumage coloration, body condition, feather corticosterone concentration, and age. We captured individuals outside the breeding season in 2019 and screened 50 individuals of four different species (Basileuterus culicivorus, Myiothlypis leucoblephara, Haplospiza unicolor, and Conopophaga lineata) for haemosporidian parasites, and tested the predictions that individuals with higher levels of feather corticosterone, lower body condition, drabber plumage coloration, and that younger birds would have a higher haemosporidian parasite occurrence. Results revealed that feather corticosterone concentration and plumage color saturation were key predictors of haemosporidian occurrence. Birds with higher feather corticosterone and less-saturated plumage had a higher likelihood of infection. These findings shed light on the intricate connections between stress, immunity, and plumage coloration in wild bird populations, providing insights into avian health and condition.
... The estimate of Heterophile/Lymphocyte ratio (H/L) is a method used to evaluate the health of birds. The method is based on the microscopic differential count of leukocytes (leukocyte profile), and stands out as a good indicator of stress in birds, thus being a proxy for their health (Gross and Siegel 1983;Post et al. 2003;Wojczulanis-Jakubas et al. 2015;Ribeiro et al. 2020Ribeiro et al. , 2022. In addition, the method stands out for being less invasive, generating more reliable data for health assessment (Clark et al. 2009). ...
Understanding how the urbanization process affects the lives of animals that live in these environments is relevant to conservation and management. In fact, the urbanization process has a direct impact on animals and can influence their health state. Thus, our objective was to investigate the immunological response of birds to the urbanization process. We recorded the H/L ratio of 723 birds of 10 species captured in Brasília (a large city in central Brazil), as a measure of chronic stress in birds. The H/L ratio was positively associated with the intensity of urbanization and negatively associated with body condition. However, body condition was not associated with intensity of urbanization. We confirmed our hypothesis that birds living in areas with greater urban intensity are more stressed. In addition, we demonstrated that the H/L ratio is negatively associated with body condition, and that this variable should be considered in studies that aim to assess the health of animals. These findings are relevant because they confirm that the urbanization process, along with all its environmental changes (increased artificial light, increased noise, suppression of vegetation, increased built-up areas, etc.), has a negative direct impact on wild populations, which have to deal with major urban changes.
... O cálculo da razão Heterofilo/Linfócito (H/L) é um método proposto para avaliar a saúde das aves. O método baseia-se na contagem diferencial microscópica de leucócitos (perfil leucocitário), e destaca-se como um bom indicador de estresse em aves, sendo assim um proxy para sua saúde (Gross & Siegel 1983;Post et al. 2003;Ribeiro et al. 2020Ribeiro et al. , 2022Wojczulanis-Jakubas et al. 2015). Além disso, o método se destaca por ser menos invasivo quando comparado a outros métodos (Clark et al. 2009). ...
Paisagens urbanas são cada vez mais dominantes ao redor do mundo criando uma nova interface para a fauna silvestre. Apesar de ter sido ignorado por muito tempo pelos ecólogos, o entendimento dos processos em áreas urbanas recebe crescente atenção para a construção de um arcabouço atual de desenvolvimento sustentável e conservação da biodiversidade. Assim, é preciso explorar de forma detalhada como as diferentes características de áreas urbanas filtram espécies e selecionam
características da fauna silvestre. Neste sentido, esta tese se propôs, utilizando espécies de aves silvestres no Distrito Federal (DF) como um modelo, a estudar a relação da expansão e intensificação urbana. O objetivo geral foi investigar as assembleias de aves urbanas e sua relação com o processo de urbanização. Pretendo entender como a urbanização afeta os indivíduos que nela persistem, avaliando sua morfologia, saúde e o uso dos recursos alimentares. Também discorro sobre adaptações metodológicas realizadas em decorrência das dificuldades da amostragem de aves nos ambientes urbanos. A tese está estruturada em oito capítulos interligados pelo tipo de ambiente explorado durante o estudo: ambientes urbanos. Esses capítulos utilizam diferentes abordagens e tem distintos objetivos. Apesar disso, todo o direcionamento do trabalho está focado nos impactos que a urbanização provoca na fauna em seus diferentes aspectos (em nível de comunidade ou de população) e os determinantes ambientais relevantes para os animais que nela vivem. Além disso, em alguns capítulos abordo questões metodológicas, tendo em vista as dificuldades de amostragem de aves nos ambientes urbanos. Por último, apresento um capítulo compilando o conhecimento atual sobre os ambientes urbanos em forma de um texto de divulgação científica para a população, que incorpora meus achados nos ambientes urbanos de Brasília. Meus resultados mostram que as áreas urbanas impactam de forma direta as aves, tanto em nível de comunidade como em nível das populações. Em nível de comunidades, observei clara redução da diversidade (taxonômica, filogenética e funcional) e mudança da estrutura da comunidade em área com maior intensidade urbana. Em nível d populações, observei um aumento da proliferação de doenças (lesões nas patas), aumento do estresse crônico (razão H/L), e mudanças morfológicas e alimentares. Esses achados confirmam minha hipótese inicial de que as áreas urbanas promovem pressões significativas sobre as espécies, afetando
os animais que nela persistem. Meus achados são relevantes pois o entendimento de como as espécies lidam com as pressões ambientais causadas pelas modificações urbanas podem ajudar gestores a tornar as cidades mais amigáveis à fauna, principalmente quando pensamos nos desafios globais de manutenção das populações nativas que estão em declínio.
... If that is the case, we expected that when one parent was incubating the egg (offspring maintenance), the other was foraging (self-maintenance) and they would exchange; the egg would then be continuously incubated and both partners could replenish their body reserves after a long incubation bout. We further expected a positive progression of this coordination over the course of the incubation period due to, for instance, hormonal changes [56]. Since the pelagic life-style of the Dovekie imposes long lasting foraging trips, we also hypothesized that parents would coordinate these trips during the chick rearing period in a way that optimized the food delivery rate to the chick. ...
... Hormonal changes in adults are likely to play a role in the regulation of parental behavior, especially during the incubation period. It is, for instance, known that the level of prolactin increases over the course of the incubation period in the Dovekie parents [35,56] but whether this increases their propensity to incubate, and therefore their level of coordination, remains unknown and will require specific studies. ...
Currently, parental care is becoming increasingly perceived as male and female cooperation, instead of being primarily shaped by sexual conflict. Most studies examining cooperating performance consider coordination of parental activities, and doing so focuses on a short time-window including only one stage of breeding (i.e., incubation or chick rearing period). Here, we considered the cooperation of breeding partners, investigating the coordination of parental care in a long-lived seabird species with long and extensive biparental care, the Dovekie (or Little Auk), Alle alle, and looked at the issue throughout the breeding season. Previous studies on this species revealed coordinated chick provisioning, but parental coordination during incubation remains unstudied. Using video recordings collected over the course of two breeding seasons, we tested whether coordination was subject to small-scale changes within each stage and whether there was a relationship between coordination levels across the two stages. We found that the level of parental coordination is overall high and increases during the incubation period but decreases through the chick rearing phases. There were some inter-annual differences in the coordination level both at the incubation and chick rearing stages. We also found some dependency between the coordination during the incubation and chick rearing periods. All these results suggest that coordination is not a fixed behavior but breeding-phase dependent. The present study thus provides insights into how parental care and parents’ cooperation is shaped by brood needs and conditions. It also highlights a relationship between coordination levels during chick rearing and incubation periods, suggesting some extent of temporal dependence in coordination of parental performance within the breeding season.
... Furthermore, either males or females or neither sex can show higher body condition: (a) males exhibit superior body condition relative to females in Red-Legged Partridges (Alectoris rufa) (Nadal et al. 2018), whereas (b) females display elevated body condition in comparison to males in Willow Flycatchers (Empidonax traillii) (Owen et al. 2005). In contrast, there can also be a lack of conspicuous differences between sexes (Scherer et al. 2014;Angel et al. 2015;Wojczulanis-Jakubas et al. 2015), or a complicated interaction between sex and age, exemplified in Swallow-Tailed Manakins (Chiroxiphia caudata), in which juvenile males surpass females in body condition, while adult females outperform adult males (Souza Penha and da Silva Rodrigues 2022). ...
Body condition in individuals is intricately linked to behaviour, physiology, and immunity. This study investigated how seasonal factors, such as reproduction and moulting, influence the body condition of 21 tanager species in the Atlantic Forest. Utilising publicly available data, I employed phylogenetic generalised linear mixed models to dissect these influences. Notably, females with brood patches exhibited concurrent body and feather moult, suggesting simultaneous energy-costly constraints. Furthermore, females with brood patches displayed higher body condition, indicating proactive preparation or increased resource availability during breeding. Lastly, individuals moulting body feathers exhibited enhanced body condition, suggesting heightened foraging activity. These data suggest complex connections between sex, moulting, and reproductive status in tanagers in the Atlantic Forest.
... Body size is usually measured based on the individual weight, selected skeletal proxy, or a set of measures [5,7,8,33,34]. Since the little auk's weight fluctuates heavily throughout the breeding season [35], it is not a good indicator of the overall size. Instead, we decided to use a single stable measurethe total head and beak length (THL). ...
Source–filter theory posits that an individual's size and vocal tract length are reflected in the parameters of their calls. In species that mate assortatively, this could result in vocal similarity. In the context of mate selection, this would mean that animals could listen in to find a partner that sounds—and therefore is—similar to them. We investigated the social calls of the little auk (Alle alle), a highly vocal seabird mating assortatively, using vocalizations produced inside 15 nests by known individuals. Source- and filter-related acoustic parameters were used in linear mixed models testing the possible impact of body size. A principal component analysis followed by a permuted discriminant function analysis tested the effect of sex. Additionally, randomization procedures tested whether partners are more vocally similar than random birds. There was a significant effect of size on the mean fundamental frequency of a simple call, but not on parameters of a multisyllable call with apparent formants. Neither sex nor partnership influenced the calls—there was, however, a tendency to match certain parameters between partners. This indicates that vocal cues are at best weak indicators of size, and other factors likely play a role in mate selection.
... :L ratios can change across the breeding season, decreasing in some species(Wojczulanis-Jakubas et al., 2015;Kulaszewicz, Wojczulanis-Jakubas & Jakubas, 2017) and increasing in others. The timing of sampling should thus be standardized if H:L ratios are to be used as a monitoring tool across years. ...
Seabirds are the most endangered avian taxa on Earth, with over a third of species globally threatened. To help slow their decline, conservation physiology seeks to determine how seabird responses to climatic and anthropogenic threats influence demographic processes, but it is not widely utilized in monitoring.
A wide variety of metrics and methods are available to the conservation practitioner; thus, the correct method selection is paramount. This is a review of physiological tools to assess both individual and population health in seabirds, outlining which tools could be accessible enough to incorporate into conservation management strategies to increase the efficacy and range of population monitoring.
Ultimately, the cost and expertise required limits the use of some tools in a community‐based management context, but they are useful in academic research in collaboration with conservation projects to generate data to inform management strategies for threatened species.
The value of the data available from particular tools is weighed against the invasiveness of the methodology to assess the practicality of incorporating physiological tools into routine seabird monitoring programmes.
A broader application of conservation physiology tools in a monitoring context could help manage threatened species; this paper summarizes a set of physiological variables from minimally invasive samples that have potential to assist in monitoring population health for seabird conservation. The full potential of these physiological tools is yet to be realized in seabirds.
... In turn, corticosterone induces the release of heterophils into the blood stream from the bone marrow, and transmigration of lymphocytes from circulation into other tissues; this may happen in situations of predator sighting, competition, heat stress and food shortage, among others (Davis et al. 2008). In seabirds, H:L has been mainly used to assess energetic trade-offs during breeding (Vleck et al. 2000, Wojczulanis-Jakubas et al. 2015, Kulaszewicz et al. 2017) and exposure to contaminants. However, because the immune status may greatly affect the circulating white blood cells' profile, changes in H:L ratios may be influenced by infection and inflammation processes, which are intrinsically linked to immunity. ...
... Both sexes are monomorphic in plumage, but males are often bigger than females (though there is a great overlap in measurements between the sexes) [31]. During incubation, the stress level expressed in the CORT level is similar in both sexes [32,33], but males have a tendency to exhibit a stronger CORT stress response than females [33]. ...
Measuring changes in surface body temperature (specifically in eye-region) in vertebrates using infrared thermography is increasingly applied for detection of the stress reaction. Here we investigated the relationship between the eye-region temperature (TEYE; measured with infrared thermography), the corticosterone level in blood (CORT; stress indicator in birds), and some covariates (ambient temperature, humidity, and sex/body size) in a High-Arctic seabird, the Little Auk Alle alle. The birds responded to the capture-restrain protocol (blood sampling at the moment of capturing, and after 30 min of restrain) by a significant TEYE and CORT increase. However, the strength of the TEYE and CORT response to acute stress were not correlated. It confirms the results of a recent study on other species and all together indicates that infrared thermography is a useful, non-invasive measure of hypothalamic-pituitary-adrenal (HPA) axis reactivity under acute activation, but it might not be a suitable proxy for natural variation of circulating glucocorticoid levels.
... The long and extensive bi-parental care (1 month of incubation + 1 month of chick rearing, possibly post-fledging care), required to raise the single chick successfully (Stempniewicz 2001), creates an excellent reproductive system in which to examine the cause and effect of sexual differences in parental efforts (Wojczulanis et al. 2006;, 2015a. This topic has long been explored with regard to sexual conflict, including some Little Auk studies, e.g. . ...
... Rights reserved. Preference and specialization on a superior prey type that guarantees the best net energy gain (Weslawski et al. 1999;Karnovsky et al. 2003;Vogedes et al. 2014;Møller et al. 2018) Flexibility of foraging behaviour Spatio-temporal variation in environmental conditions in foraging areas (Jakubas et al. , 2016Welcker et al. 2009a, b;Harding et al. 2009a;Kwasniewski et al. 2010Kwasniewski et al. , 2012Karnovsky et al. 2011;Brown et al. 2012;Grémillet et al. 2012;Amélineau et al. 2019) Predator-prey interaction Highly synchronized breeding, strong interrelationships with a limited number of predators (Stempniewicz 1995;Burnham 2005;Wojczulanis et al. 2005;Jakubas and Wojczulanis-Jakubas 2010) Trade-off between the benefits of investment in current offspring and costs to future reproduction Long-lived, iteroparous species with low annual fecundity are less exposed to the risk of mortality during a given breeding attempt (Gębczyński et al. 1996;Harding et al. 2009a, b;Welcker et al. 2009b;Hovinen et al. 2014b;Kidawa et al. 2015Kidawa et al. , 2017 Ecosystem services Importance as a habitat role of an ecosystem engineer-transport of marine-derived nutrients to land Large colonies provide huge amounts of organic matter to nutrient-deprived tundra forming green oases (Stempniewicz 1990;Skrzypek et al. 2015;Zwolicki et al. 2016b;González-Bergonzoni et al. 2017;Mosbech et al. 2018) Role of a social engineer-hunter gathering societies regardless of sex or age Important, easily obtainable game species for the Innuit in Greenland Energetics Carry-over effects from non-breeding to breeding areas (influence of non-breeding location on survival and reproductive performance) Breeding in the High Arctic and wintering in the sub-Arctic and temperate zones (Dufour et al. 2021; Energy allocation between costly functions, i.e. immune function-reproduction, oxidative stressreproduction Long and extensive bi-parental care, costly foraging, high daily energy requirements (Kulaszewicz et al. 2017(Kulaszewicz et al. , 2018 Behavioural ecology & eco-physiology Stress response during the breeding season Long-lived, iteroparous species-expected to prevent their own survival from being jeopardized (Wojczulanis-Jakubas et al. 2015a, 2018c Coordination of parental care Presence of dual foraging strategy during the chickrearing period (alternation of long and short foraging trips) (Wojczulanis-Jakubas et al. 2018a;Grissot et al. 2019) Sexually transmitted disease Low frequency of extra-pair paternity (2%) (Wojczulanis-Jakubas et al. 2011a) Role and function of bi-modal foraging strategy Dual foraging strategy during the chick-rearing period (alternation of long and short forging trips) (Welcker et al. 2009aWojczulanis-Jakubas et al. 2010a;Jakubas et al. 2012Jakubas et al. , 2014) Role of body reserves in incubating adults and chicks ...
... Reduction in mass at the end of chick growth, increase in adult body mass during incubation (Taylor and Konarzewski 1989;Taylor 1994;Jakubas et al. 2008a) Eco-immunology Factors affecting haematological stress Expected trade-offs between immune function and reproduction (Jakubas et al. 2008a, 2015a Lack of blood parasites often affects immune function (Wojczulanis-Jakubas et al. 2010b) Evolution Transition from biparental to uniparental chick care ...
The Little Auk Alle alle is a small planktivorous auk breeding colonially in the High Arctic. Owing to its large population size and bi-environmental lifestyle, resulting in the large-scale transport of matter from sea to land, the Little Auk is one of the most important components of the marine and terrestrial ecosystems in the Arctic. As a result of globalization, which facilitates access to remote areas of the Earth, a growing number of studies is being dedicated to this endemic Arctic seabird. Research has focussed primarily on the importance of the Little Auk as an ecological indicator reacting to the climatic and oceanological changes that are particularly evident in the Arctic as a result of Arctic amplification (warming is more rapid in the Arctic than in any other region on Earth). Importantly, the species is also used as a model to investigate matter and energy flow through the ecosystem, mate choice, parental care and biological rhythms. Here, we review the natural history of the Little Auk, highlighting studies with the potential to provide answers to universal questions regarding the response of seabirds to climate variability and avian reproductive behaviour, e.g. threshold of foraging flexibility in response to environmental variability, carry-over effects between the breeding and non-breeding periods, the reasons for the transition from bi- to uni-parental care, parental coordination mechanisms.
