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![Average changes in body mass, food intake, and nitrogen (N) balance in Hermit Thrushes and White-throated Sparrows in the nonmigratory state (n = 20 and n = 22, respectively) that ingested different amounts of protein. Brackets along the x-axis show the four dietary protein groups (3.6%, 6.7%, 9.7%, and 12.8%) that were used to produce this range in dietary N intake. Changes in N balance as a function of N intake by Hermit Thrushes and White-throated Sparrows are described by the equations y = 0.430x − 22.82 (R 2 = 0.75, n = 20) and y = 0.358x − 16.44 (R 2 = 0.63, n = 22), respectively. (A) Horizontal shaded area depicts the average (± 90% confidence interval [CI]) change in body mass of birds in steady state (Hermit Thrush, n = 20; White-throated Sparrow, n = 22) during the 14 days prior to the start of total-collection trials. Horizontal dashed lines and surrounding shaded area depict (B and E) food intake and (C and F) N balance (± 90% CI) of birds in the nonmigratory state that consumed adequate dietary protein (≥9.7% protein) during the total-collection trials.](profile/Scott-Mcwilliams-2/publication/239732176/figure/fig2/AS:667857302061063@1536240997561/Average-changes-in-body-mass-food-intake-and-nitrogen-N-balance-in-Hermit-Thrushes.png)
Average changes in body mass, food intake, and nitrogen (N) balance in Hermit Thrushes and White-throated Sparrows in the nonmigratory state (n = 20 and n = 22, respectively) that ingested different amounts of protein. Brackets along the x-axis show the four dietary protein groups (3.6%, 6.7%, 9.7%, and 12.8%) that were used to produce this range in dietary N intake. Changes in N balance as a function of N intake by Hermit Thrushes and White-throated Sparrows are described by the equations y = 0.430x − 22.82 (R 2 = 0.75, n = 20) and y = 0.358x − 16.44 (R 2 = 0.63, n = 22), respectively. (A) Horizontal shaded area depicts the average (± 90% confidence interval [CI]) change in body mass of birds in steady state (Hermit Thrush, n = 20; White-throated Sparrow, n = 22) during the 14 days prior to the start of total-collection trials. Horizontal dashed lines and surrounding shaded area depict (B and E) food intake and (C and F) N balance (± 90% CI) of birds in the nonmigratory state that consumed adequate dietary protein (≥9.7% protein) during the total-collection trials.
Source publication
Many songbirds are seasonally frugivorous and eat primarily fruit during migration and insects or seeds during nonmigratory periods. Previous work has suggested that most wild fruits may have inadequate protein for birds. Assessing the nutritional adequacy of fruit requires knowing the protein requirements of birds in relation to the composition of...
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Citations
... Alternately, life history stages may be associated with different nutritional requirements and diets high in fruit may contain a macronutrient (i.e. carbohydrate, fat, protein) profile better suited for migratory fattening (e.g., high carbohydrate and fat; Langlois and McWilliams 2010). A recent study by Blendinger et al. (2022) demonstrated dietary matching of macronutrient targets in a community of overwintering Swainson's thrushes and other songbirds, which highlights the plausibility of this mechanism for migratory thrushes. ...
Migration is an energetically challenging and risky life history stage for many animals, but could be supported by dietary choices en route, which may create opportunities to improve body and physiological condition. However, proposed benefits of diet shifts, such as between seasonally available invertebrates and fruits, have received limited investigation in free-living animals. We quantified diet composition and magnitude of autumn diet shifts over two time periods in two closely-related species of migratory songbirds on stopover in the northeastern U.S. (Swainson’s thrush [Catharus ustulatus], long-distance migrant, N = 83; hermit thrush [C. guttatus], short-distance migrant, N = 79) and used piecewise structural equation models to evaluate the relationships among (1) migration timing, (2) dietary behavior, and (3) morphometric and physiological condition indices. Tissue isotope composition indicated that both species shifted towards greater fruit consumption. Larger shifts in recent weeks corresponded to higher body condition in Swainson’s, but not hermit thrushes, and condition was more heavily influenced by capture date in Swainson’s thrushes. Presence of “high-antioxidant” fruits in fecal samples was unrelated to condition in Swainson’s thrushes and negatively related to multiple condition indices in hermit thrushes, possibly indicating the value of fruits during migration is related more to their energy and/or macronutrient content than antioxidant content. Our results suggest that increased frugivory during autumn migration can support condition, but those benefits might depend on migration strategy: a longer-distance, more capital-dependent migration strategy could require stricter regulation of body condition aided by increased fruit consumption.
... Many mi- gratory birds must eat both fruits and insects to meet their energy requirements (Suthers et al., 2000;Smith et al., 2007). Langlois and McWilliams (2010) found a decrease in protein requirements in birds during migration, and Orlowski et al. (2011) described a trend toward a significant increase in the proportion of berries in the diet of black redstart from July to October. This can be seen as an adaptation of birds to survive in invertebrate scarcity by increasing the consumption of plant berries and fruits. ...
Parthenocissus inserta (A. Kern.) Fritsch. adapts to living in the forests of Ukraine. The influence of P. inserta on native species and its consortial ties with representatives of the secondary ranges biota, in particular birds, has not been studied. The purpose of this study is to make an inventory of the consorts’ ornithocomplexes of P. inserta , to give a comparative analysis of topic and trophic consorts as a result of an introduced species’ participation in the transformation of habitat’s conditions. The material was collected from 2019 to 2022 in forest parks and urban green spaces of the Kyiv city. The bird distribution was determined by the standard method of counting birds at points. Exactly 12.2 ha of P. inserta plantations were surveyed. Trophic consortium relationships of P. inserta with 32 bird species and topic ones with six bird species were revealed. The species composition of consorts was higher in forest fragments than in urban plantations (26 and 21 species, respectively). In the ornithocomplexes of P. inserta consorts in forest biotopes, there was a smaller pressure of dominant species and a more evenly ranked distribution of species by abundance than in urbanized ones. The similarity of the consort’s species composition in urbanized and natural biotopes according to the Sorensen index was 0.64, in consorts 1 and 2 of the consortium concentres was 0.32, and in topic and trophic consorts was 0.27. According to the status of stay in the region, trophic consorts of P. inserta were mainly resident birds – 20 species (62.50%), wintering birds – six species (18.75%), and birds migrating through the region – six species of birds (18.75%). Among the topic consorts, there were four species of sedentary species and two species arriving for nesting. Principal component analysis revealed the largest positive relationship between P. inserta planting area and the number of consort bird species nesting (0.999) and feeding (0.889) on girlish vine plants. We predict that in the future, P. inserta will be more strongly woven into the matter cycle of the secondary range ecosystems. The study of consortial relationships between invasive plants and birds, taking into account the knowledge of the ecological characteristics of consort birds, will make it possible to more effectively prevent the spread of plants into natural biotopes.
... where for a gulper bird the energy acquired in 1 min by a species for acclimatisation and maintenance of fruit-eating birds (Denslow et al., 1987;Langlois & McWilliams, 2010). While we are aware that physiology varies within and between species, in the absence of empirical data on the optimal macronutrient mixture for wild birds, we assumed the estimated nutritional target as representative of the average optimal mixture of macronutrients for all birds. ...
According to diet‐regulation hypotheses, animals select food to regulate the intake of macronutrients or maximise energy feeding efficiency. Specifically, the nutrient balance model proposes that foraging is primarily a process of balancing multiple nutrients to achieve a nutritional intake target, while the energy maximisation model proposes that foraging aims to maximise energy.
Here, we evaluate the adjustment of fruit diets (the fruit‐derived component of the diets) to nutritional and energy intake targets, characterising the nutrient balance and energy maximisation strategies across fruit‐eating bird species with different fruit‐handling behaviours (‘gulpers’, which swallow whole fruits, and ‘mashers’, which process the fruit in the beak) in subtropical Andean forests. Food‐handling behaviour determines the food intake rate and, consequently, influences animal efficiency to obtain nutrients and energy.
We used extensive field data from the diet of fruit‐eating birds to test how species adjust their food intake. We used nutritional geometry to explore macronutrient balance and the effectiveness framework to explore energy‐acquisition effectiveness.
Observed diets showed a good fit with predictions of a diet balanced in macronutrient proportions. With few exceptions, diets clustered near an optimal macronutrient mixture and did not differ from each other in terms of maximising energy intake. Moreover, when comparing our results with a random diet based on local fruit availability, birds tended to fit better to the nutritional target, and less to the energy target, than expected from a random diet. Fruit‐handling behaviour did not affect the ability of bird species to reach a nutritional target but it affected species energy acquisition, which was lower in mashers than in gulpers.
This study explores for the first time different diet‐regulation strategies in wild fruit‐eating birds, and supports the argument that the diet reflects a specific regulation of macronutrients. Understanding why birds select fruits is a complex question requiring multiple considerations. The nutrient balance model explains the relevance of nutrient composition in the fruit selection by fruit‐eating birds, although it is still necessary to determine its relative importance with respect to other dietary drivers.
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... If juvenile songbirds have more lean mass that turns over more rapidly, then they may require greater protein intake during refueling than adults. More studies are needed on songbird protein requirements (Langlois and McWilliams, 2010), protein turnover, lean mass flexibility, and its energetic costs in juvenile songbirds. ...
Fat contributes most of the energy for migratory flight of birds, whereas lean body tissues (muscles and organs) contribute amino acids and water to maintain metabolic and osmotic homeostasis. During refueling at stopover sites, both fat and lean mass are recovered, but the dynamics of this recovery are poorly understood. We used non-invasive quantitative magnetic resonance (QMR) analysis to measure fat and lean mass of > 3,500 individuals of 25 songbird species during six spring and three autumn migration seasons between 2009 and 2019 at Long Point, ON, Canada. We used allometric scaling analysis and linear mixed-effects modeling of body composition data at both the population level (single capture) and the individual level (recapture). In the population-level analysis, lean mass scaled hypoallometrically with body mass, such that for every 20% increase in body mass, lean mass was predicted to increase by 12.1% in spring and 12.8% in autumn. Fat scaled hyperallometrically with body mass, such that for every 20% increase in body mass, fat mass was predicted to increase by 144% in spring and 136% in autumn. At the individual level, these allometric relationships were more extreme. As a result of this differential allometry, at low body masses, lean and fat mass contributes nearly equally to changes in mass, but at high body mass fat deposition becomes progressively more dominant. Spring migrants deposited relatively more fat than autumn migrants, and in autumn juvenile birds tended to have greater lean mass than adults. Our findings show that lean mass deposition during refueling by songbirds is substantial, and in line with the losses of protein expected in flight. The process of fat and lean mass deposition is characterized by non-linear dynamics which are influenced by the current body composition, season, and, to a lesser extent, age. The patterns suggest that the need for dietary protein to rebuild lean mass will be greater when body mass is low, during autumn migration, and in juvenile birds.
... Further, birds get their required amount of protein due to higher food intake rates while preparing for migration and refueling at the stopover sites, even if the protein content in their food is low (Langlois and McWilliams, 2010;Marshall et al., 2015). Foods containing high-carbohydrates over high-protein is preferred by the yellow-rumped warblers (Setophaga coronate), adjusting their food intake seasonally to match changing energy targets for energy sources (Marshall et al., 2015). ...
Migratory birds undergo physiological and behavioral changes to fuel their high energy demanding migratory flights. They increase their food intake as a part of the preparation for migration which results in increase in their body mass. Fat, carbohydrate and protein acquired from food are stored mainly in the adipose tissue (triglycerides), muscle and liver (glycogen) and body organs (protein) in migratory birds. These stored foods act as fuels to support birds’ migratory flights. Dietary carbohydrates and lipids not only provide energy for migration but also help in fattening as carbohydrates can be converted into fat and lipids which can be stored. Lipolysis of adipose-stored fats leads to the production of triglycerides, fatty acids and glycerol, which provide energy for migration. Fats are depleted after long migratory flights and replenished during refueling at the stopover sites. Being chemically reduced and hydrophobic in nature, fat releases more energy on oxidation as compared to carbohydrate and protein. Due to its high energy-yielding nature, the fat is the preferred fuel to support migration in birds. Migratory birds deposit fat and deplete it during the course of migration. Though, the stored fat acts as the primary source of energy, metabolism of body protein also provides energy for migratory flights. Uric acid in plasma is elevated when protein is catabolized. The metabolism of carbohydrate, stored as glycogen in liver and muscle in migratory birds, produces glucose which also fuels migration. Glucose in migratory birds is maintained at stable levels in plasma and it provides energy only for a flight of short period. Further, catabolism of carbohydrate and protein results in release of metabolic water which helps the migratory birds to maintain their water balance during long dehydrating flight conditions. Different levels of plasma metabolites in migratory birds act as significant indicators of their physiological and metabolic state. Plasma metabolites also give an idea of feeding, fasting and refueling during migration in birds. The available information is scanty and fragmented about how birds meet their migratory requirements and overcome the physiological challenges encountered during migration. The present review article, therefore, focuses on the biomolecules and their plasma biochemistry during migration in birds.
... After the 10-week acclimation period, we offered birds only the casein-based acclimation diet (no mealworms) for the next 6 weeks. Birds were then used in a protein requirement experiment (Langlois and McWilliams 2010) for 9 days. Thereafter, birds were switched to a crystalline amino acid-based diet (diet A for all EAA experiments; Online Resources Table 1). ...
... Dried samples were homogenized using mortar and pestle. Methods for measuring nitrogen concentration of food and excreta are described in Langlois and McWilliams (2010). ...
Wild birds must consume certain amounts of protein and an appropriate balance of amino acids while inhabiting environments where foods often differ in the quantity and quality of available protein. The requirements for amino acids are well documented for domestic bird species but are largely unknown for wild birds, which makes it impossible to reliably assess the nutritional adequacy of foods eaten by wild birds. We measured the maintenance requirements for three essential amino acids (lysine, methionine, and arginine) in two species of songbird, the omnivorous Hermit Thrush (Catharus guttatus) and granivorous White-throated Sparrow (Zonotrichia albicollis). Hermit Thrushes and White-throated Sparrows had similar requirements for lysine (20.02 and 19.95 mg/day, respectively) and methionine (12.3 and 10.85 mg/day, respectively), whereas thrushes had lower requirements for arginine (18.07 mg/day) compared to sparrows (34.5 mg/day). Consistent with previous studies, most birds fed diets with inadequate essential amino acid concentrations reduced food intake and fecal output, lost body mass, and had lower, but not negative nitrogen balance. However, we provide the first evidence that songbirds overcompensate when they consume diets very deficient in lysine. Available data on amino acid concentrations in natural foods suggests that most insects contain relatively high concentrations of all essential amino acids, seeds likely satisfy requirements of lysine and arginine but not methionine for Hermit Thrushes and White-throated Sparrows, whereas fruits generally contain inadequate amounts of all essential amino acids. Therefore, birds that eat mostly fruit may consume enough protein but likely must eat other types of foods to satisfy their essential amino acid requirements.
... Birds may also alter their food preferences during migration, for example, by including more fruit in the diet when it is available in the autumn (Bairlein, 2002;Berthold, 1993;Parrish, 1997). High dietary energy (carbohydrates and lipids) to protein ratios, such as those found in fruit or seeds, promote fattening (Bairlein, 2002) because carbohydrates can be readily converted to fat, lipids can be directly absorbed and stored, and high food intake rates allow migrating birds to meet protein requirements, even if the protein content of their diet is low (Langlois and McWilliams, 2010;Marshall et al., 2015). Yellow-rumped warblers (Setophaga coronata) prefer high-carbohydrate to high-protein diets, adjusting intake seasonally to match changing energy targets (Marshall et al., 2015). ...
Migratory birds are physiologically specialized to accumulate massive fat stores (up to 50-60% of body mass), and to transport and oxidize fatty acids at very high rates to sustain flight for many hours or days. Target gene, protein and enzyme analyses and recent -omic studies of bird flight muscles confirm that high capacities for fatty acid uptake, cytosolic transport, and oxidation are consistent features that make fat-fueled migration possible. Augmented circulatory transport by lipoproteins is suggested by field data but has not been experimentally verified. Migratory bats have high aerobic capacity and fatty acid oxidation potential; however, endurance flight fueled by adipose-stored fat has not been demonstrated. Patterns of fattening and expression of muscle fatty acid transporters are inconsistent, and bats may partially fuel migratory flight with ingested nutrients. Changes in energy intake, digestive capacity, liver lipid metabolism and body temperature regulation may contribute to migratory fattening. Although control of appetite is similar in birds and mammals, neuroendocrine mechanisms regulating seasonal changes in fuel store set-points in migrants remain poorly understood. Triacylglycerol of birds and bats contains mostly 16 and 18 carbon fatty acids with variable amounts of 18:2n-6 and 18:3n-3 depending on diet. Unsaturation of fat converges near 70% during migration, and unsaturated fatty acids are preferentially mobilized and oxidized, making them good fuel. Twenty and 22 carbon n-3 and n-6 polyunsaturated fatty acids (PUFA) may affect membrane function and peroxisome proliferator-activated receptor signaling. However, evidence for dietary PUFA as doping agents in migratory birds is equivocal and requires further study.
... Arguably the most important constraint during migration is finding sufficient resources to meet energetic demands (McWilliams et al. 2004, McGrath et al. 2009. Many landbirds are known to change their diets to high-energy foods during migration, including fruits and nectar, which may also satisfy their protein requirements during migration even though the protein content of these foods is relatively low (Langlois and McWilliams 2010). In northern latitudes, birds that are predominantly insectivorous during the breeding season change their diets to eat more fruit during fall migration (Parrish 1997). ...
Habitats around the Gulf of Mexico (GOM) provide critical resources for Nearctic-Neotropical migratory landbirds, the majority of which travel across or around the GOM every spring and fall as they migrate between temperate breeding grounds in North America and tropical wintering grounds in the Caribbean and Central and South America. At the same time, ecosystems in the GOM are changing rapidly, with unknown consequences for migratory landbird populations, many of which are experiencing population declines. In general, the extent to which events encountered en route limit migratory bird populations is not well understood. At the same time, information from weather surveillance radar, stable isotopes, tracking, eBird, and genetic datasets is increasingly available to address many of the unanswered questions about bird populations that migrate through stopover and airspace habitats in the GOM. We review the state of the science and identify key research needs to understand the impacts of en route events around the GOM region on populations of intercontinental landbird migrants that breed in North America, including: (1) distribution, timing, and habitat associations; (2) habitat characteristics and quality; (3) migratory connectivity; and (4) threats to and current conservation status of airspace and stopover habitats. Finally, we also call for the development of unified and comprehensive long-term monitoring guidelines and international partnerships to advance our understanding of the role of habitats around the GOM in supporting migratory landbird populations moving between temperate breeding grounds and wintering grounds in Mexico, Central and South America, and the Caribbean.
... Dietary protein is required to replace daily endogenous losses and for new tissue growth, but high protein diets promote satiety and reduce weight gain (Davidenko et al. 2013). High total energy intake and little change in protein requirement allows migrants to refuel eating fruits with very low protein content (Langlois and McWilliams 2010). So, beyond the ecological benefits of abundance and ease of capture, fruit consumption can promote fat deposition and some secondary metabolites in fruit may also provide antioxidants to reduce oxidative damage during flight (Skrip et al. 2015). ...
The catabolism of protein from organs and muscles during migratory flight is necessary to produce glucose, key metabolic intermediates, and water, but may have negative effects on flight range and refueling at stopovers. We tested the hypothesis, suggested by previous studies, that birds that eat high-protein insect diets use more protein for fuel in flight than those that eat high-carbohydrate fruits. First, we fed migratory yellow-rumped warblers synthetic fruit or mixed insect/fruit diets, and measured metabolic rates and fuel mixture under basal conditions and during exercise in a hop/hover wheel respirometer. Birds eating the fruit diet had greater plasma triglyceride and non-esterified fatty acid concentrations, and the higher protein mixed diet increased plasma uric acid only during feeding. Diet did not affect metabolic rates or the fuel mixture under resting or exercise conditions. We then fed yellow-rumped warblers synthetic diets that differed only in the relative proportion of carbohydrate and protein (60:15 versus 15:60 as % dry mass) and tested them in wind tunnel flights lasting up to six hours. Birds fed the high carbohydrate diet became heavier and fatter than when fed the high protein diet. Plasma uric acid concentration was increased and plasma phospholipid concentration was decreased by the high protein diet in the pre-flight state (after a 3 h fast), but diet only affected plasma phospholipids during flight (lower in high protein birds). Neither diet nor amount of body fat affected the rate of loss of lean mass or fat during flight. Inter-individual or seasonal differences in diet do not appear to influence the amount of protein catabolized during endurance flight. However, birds fed the high carbohydrate diet had greater voluntary flight duration, independent of body fatness, suggesting that there may be other performance benefits of high carbohydrate diets for migratory birds.
... It is thought that this ability to migrate, and survive across a diversity of environments, is an adaptation to seasonality in resources (Newton, 2008;Somveille et al., 2015) and a benefit of physiological flexibility (i.e., ecophysiology) (McWilliams & Karasov, 2005). For example, plasticity in foraging behaviour and digestive physiology allows birds that are typically granivores or frugivores during the winter to shift to a protein-rich diet based on insects during the breeding season (Levey & Karasov, 1989;Langlois & McWilliams, 2010;Diggs et al., 2011). This behavioural and physiological flexibility is essential for birds to take advantage of novel environments and respond to environmental change (Griffis-Kyle & Beier, 2005;Sol & Lefebvre, 2006;Wright et al., 2010). ...
Aim
Plasticity in migratory and foraging behaviour allows species to exploit dynamic and novel habitats. This is especially important during seasonal transitions as species track shifting environmental resources and potentially associate with a diversity of habitats. Although land cover associations are thought to vary across seasons for many species, the prevalence of these dynamic relationships across species’ distributions are unknown. Our goal was to quantify the extent to which flexibility in seasonal land cover associations exists among forest breeding birds with differing migratory and foraging strategies.
Location
Eastern United States.
Methods
We used data on bird occurrence from eB ird in conjunction with dynamic species distribution modelling to quantify seasonal plasticity in species land cover associations for 43 forest breeding bird species. We employed a multi‐scaled approach relying on adaptive regression models to quantify spatiotemporally varying associations between species’ occurrences and land cover diversity and composition. We estimated how these associations varied from spring to autumn and across multiple regions.
Results
Species demonstrated seasonal shifts in land cover associations and, despite being forest dependent species, were more likely to occur in human‐modified landscapes during seasonal transitions. From spring to autumn, Neotropical migrants were more likely to occur in landscapes of lower land cover diversity, but showed the highest seasonal plasticity in land cover associations. Residents and temperate migrants occurred in landscapes with a higher diversity of land cover, but were less variable in their seasonal land cover associations. Following summer, migratory and insectivorous birds took advantage of a wider array of land cover ranging from open to developed landscapes.
Main conclusions
Species move across landscapes in a seasonally dynamic fashion, and yet concepts of the ecological niche and species–environmental relationships are often considered static. Dynamic species distribution modelling can uncover seasonally complex species–environment relationships, and identify novel aspects of habitat associations critical for supporting full life cycle research and conservation efforts.
