- Groningen Institute for Evolutionary Life Sciences
Conservation Ecology Group
Nijenborgh 7
9747 AG GRONINGEN
The Netherlands
Postal address:
PO Box 11103
9700 CC GRONINGEN
The Netherlands
------------------------------------------------------- - +31-(0)503632028
Jeroen Reneerkens
Aarhus University, Bioscience, Post-Doc
- Animal Ecology, Chemical Ecology, Avian Ecology, Avian migration, Evolutionary Ecology, Ecophysiology, and 11 moreMigration Studies, Birds (Ecology), Biology, Migration, Population ecology, Population Dynamics, Avian Behavior, Avian Demography, Survival Analysis, Bird Migration, and Ecology of Bird Migrationedit
Kubelka et al. (Report, 9 November 2018, p. 680-683) claim that climate change has disrupted patterns of nest predation in shorebirds. They report that predation rates have increased since the 1950s, especially in the Arctic. We describe... more
Kubelka et al. (Report, 9 November 2018, p. 680-683) claim that climate change has disrupted patterns of nest predation in shorebirds. They report that predation rates have increased since the 1950s, especially in the Arctic. We describe methodological problems with their analyses and argue that there is no solid statistical support for their claims.
Research Interests:
The behavioural rhythms of organisms are thought to be under strong selection, influenced by the rhythmicity of the environment 1–4. Such behavioural rhythms are well studied in isolated individuals under laboratory conditions 1,5 , but... more
The behavioural rhythms of organisms are thought to be under strong selection, influenced by the rhythmicity of the environment 1–4. Such behavioural rhythms are well studied in isolated individuals under laboratory conditions 1,5 , but free-living individuals have to temporally synchronize their activities with those of others, including potential mates, competitors, prey and predators 6–10. Individuals can temporally segregate their daily activities (for example, prey avoiding predators, subordinates avoiding dominants) or synchronize their activities (for example, group foraging, communal defence, pairs reproducing or caring for offspring) 6–9,11. The behavioural rhythms that emerge from such social synchronization and the underlying evolutionary and ecological drivers that shape them remain poorly understood 5–7,9. Here we investigate these rhythms in the context of biparental care, a particularly sensitive phase of social synchronization 12 where pair members potentially compromise their individual rhythms. Using data from 729 nests of 91 populations of 32 biparentally incubating shorebird species, where parents synchronize to achieve continuous coverage of developing eggs, we report remarkable within-and between-species diversity in incubation rhythms. Between species, the median length of one parent's incubation bout varied from 1–19 h, whereas period length—the time in which a parent's probability to incubate cycles once between its highest and lowest value—varied from 6–43 h. The length of incubation bouts was unrelated to variables reflecting energetic demands, but species relying on crypsis (the ability to avoid detection by other animals) had longer incubation bouts than those that are readily visible or who actively protect their nest against predators. Rhythms entrainable to the 24-h light–dark cycle were less prevalent at high latitudes and absent in 18 species. Our results indicate that even under similar environmental conditions and despite 24-h environmental cues, social synchronization can generate far more diverse behavioural rhythms than expected from studies of individuals in captivity 5–7,9. The risk of predation, not the risk of starvation, may be a key factor underlying the diversity in these rhythms.
Research Interests:
How species interact modulate their dynamics, their response to environmental change, and ultimately the functioning and stability of entire communities. Work conducted at Zackenberg, Northeast Greenland, has changed our view on how... more
How species interact modulate their dynamics, their response to environmental change, and ultimately the functioning and stability of entire communities. Work conducted at Zackenberg, Northeast Greenland, has changed our view on how networks of arctic biotic interactions are structured, how they vary in time, and how they are changing with current environmental change: firstly, the high arctic interaction webs are much more complex than previously envisaged, and with a structure mainly dictated by its arthropod component. Secondly, the dynamics of species within these webs reflect changes in environmental conditions. Thirdly, biotic interactions within a trophic level may affect other trophic levels, in some cases ultimately affecting land–atmosphere feedbacks. Finally, differential responses to environmental change may decouple interacting species. These insights form Zackenberg emphasize that the combination of long-term, ecosystem-based monitoring, and targeted research projects offers the most fruitful basis for understanding and predicting the future of arctic ecosystems.
Research Interests:
1. Animals adjust to seasonal challenges in physical, behavioural and spatial ways. Such adjustments are commonly associated with diet changes that often can be characterised isotopically. 2. We introduce the 'double diet switch model',... more
1. Animals adjust to seasonal challenges in physical, behavioural and spatial ways. Such adjustments are commonly associated with diet changes that often can be characterised isotopically. 2. We introduce the 'double diet switch model', with which the occurrence and timing of two subsequent diet switches of an individual animal can be traced with a single sample assayed for stable isotopes. We demonstrate the model for Sanderling, Calidris alba, a small shorebird that migrates from the Nearctic tundra breeding grounds to the intertidal flats of the Wadden Sea; during this migration some birds may stage in the North Atlantic areas. 3. The 'double diet switch model' successfully predicted the occurrence and timing of two diet switches in 59 San-derlings captured in the Wadden Sea in July–September. Excluding birds that likely had over-summered at North Atlantic staging areas, the model predicted that Sanderlings departed from the Arctic on 13 July (range: 9–17 July), had a staging duration of 18Á6 days in the North Atlantic, and arrived in the Wadden Sea on 1 August (31 July–1 August).The estimated mean Arctic departure dates coincided with the mean hatching date, suggesting that many individuals failed to produce young or left the care to a partner. Estimated mean arrival date matched the main arrival period in the Wadden Sea obtained from observation data. In this study we did not use lipid-free tissues, which may bias model predictions. After correcting for lipid components, the estimated departure date was 11 days later and the staging duration 8Á5 days shorter, while arrival date was similar. 4. The 'double diet switch model' successfully identified the occurrence and timing of two subsequent diet switches. The 'double diet switch model' will not only apply to switches between three isotopic levels (as in the case study on Sanderling) but also to scenarios where the second switch reverses to the initial isotopic level. Due to this general applicability, the model can be adapted to a wide range of taxa and situations. Foreseeable applications include changes in habitat and food type, ontogenetic development or drastic phenotypic changes such as the metamorphosis in insects and amphibians.
Research Interests:
Many migratory bird species show high levels of site fidelity to their wintering sites, which confers advantages due to prior knowledge, but may also limit the ability of the individual to move away from degrading sites or to detect... more
Many migratory bird species show high levels of site fidelity to their wintering sites, which confers advantages due to prior knowledge, but may also limit the ability of the individual to move away from degrading sites or to detect alternative foraging opportunities. Winter site fidelity often varies among age groups, but sexual differences have seldom been recorded in birds. We studied a population of individually colour-marked sanderlings wintering in and around the Tejo estuary, a large estuarine wetland on the western coast of Portugal. For 160 individuals, sighted a total of 1,249 times between November 2009 and March 2013, we calculated the probability that they moved among five distinct wintering sites and how this probability is affected by distance between them. To compare site fidelity among age classes and sexes, as well as within the same winter and over multiple winters, we used a Site Fidelity Index (SFI). Birds were sexed using a discriminant function based on biometrics of a large set of molecularly sexed sanderlings (n = 990). The vast majority of birds were observed at one site only, and the probability of the few detected movements between sites was negatively correlated with the distance among each pair of sites. Hardly any movements were recorded over more than 15 km, suggesting small home ranges. SFI values indicated that juveniles were less site-faithful than adults which may reflect the accumulated knowledge and/or dominance of older animals. Among adults, females were significantly less site faithful than males. A sexual difference in winter site fidelity is unusual in shorebirds. SFI values show site-faithfulness is lower when multiple winters were considered, and most birds seem to chose a wintering site early in the season and use that site throughout the winter. Sanderlings show a very limited tendency to explore alternative wintering options, which might have implications for their survival when facing habitat change or loss (e.g., like severe beach erosion as can be the case at one of the study sites).
Research Interests:
Climate change may influence the phenology of organisms unequally across trophic levels and thus lead to phenological mismatches between predators and prey. In cases where prey availability peaks before reproducing predators reach maximal... more
Climate change may influence the phenology of organisms unequally across trophic levels and thus lead to phenological mismatches between predators and prey. In cases where prey availability peaks before reproducing predators reach maximal prey demand, any negative fitness consequences would selectively favor resynchronization by earlier starts of the reproductive activities of the predators. At a study site in northeast Greenland, over a period of 17 years, the median emergence of the invertebrate prey of Sanderling Calidris alba advanced with 1.27 days per year. Yet, over the same period Sanderling did not advance hatching date. Thus, Sanderlings increasingly hatched after their prey was maximally abundant. Surprisingly, the phenological mismatches did not affect chick growth, but the interaction of the annual width and height of the peak in food abundance did. Chicks grew especially better in years when the food peak was broad. Sanderling clutches were most likely to be depredated early in the season , which should delay reproduction. We propose that high early clutch pre-dation may favor a later reproductive timing. Additionally, our data suggest that in most years food was still abundant after the median date of emergence, which may explain why Sanderlings did not advance breeding along with the advances in arthropod phenology.
Research Interests:
The population of Sanderlings Calidris alba along the East Atlantic flyway has grown considerably during the last decades. Perhaps reflecting this augmented population size, increasing numbers of Sanderling have been reported to stage in... more
The population of Sanderlings Calidris alba along the East Atlantic flyway has grown considerably during the last decades. Perhaps reflecting this augmented population size, increasing numbers of Sanderling have been reported to stage in the Wadden Sea during spring and autumn migration. Estimates of the numbers of Sanderlings in the Wadden Sea have previously been based on a limited number of counts that were not corrected for the turnover of individuals. In this study, we accounted for turnover using estimates of the probability that
individually colour-ringed Sanderlings are still present two days after a sighting. In combination with daily counts during high tide, we estimated the total number of Sanderlings that used the island Griend and surrounding mudflats, in the western Dutch Wadden Sea, during southward passage in 2013 and 2014. We also estimated minimal staging durations of Sanderlings at Griend. Non-moulting birds were significantly heavier upon capture, which suggests that they were refuelling for long non-stop migratory flights. Winter sightings confirmed that the non-moulting Sanderlings winter in sub-Saharan Africa and that the moulting Sanderlings spent the winter in Europe or northern Africa. With an average minimal stay in the western Dutch Wadden Sea of 9 days in 2013 and 12 in 2014, non-moulting Sanderlings stayed for a much shorter time
than moulting Sanderlings, which stayed for 32 days in 2013 and 36 days in 2014. Non-moulting individuals were less likely to be resighted between years. Estimates of minimal staging duration are likely underestimates of the true staging duration, and we propose that moulting Sanderlings probably complete
their wing moult in the Wadden Sea. We estimated that the total number of Sanderlings using the western Dutch Wadden Sea before migration to European or African wintering areas were 27,546 (95% CI 22,739–41,449) in 2013 and 22,574 (95% CI 16,436–46,114) in 2014. This would amount to 11–14% of a total flyway population of 200,000 individuals, representing an amazing degree of concentration for what is regarded as a rather widely and thinly spread shorebird species.
individually colour-ringed Sanderlings are still present two days after a sighting. In combination with daily counts during high tide, we estimated the total number of Sanderlings that used the island Griend and surrounding mudflats, in the western Dutch Wadden Sea, during southward passage in 2013 and 2014. We also estimated minimal staging durations of Sanderlings at Griend. Non-moulting birds were significantly heavier upon capture, which suggests that they were refuelling for long non-stop migratory flights. Winter sightings confirmed that the non-moulting Sanderlings winter in sub-Saharan Africa and that the moulting Sanderlings spent the winter in Europe or northern Africa. With an average minimal stay in the western Dutch Wadden Sea of 9 days in 2013 and 12 in 2014, non-moulting Sanderlings stayed for a much shorter time
than moulting Sanderlings, which stayed for 32 days in 2013 and 36 days in 2014. Non-moulting individuals were less likely to be resighted between years. Estimates of minimal staging duration are likely underestimates of the true staging duration, and we propose that moulting Sanderlings probably complete
their wing moult in the Wadden Sea. We estimated that the total number of Sanderlings using the western Dutch Wadden Sea before migration to European or African wintering areas were 27,546 (95% CI 22,739–41,449) in 2013 and 22,574 (95% CI 16,436–46,114) in 2014. This would amount to 11–14% of a total flyway population of 200,000 individuals, representing an amazing degree of concentration for what is regarded as a rather widely and thinly spread shorebird species.
Research Interests:
The Greenlandic and west-central Siberian breeding populations of Sanderlings Calidris alba are separated by ca. 2000 km during the breeding season, but mix in Europe to some extent during migration. However, the number of Siberian... more
The Greenlandic and west-central Siberian breeding populations of Sanderlings Calidris alba are separated by ca. 2000 km during the breeding season, but mix in Europe to some extent during migration. However, the number of Siberian Sanderlings that spend the nonbreeding season along the East Atlantic Flyway (extending from western Europe to South Africa), if any, is unknown. Although both populations are considered part of the nominate subspecies C. a. alba based on morphology, population structure in Sanderlings has yet to be described with molecular methods. We examined genetic differentiation at the mtDNA control region (CR) and seven microsatellite loci between Greenland- and Siberia-breeding Sanderlings in order to: (1) develop a diagnostic tool
for assessing the breeding origin of Sanderlings along the East Atlantic Flyway, and (2) provide a comparison with the co-distributed and ecologically similar Red Knot, in which CR differentiation of geographically analogous populations (C. canutus islandica and C. c. canutus) has indicated isolation of lineages near the time of the last glacial maximum. By contrast, we found only weak differentiation between the Sanderling breeding populations at the CR, and no differentiation at microsatellite loci. These results suggest that the assignment of breeding origin of Sanderlings on Afro-European flyways will not be possible with simple and inexpensive genetic methods, and imply that Sanderlings and Red Knots have very different
post-glacial phylogeographic histories.
for assessing the breeding origin of Sanderlings along the East Atlantic Flyway, and (2) provide a comparison with the co-distributed and ecologically similar Red Knot, in which CR differentiation of geographically analogous populations (C. canutus islandica and C. c. canutus) has indicated isolation of lineages near the time of the last glacial maximum. By contrast, we found only weak differentiation between the Sanderling breeding populations at the CR, and no differentiation at microsatellite loci. These results suggest that the assignment of breeding origin of Sanderlings on Afro-European flyways will not be possible with simple and inexpensive genetic methods, and imply that Sanderlings and Red Knots have very different
post-glacial phylogeographic histories.
Research Interests:
How food webs are structured has major implications for their stability and dynamics. While poorly studied to date, arctic food webs are commonly assumed to be simple in structure, with few links per species. If this is the case, then... more
How food webs are structured has major implications for their stability and dynamics. While poorly studied to date, arctic food webs are commonly assumed to be simple in structure, with few links per species. If this is the case, then different parts of the web may be weakly connected to each other, with populations and species united by only a low number of links. We provide the first highly resolved description of trophic link structure for a large part of a high-arctic food web. For this purpose, we apply a combination of recent techniques to describing the links between three predator guilds insectivorous birds, spiders, and lepidopteran parasitoids) and their two dominant prey orders (Diptera and Lepidoptera). The resultant web shows a dense link structure and no compartmentalization or modularity across the three predator
guilds. Thus, both individual predators and predator guilds tap heavily into the prey community of each other, offering versatile scope for indirect interactions across different parts of the web. The current description of a first but single arctic web may serve as a benchmark toward which to gauge future webs
resolved by similar techniques. Targeting an unusual breadth of predator guilds, and relying on techniques with a high resolution, it suggests that species in this web are closely connected. Thus, our findings call for similar explorations of
link structure across multiple guilds in both arctic and other webs. From an applied perspective, our description of an arctic web suggests new avenues for understanding how arctic food webs are built and function and of how they respond to current climate change. It suggests that to comprehend the community-level consequences of rapid arctic warming, we should turn from analyses of populations, population pairs, and isolated predator–prey interactions to considering the full set of interacting species.
guilds. Thus, both individual predators and predator guilds tap heavily into the prey community of each other, offering versatile scope for indirect interactions across different parts of the web. The current description of a first but single arctic web may serve as a benchmark toward which to gauge future webs
resolved by similar techniques. Targeting an unusual breadth of predator guilds, and relying on techniques with a high resolution, it suggests that species in this web are closely connected. Thus, our findings call for similar explorations of
link structure across multiple guilds in both arctic and other webs. From an applied perspective, our description of an arctic web suggests new avenues for understanding how arctic food webs are built and function and of how they respond to current climate change. It suggests that to comprehend the community-level consequences of rapid arctic warming, we should turn from analyses of populations, population pairs, and isolated predator–prey interactions to considering the full set of interacting species.
Research Interests:
Research Interests:
Research Interests:
Research Interests: Avian migration, Biology, Functional Ecology, Animal Ecology, Ecophysiology, and 12 moreEvolutionary Ecology, Avian Ecology, Biological Sciences, Environmental Sciences, Energy Expenditure, Daily Energy Expenditure, High Arctic, Body Mass, Functional, Breeding birds, Allometric Scaling, and Time Budget
Sanderlings (Calidris alba) are long-distance migratory shorebirds with a non-breeding range that spans temperate and tropical coastal habitats. Breeding in the High Arctic combined with non-breeding seasons in the tropics necessitate... more
Sanderlings (Calidris alba) are long-distance migratory shorebirds with a non-breeding range that spans temperate and tropical coastal habitats. Breeding in the High Arctic combined with non-breeding seasons in the tropics necessitate long migrations, which are energetically demanding. On an annual basis, the higher energy expenditures during migration might pay off if food availability in the tropics is higher than at temperate latitudes. We compared foraging behaviour of birds at a north temperate and a tropical non-breeding site in the Netherlands and Ghana, respectively. In both cases the birds used similar habitats (open beaches), and experienced similar periods of daylight, which enabled us to compare food abundance and availability, and behavioural time budgets and food intake. During the non-breeding season, Sanderlings in the Netherlands spent 79% of their day foraging; in Ghana birds spent only 38% of the daytime period foraging and the largest proportion of their time resting (58%). The main prey item in the Netherlands was the soft-bodied polychaete Scolelepis squamata, while Sanderlings in Ghana fed almost exclusively on the bivalve Donax pulchellus, which they swallowed whole and crushed internally. Average availability of polychaete worms in the Netherlands was 7.4 g ash free dry mass (AFDM) m −2 , which was one tenth of the 77.1 g AFDM m −2 estimated for the beach in Ghana. In the tropical environment of Ghana the Sanderlings combined relatively low energy requirements with high prey intake rates (1.64 mg opposed to 0.13 mg AFDM s −1 for Ghana and the Netherlands respectively). Although this may suggest that the Ghana beaches are the most favourable environment, processing the hard-shelled bivalve (D. pulchellus) which is the staple food could be costly. The large amount of daytime spent resting in Ghana may be indicative of the time needed to process the shell fragments, rather than indicate rest.
Research Interests:
Arctic weather in spring is unpredictable and can also be extreme, so Arctic-breeding birds must be flexible in their breeding to deal with such variability. Unpredictability in weather conditions will only intensify with climate change... more
Arctic weather in spring is unpredictable and can also be extreme, so Arctic-breeding birds must be flexible in their breeding to deal with such variability. Unpredictability in weather conditions will only intensify with climate change and this in turn could affect reproductive capability of migratory
birds. Adjustments to coping strategies are therefore crucial, so here we examined the plasticity of the adrenocorticotropic stress response in two Arctic songbird species—the snow bunting (Plectrophenax nivalis) and Lapland longspur (Calcarius lapponicus)—breeding in northwest Greenland. Across the breeding season, the stress response was strongest at arrival and least robust during molt in male snow buntings. Snow bunting females had higher baseline but similar stress induced corticosterone levels compared to males. Modification of the stress response was not due to adrenal insensitivity, but likely regulated at the anterior pituitary gland. Compared to
independent nestlings and adult snow buntings, parental-dependent chicks had a more robust stress response. For Lapland longspurs, baseline corticosterone was highest at arrival in both male and females, and arriving males displayed a higher stress response compared to arriving females. Comparison of male corticosterone profiles collected at arrival in Greenland (76°N) and Alaska (67–71°N;) reveal that both species have higher stress responses at the more northern location. Flexibility in the stress response may be typical for birds nesting at the leading edges of their range and this ability will become more relevant as global climate change results in major shifts of breeding habitat and phenology for migratory birds.
birds. Adjustments to coping strategies are therefore crucial, so here we examined the plasticity of the adrenocorticotropic stress response in two Arctic songbird species—the snow bunting (Plectrophenax nivalis) and Lapland longspur (Calcarius lapponicus)—breeding in northwest Greenland. Across the breeding season, the stress response was strongest at arrival and least robust during molt in male snow buntings. Snow bunting females had higher baseline but similar stress induced corticosterone levels compared to males. Modification of the stress response was not due to adrenal insensitivity, but likely regulated at the anterior pituitary gland. Compared to
independent nestlings and adult snow buntings, parental-dependent chicks had a more robust stress response. For Lapland longspurs, baseline corticosterone was highest at arrival in both male and females, and arriving males displayed a higher stress response compared to arriving females. Comparison of male corticosterone profiles collected at arrival in Greenland (76°N) and Alaska (67–71°N;) reveal that both species have higher stress responses at the more northern location. Flexibility in the stress response may be typical for birds nesting at the leading edges of their range and this ability will become more relevant as global climate change results in major shifts of breeding habitat and phenology for migratory birds.
Research Interests:
Research in the Netherlands knows a long history in bird tracking studies. In this introduction to the special issue of Limosa on bird tracking, we provide an overview of different bird tracking techniques, and their use in the... more
Research in the Netherlands knows a long history in bird
tracking studies. In this introduction to the special issue of
Limosa on bird tracking, we provide an overview of different
bird tracking techniques, and their use in the
Netherlands. Also studies were considered in which
birds tagged abroad passed or ended up in the Netherlands. We identified an impressive amount of Dutch tracking studies. Radio transmitters have been used most frequently, mainly for studies focussing on local behaviour (e.g. habitat use). For migration studies researchers relied on (gps-based) satellite telemetry and, recently, light-level geolocation. Modern gps-loggers like the UvA-BiTS and e-obs are currently the most advanced tracking systems, and because of the plethora of accurate data these systems provide, they have been used for both local habitat use and migration studies. More complex tracking systems, such as Encounternet and TOA have only been used by specialised institutions. Tracking studies have enormously boosted our understanding of the behaviour and movements of birds, both at the local and global scale.
tracking studies. In this introduction to the special issue of
Limosa on bird tracking, we provide an overview of different
bird tracking techniques, and their use in the
Netherlands. Also studies were considered in which
birds tagged abroad passed or ended up in the Netherlands. We identified an impressive amount of Dutch tracking studies. Radio transmitters have been used most frequently, mainly for studies focussing on local behaviour (e.g. habitat use). For migration studies researchers relied on (gps-based) satellite telemetry and, recently, light-level geolocation. Modern gps-loggers like the UvA-BiTS and e-obs are currently the most advanced tracking systems, and because of the plethora of accurate data these systems provide, they have been used for both local habitat use and migration studies. More complex tracking systems, such as Encounternet and TOA have only been used by specialised institutions. Tracking studies have enormously boosted our understanding of the behaviour and movements of birds, both at the local and global scale.
Research Interests:
To be able to set priorities in species conservation planning, we need to know how these species prioritize the environment themselves, i.e. what they consider to be better and worse sites. We present a unique and relevant case from... more
To be able to set priorities in species conservation planning, we need to know how these species prioritize the environment themselves, i.e. what they consider
to be better and worse sites. We present a unique and relevant case from tropical West-Africa based on 20 years of monthly counts of wetland sites spread along the 550 km long coast of Ghana. The Ghanaian Sanderling Calidris alba
population increased almost fourfold from average monthly total counts of c. 1350 Sanderlings to 4850 during the study period. Interestingly, with this considerable increase, the sites with the larger numbers at the start of the survey showed the smallest relative increases during 20 years of monitoring. This pattern is consistent with a buffer effect and suggests that with an increasing overall population the best quality sites are filled up, so that additional birds will be forced to use lower quality sites. The preferred site in Ghana, a stretch of beach near the village of Esiama between the Amansuri-Ankobra estuaries, is now entirely unprotected. We argue that the site should be placed higher on the conservation agenda given the fact that up to 3.5% of the Sanderling population connecting Greenland with West- and southern Africa rely on this site.
to be better and worse sites. We present a unique and relevant case from tropical West-Africa based on 20 years of monthly counts of wetland sites spread along the 550 km long coast of Ghana. The Ghanaian Sanderling Calidris alba
population increased almost fourfold from average monthly total counts of c. 1350 Sanderlings to 4850 during the study period. Interestingly, with this considerable increase, the sites with the larger numbers at the start of the survey showed the smallest relative increases during 20 years of monitoring. This pattern is consistent with a buffer effect and suggests that with an increasing overall population the best quality sites are filled up, so that additional birds will be forced to use lower quality sites. The preferred site in Ghana, a stretch of beach near the village of Esiama between the Amansuri-Ankobra estuaries, is now entirely unprotected. We argue that the site should be placed higher on the conservation agenda given the fact that up to 3.5% of the Sanderling population connecting Greenland with West- and southern Africa rely on this site.
Research Interests:
Sandpipers and allies (Scolopacidae) show an astounding diversity in mating and parental care strategies. Comparative studies have tried to interpret this variation in terms of phylogenetic constraints and ecological shaping factors. In... more
Sandpipers and allies (Scolopacidae) show an astounding diversity in mating and parental care strategies. Comparative studies have tried to interpret this variation in terms of phylogenetic constraints and ecological shaping factors. In such analyses, mating and parental care systems are necessarily discretely classified at the species level. The few available descriptive studies on breeding strategies of the Sanderling (Calidris alba) came to variable conclusions, which, in turn, were inconsistently used in these comparative studies. We provide empirical data on mating and
parental care patterns in Sanderlings studied during six summers in northeast Greenland. In 135 clutches, we determined parental care from incubation profiles using temperature loggers and confirmed that both uniparental incubation by both sexes and biparental incubation (45 and 90 clutches, respectively) occurred. We used microsatellite-based parentage analyses to describe the degree of extrapair mating. In 48 completely assayed families, we found 6 cases of polygamy (4 cases of polyandry, 2 cases of polygyny) that involved both uniparental and biparental clutches. This implies substantial variation in the patterns of mating and parental care, defying categorical assignments even at the local level. We conclude that the classification of mating strategy and parental care pattern for the Sanderling has been rather coarse, and that comparative analyses have not taken the observed ntrapopulation variability into account. Because sandpipers show such variable reproductive behavior, between and within species,
more detailed descriptive studies using parentage analyses are required to revisit previous statements about the intensity of sexual selection, including sexual size dimorphism, in shorebirds. In view of the great variability, methods of comparison will need elaboration too.
parental care patterns in Sanderlings studied during six summers in northeast Greenland. In 135 clutches, we determined parental care from incubation profiles using temperature loggers and confirmed that both uniparental incubation by both sexes and biparental incubation (45 and 90 clutches, respectively) occurred. We used microsatellite-based parentage analyses to describe the degree of extrapair mating. In 48 completely assayed families, we found 6 cases of polygamy (4 cases of polyandry, 2 cases of polygyny) that involved both uniparental and biparental clutches. This implies substantial variation in the patterns of mating and parental care, defying categorical assignments even at the local level. We conclude that the classification of mating strategy and parental care pattern for the Sanderling has been rather coarse, and that comparative analyses have not taken the observed ntrapopulation variability into account. Because sandpipers show such variable reproductive behavior, between and within species,
more detailed descriptive studies using parentage analyses are required to revisit previous statements about the intensity of sexual selection, including sexual size dimorphism, in shorebirds. In view of the great variability, methods of comparison will need elaboration too.
The Long-tailed Skua, a small (,300 g) Arctic-breeding predator and seabird, is a functionally very important component of the Arctic vertebrate communities in summer, but little is known about its migration and winter distribution. We... more
The Long-tailed Skua, a small (,300 g) Arctic-breeding predator and seabird, is a functionally very important component of
the Arctic vertebrate communities in summer, but little is known about its migration and winter distribution. We used lightlevel
geolocators to track the annual movements of eight adult birds breeding in north-east Greenland (n = 3) and Svalbard
(n = 5). All birds wintered in the Southern Hemisphere (mean arrival-departure dates on wintering grounds: 24 October-21
March): five along the south-west coast of Africa (0–40uS, 0–15uE), in the productive Benguela upwelling, and three further
south (30–40uS, 0–50uE), in an area extending into the south-west Indian Ocean. Different migratory routes and rates of
travel were documented during post-breeding (345 km d21 in late August-early September) and spring migrations (235 km
d21 in late April) when most birds used a more westerly flyway. Among the different staging areas, a large region off the
Grand Banks of Newfoundland appears to be the most important. It was used in autumn by all but one of the tracked birds
(from a few days to three weeks) and in spring by five out of eight birds (from one to more than six weeks). Two other
staging sites, off the Iberian coast and near the Azores, were used by two birds in spring for five to six weeks. Over one year,
individuals travelled between 43,900 and 54,200 km (36,600–45,700 when excluding staging periods) and went as far as 10,500–13,700 km (mean 12,800 km) from their breeding sites. This study has revealed important marine areas in both the
south and north Atlantic Ocean. Sustainable management of these ocean basins will benefit Long-tailed Skuas as well as
other trans-equatorial migrants from the Arctic.
the Arctic vertebrate communities in summer, but little is known about its migration and winter distribution. We used lightlevel
geolocators to track the annual movements of eight adult birds breeding in north-east Greenland (n = 3) and Svalbard
(n = 5). All birds wintered in the Southern Hemisphere (mean arrival-departure dates on wintering grounds: 24 October-21
March): five along the south-west coast of Africa (0–40uS, 0–15uE), in the productive Benguela upwelling, and three further
south (30–40uS, 0–50uE), in an area extending into the south-west Indian Ocean. Different migratory routes and rates of
travel were documented during post-breeding (345 km d21 in late August-early September) and spring migrations (235 km
d21 in late April) when most birds used a more westerly flyway. Among the different staging areas, a large region off the
Grand Banks of Newfoundland appears to be the most important. It was used in autumn by all but one of the tracked birds
(from a few days to three weeks) and in spring by five out of eight birds (from one to more than six weeks). Two other
staging sites, off the Iberian coast and near the Azores, were used by two birds in spring for five to six weeks. Over one year,
individuals travelled between 43,900 and 54,200 km (36,600–45,700 when excluding staging periods) and went as far as 10,500–13,700 km (mean 12,800 km) from their breeding sites. This study has revealed important marine areas in both the
south and north Atlantic Ocean. Sustainable management of these ocean basins will benefit Long-tailed Skuas as well as
other trans-equatorial migrants from the Arctic.
In August and September 2011 we observed a very large number of Sanderlings on the mudflats close to the island of Griend in the central Dutch Wadden Sea. Colour-ring resightings of birds that were ringed in the Wadden Sea or abroad... more
In August and September 2011 we observed a very large number of Sanderlings on the mudflats close to the island of Griend in the central Dutch Wadden Sea. Colour-ring resightings of birds that were ringed in the Wadden Sea or abroad and/or were later re-sighted elsewhere showed that the Wadden Sea is visited by Sanderlings that winter anywhere along the Western European and West-African coast south of the Wadden Sea, from The Netherlands south to at least Namibia. These Sanderlings breed in Greenland. Whether Western Europe is also frequented by Sanderlings from the Siberian breeding populations remains a matter of debate. Based on a few counts, as well as the proportion of colourringed individuals in flocks and the total number of different individuals present in the area at the time, we estimate that in August 37,000 (95% confidence interval 13,200 – 61,800)
and in September 11,200 (CI 4,500 – 17,900) Sanderlings used the central western Dutch Wadden Sea during the southward migration season of 2011. The presence of 16% juveniles in September which were not observed in August suggests a fair amount of turnover. This suggests that a third of the
presently estimated total population size may stop over in the Wadden Sea, but we take this conclusion with a grain of salt and suggest that both the total population size estimate and the estimate of the number of Sanderlings in the Wadden Sea need reassessment.
and in September 11,200 (CI 4,500 – 17,900) Sanderlings used the central western Dutch Wadden Sea during the southward migration season of 2011. The presence of 16% juveniles in September which were not observed in August suggests a fair amount of turnover. This suggests that a third of the
presently estimated total population size may stop over in the Wadden Sea, but we take this conclusion with a grain of salt and suggest that both the total population size estimate and the estimate of the number of Sanderlings in the Wadden Sea need reassessment.
Telescope scanning of flocks of shorebirds to age individuals by plumage characteristics has increasingly been used to assess the proportion of first-year birds in local populations. To standardise measurements of the proportion of... more
Telescope scanning of flocks of shorebirds to age individuals by plumage characteristics has increasingly been used to assess the proportion of first-year birds in local populations. To standardise measurements of the
proportion of juveniles for a local wintering population it is necessary to know when this can be measured without possible biases due to migration or moult. We investigated how the proportion of juvenile Sanderlings
Calidris alba changed between mid-Jul and early Nov 2009–2011 on the Island of Tiree, Scotland. We suggest measuring juvenile proportion of locally wintering Sanderlings in NW Europe between mid-September and
the end of October, because migration has terminated by then and juveniles can still be aged using field characteristics. During this time of the year the proportion of juveniles at Tiree was similar between the three years (6–9%).
proportion of juveniles for a local wintering population it is necessary to know when this can be measured without possible biases due to migration or moult. We investigated how the proportion of juvenile Sanderlings
Calidris alba changed between mid-Jul and early Nov 2009–2011 on the Island of Tiree, Scotland. We suggest measuring juvenile proportion of locally wintering Sanderlings in NW Europe between mid-September and
the end of October, because migration has terminated by then and juveniles can still be aged using field characteristics. During this time of the year the proportion of juveniles at Tiree was similar between the three years (6–9%).
We isolated and tested six novel microsatellite loci in Sanderling (Calidris alba) from Greenland for paternity analyses. In addition, we tested 11 already published microsatellite markers which were originally developed for the... more
We isolated and tested six novel microsatellite
loci in Sanderling (Calidris alba) from Greenland for
paternity analyses. In addition, we tested 11 already published
microsatellite markers which were originally
developed for the congeneric species, the Pectoral Sandpiper
(C. melanotos). All loci were polymorphic, but five of
the cross-species loci were not scorable due to suboptimal
amplification patterns. The 12 successful loci were tested
on 87 individuals, yielding an average of 9.0 (range 4–19)
alleles per locus and mean expected heterozygosity of
0.70. Because this dataset contained families, tests for
Hardy–Weinberg equilibrium, linkage disequilibrium and
probability of identity were done on a subset of the data
containing 25 adults caught in the same year. The overall
probability of identity was 1.0 9 10-13. Only one locus
displayed significant homozygote excess and all loci were
unlinked. On the basis of female heterozygotes, all loci are
assumed to be autosomal.
loci in Sanderling (Calidris alba) from Greenland for
paternity analyses. In addition, we tested 11 already published
microsatellite markers which were originally
developed for the congeneric species, the Pectoral Sandpiper
(C. melanotos). All loci were polymorphic, but five of
the cross-species loci were not scorable due to suboptimal
amplification patterns. The 12 successful loci were tested
on 87 individuals, yielding an average of 9.0 (range 4–19)
alleles per locus and mean expected heterozygosity of
0.70. Because this dataset contained families, tests for
Hardy–Weinberg equilibrium, linkage disequilibrium and
probability of identity were done on a subset of the data
containing 25 adults caught in the same year. The overall
probability of identity was 1.0 9 10-13. Only one locus
displayed significant homozygote excess and all loci were
unlinked. On the basis of female heterozygotes, all loci are
assumed to be autosomal.
Research Interests:
Birds breeding in cold environments regularly have to interrupt incubation to forage, causing a trade-off between two mutually exclusive behaviours. Earlier studies showed that uniparental Arctic sandpipers overall spend less time... more
Birds breeding in cold environments regularly have to interrupt incubation to forage, causing a trade-off between two mutually exclusive behaviours. Earlier studies showed that uniparental Arctic sandpipers overall spend less time incubating their eggs than biparental species, but interspecific differences in size and ecology were potential confounding factors. This study reports on a within-species comparison of breeding schedules and metal egg temperatures in uni- and biparental sanderlings (Calidris alba) in Northeast Greenland in relation to ambient temperature. We recorded incubation schedules with nest temperature loggers in 34 sanderling clutches (13 uniparentals, 21 biparentals). The temperature of a metal egg placed within the clutch of 17 incubating birds (6 uniparentals, 9 biparentals) was measured as an indicator of the heat put into eggs. Recess frequency, recess duration and total recess time were higher in uniparentals than in biparentals and positively correlated with ambient temperatures in uniparentals only. Uniparental sanderlings maintained significantly higher metal egg temperatures during incubation than biparentals (1.4uC difference on average). Our results suggest that uniparental sanderlings compensate for the lower nest attendance, which may prolong the duration of the incubation period and negatively affect the condition of the hatchlings, by maintaining a higher heat flux into the eggs.
Research Interests:
By following the fate of both floated and non-floated eggs from individual clutches of four Arctic wader (shorebird) species, we show that the use of the flotation method for determining incubation stage of eggs (which involves both the... more
By following the fate of both floated and non-floated eggs from individual clutches of four Arctic wader (shorebird) species, we show that the use of the flotation method for determining incubation stage of eggs (which involves both the submersion and handling of eggs) does not negatively affect hatchability.
Research Interests:
Despite the worldwide occurrence of Sanderlings Calidris alba on popular beaches, strikingly little is known about their biology compared to other common waders. Here we review the limited available knowledge of Sanderlings that use... more
Despite the worldwide occurrence of Sanderlings Calidris alba on popular beaches, strikingly little is known about their biology compared to other common waders. Here we review the limited available knowledge of Sanderlings that use African–Eurasian flyways. The basis for this review was a workshop on Sanderlings, held during the International Wader Study Group conference in Jastrzębia Góra, Poland in 2008. We focus on biogeography, trends, numbers, diet, migration patterns and reproduction. Gaps in our knowledge are identified and we discuss the evidence for a Siberian origin of Sanderlings wintering in NW Europe, and plead for more
non-estuarine surveys and collaboration between colour-ring projects both in space and time to get a better understanding of population dynamics and migration phenology.
non-estuarine surveys and collaboration between colour-ring projects both in space and time to get a better understanding of population dynamics and migration phenology.
Research Interests:
It has long been recognised that nest depredation by olfactory-searching mammals greatly influences the reproductive success of ground-nesting birds. Yet adaptations of birds to diminish smell during nesting have rarely been... more
It has long been recognised that nest depredation by
olfactory-searching mammals greatly influences the
reproductive success of ground-nesting birds. Yet
adaptations of birds to diminish smell during nesting have
rarely been investigated. Recently, a remarkable shift in
the composition of uropygial gland secretions (preen
waxes) was discovered in many ground-nesting shorebirds
and ducks that begin incubation, during which the usual
mixtures of monoester preen waxes are replaced by
mixtures of less volatile diester waxes. In this study we
show experimentally that an olfactory-searching dog had
greater difficulty detecting mixtures of the less volatile
diesters than mixtures of monoesters. This is consistent
with the hypothesis that diester preen waxes reduce birds’
smell and thereby reduce predation risk.
olfactory-searching mammals greatly influences the
reproductive success of ground-nesting birds. Yet
adaptations of birds to diminish smell during nesting have
rarely been investigated. Recently, a remarkable shift in
the composition of uropygial gland secretions (preen
waxes) was discovered in many ground-nesting shorebirds
and ducks that begin incubation, during which the usual
mixtures of monoester preen waxes are replaced by
mixtures of less volatile diester waxes. In this study we
show experimentally that an olfactory-searching dog had
greater difficulty detecting mixtures of the less volatile
diesters than mixtures of monoesters. This is consistent
with the hypothesis that diester preen waxes reduce birds’
smell and thereby reduce predation risk.
Research Interests:
Previous studies have shown that preen wax composition in some sandpipers shifts from the usual monoesters to diesters during the breeding season, possibly to reduce the ability of mammalian predators to find nests using olfactory cues.... more
Previous studies have shown that preen wax composition in some sandpipers shifts from the usual monoesters to diesters during the breeding season, possibly to reduce the ability of mammalian predators to find nests using olfactory cues. To investigate further the relationship between incubation and wax secretion, we examined seven sandpiper species with different incubation patterns (species in which both sexes incubate, in which only males incubate and in which only females incubate). During the breeding period, diester preen wax was secreted almost exclusively by the incubating sex in species with uniparental incubation, and by both sexes in species with biparental incubation. These findings suggest that diester preen waxes have a function that is directly related to incubation. Unexpectedly, in female-incubating Curlew Sandpiper Calidris ferruginea and Buff-breasted Sandpiper
Tryngites subruficollis , some males also secreted diester preen waxes during the breeding period. This suggests that some males may in fact incubate, that these waxes may be a remnant from their evolutionary past when both sexes incubated, or that males need to be olfactorally cryptic because they are involved in the making of nest scrapes.
The seasonal pattern of preen wax composition was also studied in captive male, female and female-mimicking male (‘faeder’) Ruff Philomachus pugnax. Captive female Ruff changed preen wax composition from monoesters to diesters in the spring despite the fact that no incubation took place. This suggests that circannual rhythms rather than actual incubation behaviour may trigger the shift to diester waxes. All captive male Ruff, including the faeders, continued to secrete monoesters, supporting the hypothesis that only the incubating sex secretes diesters.
Tryngites subruficollis , some males also secreted diester preen waxes during the breeding period. This suggests that some males may in fact incubate, that these waxes may be a remnant from their evolutionary past when both sexes incubated, or that males need to be olfactorally cryptic because they are involved in the making of nest scrapes.
The seasonal pattern of preen wax composition was also studied in captive male, female and female-mimicking male (‘faeder’) Ruff Philomachus pugnax. Captive female Ruff changed preen wax composition from monoesters to diesters in the spring despite the fact that no incubation took place. This suggests that circannual rhythms rather than actual incubation behaviour may trigger the shift to diester waxes. All captive male Ruff, including the faeders, continued to secrete monoesters, supporting the hypothesis that only the incubating sex secretes diesters.
Research Interests:
Recently, a shift in preen wax composition, from lower molecular weight monoesters to higher molecular weight diesters, was described for individuals of a sandpiper species (red knot, Calidris canutus) that were about to leave for the... more
Recently, a shift in preen wax composition, from lower molecular weight monoesters to higher molecular weight diesters, was described for individuals of a sandpiper species (red knot, Calidris canutus) that were about to leave for the tundra breeding grounds. The timing of the shift indicated that diester waxes served as a quality signal during mate choice. Here, this hypothesis is evaluated on the basis of a survey of preen wax composition in 19 sandpiper species. All of these species showed the same shift observed in the high-Arctic breeding red knots. As the shift also occurred in temperate breeding species, it is not speci c to tundra-breeding sandpipers. Both sexes produced the diester waxes during the incubation period until hatching, in addition to the short period of courtship, indicating that diesters’ functions extend beyond
that of a sexually selected ‘make-up’. The few non-incubating birds examined (males of curlew sandpipers (C. ferruginea) and ruffs (Philomachus pugnax)) had the lowest likelihood of secreting diesters, indicating a functional role for diester preen waxes during incubation. We propose that diester preen waxes enhance olfactory crypsis at the nest.
that of a sexually selected ‘make-up’. The few non-incubating birds examined (males of curlew sandpipers (C. ferruginea) and ruffs (Philomachus pugnax)) had the lowest likelihood of secreting diesters, indicating a functional role for diester preen waxes during incubation. We propose that diester preen waxes enhance olfactory crypsis at the nest.
Research Interests:
A uniquely intense field effort at Zackenberg, NE Greenland, in June–July 2003 made it possible, for the first time, to compare two methods of measuring breeding densities of two notoriously difficult-to-census High Arctic breeding... more
A uniquely intense field effort at Zackenberg, NE Greenland, in June–July 2003 made it possible, for the first time, to compare two methods of measuring breeding densities of two notoriously difficult-to-census High Arctic breeding shorebirds (Red Knot Calidris canutus and Sanderling Calidris alba): (1) mapping of displays and other activities of birds in a rapid assessment early in the season, and (2) systematic ‘roping’ of potential breeding areas to disturb and then find incubating birds on, or very close to, their nests. The latter method is particularly relevant to species that rely on crypsis to avoid nest detection. During 16 and 19 June an experienced observer, in a standardized way, mapped all visual observations of Red Knot and Sanderling over a 4.0 km2
study area, which consisted mainly of low-angle mountain slopes between altitudes of 100 and 400 m. The observations were interpreted to represent 8–9 ‘pairs’ of Red Knot and 13–17 ‘pairs’ of Sanderling. Observations nearby allowed for a few additional pairs of Red Knot. Between 17 June and 5 July a team of five observers systematically roped the same study area and found two Red Knot nests and 15 Sanderling nests. Most of the study area remained under daily scrutiny until 19 July, and during these visits we encountered two more families
of Red Knots and seven more Sanderling families. Thus, the roping effort yielded a few more Sanderling ‘pairs’ than expected from the early-season survey, but fewer Red Knot. This may imply that either: (1) the early-season rapid assessment particularly overestimated the knot population, and/or (2) relative to Sanderlings, knot nests were heavily depredated before roping, and/or (3) incubating birds escaped notice during roping, and/or (4) some of the local Red Knots may not have started a breeding attempt at all. Further work with radiotagged individuals is necessary to establish whether we need to invoke non-breeding as a cause of the discrepancy.
study area, which consisted mainly of low-angle mountain slopes between altitudes of 100 and 400 m. The observations were interpreted to represent 8–9 ‘pairs’ of Red Knot and 13–17 ‘pairs’ of Sanderling. Observations nearby allowed for a few additional pairs of Red Knot. Between 17 June and 5 July a team of five observers systematically roped the same study area and found two Red Knot nests and 15 Sanderling nests. Most of the study area remained under daily scrutiny until 19 July, and during these visits we encountered two more families
of Red Knots and seven more Sanderling families. Thus, the roping effort yielded a few more Sanderling ‘pairs’ than expected from the early-season survey, but fewer Red Knot. This may imply that either: (1) the early-season rapid assessment particularly overestimated the knot population, and/or (2) relative to Sanderlings, knot nests were heavily depredated before roping, and/or (3) incubating birds escaped notice during roping, and/or (4) some of the local Red Knots may not have started a breeding attempt at all. Further work with radiotagged individuals is necessary to establish whether we need to invoke non-breeding as a cause of the discrepancy.
Research Interests:
It has recently been shown that sandpipers (Scolopacidae) abruptly switch the chemical composition of their preen gland secretions from mono- to diester waxes just before the period of courtship. The timing and context of the shift... more
It has recently been shown that sandpipers (Scolopacidae) abruptly switch the chemical composition of their preen gland secretions from mono- to diester waxes just before the
period of courtship. The timing and context of the shift suggested that diesters could provide a visible quality signal during mate choice. We used captive red knots Calidris
canutus to test whether mono- and diester preen waxes affect the light reflectance (‘‘colour’’) of the plumage. We also determined light absorbance spectra of the two wax types. The reflectance of breast feathers of the breeding plumage was measured with spectrophotometry when birds secreted monoesters and six weeks later when they secreted diester preen waxes. Light reflectance was also measured after removing the mono- and diester waxes from the plumage with a solvent. The results show that: (1) diester preen waxes absorb more light, especially ultraviolet (UV), than monoester
preen waxes, but that (2) the compositional shift in the preen waxes did not change plumage reflectance and, (3) the removal of preen waxes did not change the reflectance
of the plumage within the light spectrum assumed visible to birds (320/700 nm). This is not consistent with the idea that compositional shifts in the preen waxes of red knots
have a visual function.
period of courtship. The timing and context of the shift suggested that diesters could provide a visible quality signal during mate choice. We used captive red knots Calidris
canutus to test whether mono- and diester preen waxes affect the light reflectance (‘‘colour’’) of the plumage. We also determined light absorbance spectra of the two wax types. The reflectance of breast feathers of the breeding plumage was measured with spectrophotometry when birds secreted monoesters and six weeks later when they secreted diester preen waxes. Light reflectance was also measured after removing the mono- and diester waxes from the plumage with a solvent. The results show that: (1) diester preen waxes absorb more light, especially ultraviolet (UV), than monoester
preen waxes, but that (2) the compositional shift in the preen waxes did not change plumage reflectance and, (3) the removal of preen waxes did not change the reflectance
of the plumage within the light spectrum assumed visible to birds (320/700 nm). This is not consistent with the idea that compositional shifts in the preen waxes of red knots
have a visual function.
Research Interests:
Research Interests:
In this study, we tested the hypothesis that baseline corticosterone levels increase with a change from constant to variable feeding schedules. Captive red knots, Calidris canutus, were presented with food that was either available... more
In this study, we tested the hypothesis that baseline corticosterone levels increase with a change from constant to variable feeding schedules. Captive red knots, Calidris
canutus, were presented with food that was either available during the same time each day (constant) or starting at variable times during the day. Food intake rates, frequency of aggressive interactions, and baseline levels of corticosterone were measured. In the majority of cases, red knots showed higher plasma corticosterone concentrations during feeding schedules that were irregular than when food was available at consistent times. These ¢ndings are supported by a previous study that showed that red knots take a long time to adjust to the newly o¡ered, predictable conditions of their aviary environment.The frequency of con£icts in the di¡erent groups and (size-corrected) body mass were not correlated with average corticosterone level.The results are examined in
the light of literature showing that increases in corticosterone in response to acute, unpredictable events mediate behavioral responses such as increased explorative behavior and memory. For red knots that have to ¢nd their food on the temperate-zone mud£ats inWestern Europe, an increased
circulating corticosterone level may be adaptive during periods when the patchily distribution of buried bivalves and the burying behavior of such prey presents them with a variable and unpredictable food supply.
canutus, were presented with food that was either available during the same time each day (constant) or starting at variable times during the day. Food intake rates, frequency of aggressive interactions, and baseline levels of corticosterone were measured. In the majority of cases, red knots showed higher plasma corticosterone concentrations during feeding schedules that were irregular than when food was available at consistent times. These ¢ndings are supported by a previous study that showed that red knots take a long time to adjust to the newly o¡ered, predictable conditions of their aviary environment.The frequency of con£icts in the di¡erent groups and (size-corrected) body mass were not correlated with average corticosterone level.The results are examined in
the light of literature showing that increases in corticosterone in response to acute, unpredictable events mediate behavioral responses such as increased explorative behavior and memory. For red knots that have to ¢nd their food on the temperate-zone mud£ats inWestern Europe, an increased
circulating corticosterone level may be adaptive during periods when the patchily distribution of buried bivalves and the burying behavior of such prey presents them with a variable and unpredictable food supply.
After a migratory flight of several thousand kilometers to their high arctic breeding grounds, red knots (Calidris canutus islandica, Scolopacidae) showed high baseline concentrations of plasma corticosterone (58 ng/mL). Such high... more
After a migratory flight of several thousand kilometers to their
high arctic breeding grounds, red knots (Calidris canutus islandica, Scolopacidae) showed high baseline concentrations of plasma corticosterone (58 ng/mL). Such high baseline corticosterone levels may be conditional for the right behavioral and metabolic adjustments to environmental and social stresses that shorebirds experience on arrival in an unpredictable tundra breeding environment. Despite the high baseline levels of corticosterone, red knots still showed a marked stress response during the postarrival period, with corticosterone concentrations increasing significantly during a 60-min period of confinement. Baseline levels of corticosterone declined as the breeding season progressed. Red knots with brood patches, that is, birds that had completed egg laying and commenced incubation, had a reduced adrenocortical response to the stress of confinement compared with red knots with no, or with halfdeveloped, brood patches. This is consistent with the idea that birds breeding in extreme environments with short breeding seasons may exhibit a decreased adrenocortical response to stressful events to prevent high corticosterone concentrations from inducing interruptions of reproductive behavior.
high arctic breeding grounds, red knots (Calidris canutus islandica, Scolopacidae) showed high baseline concentrations of plasma corticosterone (58 ng/mL). Such high baseline corticosterone levels may be conditional for the right behavioral and metabolic adjustments to environmental and social stresses that shorebirds experience on arrival in an unpredictable tundra breeding environment. Despite the high baseline levels of corticosterone, red knots still showed a marked stress response during the postarrival period, with corticosterone concentrations increasing significantly during a 60-min period of confinement. Baseline levels of corticosterone declined as the breeding season progressed. Red knots with brood patches, that is, birds that had completed egg laying and commenced incubation, had a reduced adrenocortical response to the stress of confinement compared with red knots with no, or with halfdeveloped, brood patches. This is consistent with the idea that birds breeding in extreme environments with short breeding seasons may exhibit a decreased adrenocortical response to stressful events to prevent high corticosterone concentrations from inducing interruptions of reproductive behavior.
1. Given the allometric scaling of thermoregulatory capacity in birds, and the cold and exposed Arctic environment, it was predicted that Arctic-breeding shorebirds should incur high costs during incubation. Using doubly labelled water... more
1.
Given the allometric scaling of thermoregulatory capacity in birds, and the cold and exposed Arctic environment, it was predicted that Arctic-breeding shorebirds should incur high costs during incubation. Using doubly labelled water (DLW), daily energy expenditure (DEE) during incubation was measured in eight shorebird species weighing between 29 and 142 g at various sites in the Eurasian and Canadian High Arctic. The results are compared with a compilation of similar data for birds at lower latitudes.
2.
There was a significant positive correlation between species average DEE and body mass (DEE (kJ day−1) = 28·12 BM (g)
0·524, r2= 0·90). The slopes of the allometric regression lines for DEE on body mass of tundra-breeding birds and lower latitude species (a sample mostly of passerines but including several shorebirds) are similar (0·548 vs 0·545). DEE is about 50% higher in birds on the tundra than in temperate breeding areas.
3.
Data for radiomarked Red Knots for which the time budgets during DLW measurements were known, indicated that foraging away from the nest on open tundra is almost
twice as costly as incubating a four-egg clutch.
4.
During the incubation phase in the High Arctic, tundra-breeding shorebirds appear to incur among the highest DEE levels of any time of the year. The rates of energy
expenditure measured here are among the highest reported in the literature so far, reaching inferred ceilings of sustainable energy turnover rates.
Given the allometric scaling of thermoregulatory capacity in birds, and the cold and exposed Arctic environment, it was predicted that Arctic-breeding shorebirds should incur high costs during incubation. Using doubly labelled water (DLW), daily energy expenditure (DEE) during incubation was measured in eight shorebird species weighing between 29 and 142 g at various sites in the Eurasian and Canadian High Arctic. The results are compared with a compilation of similar data for birds at lower latitudes.
2.
There was a significant positive correlation between species average DEE and body mass (DEE (kJ day−1) = 28·12 BM (g)
0·524, r2= 0·90). The slopes of the allometric regression lines for DEE on body mass of tundra-breeding birds and lower latitude species (a sample mostly of passerines but including several shorebirds) are similar (0·548 vs 0·545). DEE is about 50% higher in birds on the tundra than in temperate breeding areas.
3.
Data for radiomarked Red Knots for which the time budgets during DLW measurements were known, indicated that foraging away from the nest on open tundra is almost
twice as costly as incubating a four-egg clutch.
4.
During the incubation phase in the High Arctic, tundra-breeding shorebirds appear to incur among the highest DEE levels of any time of the year. The rates of energy
expenditure measured here are among the highest reported in the literature so far, reaching inferred ceilings of sustainable energy turnover rates.
Research Interests:
Birds living in seasonal environments change physiology and behavior in correspondence to temporally changing environmental supplies, demands and opportunities. We recently reported that the chemical composition of uropygial gland... more
Birds living in seasonal environments change physiology and behavior in correspondence to temporally changing environmental supplies, demands and opportunities. We
recently reported that the chemical composition of uropygial gland secretions of sandpipers (Scolopacidae, order Charadriformes) changes during the breeding season from mixtures of monoesters to diesters, which fulfill specific functions related to incubation. A proper temporal match between the expression of diester preen waxes and incubation requires a flexible organization of the trait. Here we analyze the possible degrees of flexibility with reference to the functionality of better-understood molt and body mass cycles of free-living and captive red knots (Calidris canutus).
The relative flexibility of seasonal cycles in preen wax composition was examined by two experimental perturbations: (1) giving birds restricted access to food and (2) monitoring them long-term under a constant photoperiodic regime. We found that wax type cannot change instantaneously, but that changing the type of wax is under similar organizational time constraints as the replacement of feathers. Just as molt and mass cycles, the seasonal rhythm of diester secretion appeared to be under endogenous control: most birds placed in a constant photoperiod still maintained seasonally changing preen waxes. Diester preen wax secretion was synchronized with the peak in body mass in spring, but became less well expressed under constant photoperiodic conditions and when food availability was limited.
recently reported that the chemical composition of uropygial gland secretions of sandpipers (Scolopacidae, order Charadriformes) changes during the breeding season from mixtures of monoesters to diesters, which fulfill specific functions related to incubation. A proper temporal match between the expression of diester preen waxes and incubation requires a flexible organization of the trait. Here we analyze the possible degrees of flexibility with reference to the functionality of better-understood molt and body mass cycles of free-living and captive red knots (Calidris canutus).
The relative flexibility of seasonal cycles in preen wax composition was examined by two experimental perturbations: (1) giving birds restricted access to food and (2) monitoring them long-term under a constant photoperiodic regime. We found that wax type cannot change instantaneously, but that changing the type of wax is under similar organizational time constraints as the replacement of feathers. Just as molt and mass cycles, the seasonal rhythm of diester secretion appeared to be under endogenous control: most birds placed in a constant photoperiod still maintained seasonally changing preen waxes. Diester preen wax secretion was synchronized with the peak in body mass in spring, but became less well expressed under constant photoperiodic conditions and when food availability was limited.
During incubation ground-breeding sandpipers such as Red Knots (Calidris canutus) create a warm and humid micro-climate in the nest, conditions that favor the growth of feather-degrading bacteria present in their plumage . Just before... more
During incubation ground-breeding sandpipers such as Red Knots (Calidris canutus) create a warm and humid micro-climate in the nest, conditions that favor the growth of feather-degrading bacteria present in their plumage . Just before incubation the composition of waxes secreted by the uropygial gland of Red Knots and other sandpipers changes quickly and completely from a mixture of only monoesters to a mixture of only diesters. We hypothesized that the change in composition of the preen wax helps protect the plumage against feather-degrading bacteria . We tested the hypothesis by studying growth of the feather-degrading bacterium Bacillus licheniformis, which we found in the plumage of Red Knots . The removal of preen waxes from feathers resulted in faster bacterial degradation, confirming earlier findings that preen wax inhibits growth of feather-degrading bacteria . However, the degradation rate of feathers with preen wax based on diesters did not differ from that of feathers with preen wax based on monoesters . We suggest that preen waxes protect feathers by forming a physical barrier to microbes rather than through chemical properties of the waxes.
There is growing evidence that female birds may adaptively bias the sex ratio of their young as a function of environmental conditions. Data on brood sex ratio in shorebirds are scarce, however. In this study we report the brood sex... more
There is growing evidence that female birds may adaptively bias the sex ratio of their young as a function of environmental conditions. Data on brood sex ratio in shorebirds are scarce, however. In this study we report the brood sex ratios and morphometrics of Arctic sandpipers. Sex was determined in 13–64 chicks of Sanderling Calidris alba, Red Knot Calidris canutus islandica, Dunlin Calidris alpina arctica, and Ruddy
Turnstone Arenaria interpres in NE Greenland during the 2003 breeding season. Brood sex ratios were biased significantly towards males in Dunlin and Ruddy Turnstone, but in Dunlin this bias disappeared in chicks older than two days. There was a non-significant bias towards females in Sanderling and Red Knot. Only for bill length in Dunlin hatchlings, there were significant differences between males and females. Surprisingly, in contrast to their parents, male chicks had longer bills than female chicks.
Turnstone Arenaria interpres in NE Greenland during the 2003 breeding season. Brood sex ratios were biased significantly towards males in Dunlin and Ruddy Turnstone, but in Dunlin this bias disappeared in chicks older than two days. There was a non-significant bias towards females in Sanderling and Red Knot. Only for bill length in Dunlin hatchlings, there were significant differences between males and females. Surprisingly, in contrast to their parents, male chicks had longer bills than female chicks.
Sanderlings Calidris alba occur worldwide along sandy beaches and have a wide range of non-breeding locations in different climate zones. Previous studies clearly indicated that ambient temperatures have profound effects on daily energy... more
Sanderlings Calidris alba occur worldwide along sandy
beaches and have a wide range of non-breeding locations
in different climate zones. Previous studies clearly
indicated that ambient temperatures have profound effects
on daily energy expenditures of Sanderlings. In this
study we investigated the foraging ecology of
Sanderlings on beaches near Esiama, Ghana and on the
Wadden Sea island of Vlieland, The Netherlands. The diet
was very different at the two locations. In Vlieland the
birds fed predominantly on the polychaete Scolelepis
squamata whereas a small shellfish Donax rugosus was
taken in Esiama (Fig. 4,5). The latter prey item was very
abundant in Esiama where a band of 2-14 m width containing
densities of 5,700-14,300 individuals per m2 occurred.
This resulted in caloric energy intake rates of 8
kJ/h foraging time in Vlieland and 130 kJ/h in Ghana. On
Vlieland the birds spent on average 79% of their time foraging
and in Esiama this was only 36% and most time (58
%) was spent resting (Fig. 2). We argue, however, that
during the long resting breaks on roosts, Sanderlings in
Ghana were in fact digesting and emptying their gut and
intestines from indigestable shell remains. During future
studies we plan to study annual and seasonal survival of
sanderlings wintering at different latitudes in relation to
disease risk and predation probability.
beaches and have a wide range of non-breeding locations
in different climate zones. Previous studies clearly
indicated that ambient temperatures have profound effects
on daily energy expenditures of Sanderlings. In this
study we investigated the foraging ecology of
Sanderlings on beaches near Esiama, Ghana and on the
Wadden Sea island of Vlieland, The Netherlands. The diet
was very different at the two locations. In Vlieland the
birds fed predominantly on the polychaete Scolelepis
squamata whereas a small shellfish Donax rugosus was
taken in Esiama (Fig. 4,5). The latter prey item was very
abundant in Esiama where a band of 2-14 m width containing
densities of 5,700-14,300 individuals per m2 occurred.
This resulted in caloric energy intake rates of 8
kJ/h foraging time in Vlieland and 130 kJ/h in Ghana. On
Vlieland the birds spent on average 79% of their time foraging
and in Esiama this was only 36% and most time (58
%) was spent resting (Fig. 2). We argue, however, that
during the long resting breaks on roosts, Sanderlings in
Ghana were in fact digesting and emptying their gut and
intestines from indigestable shell remains. During future
studies we plan to study annual and seasonal survival of
sanderlings wintering at different latitudes in relation to
disease risk and predation probability.
We studied time budgets of precocial chicks of American Golden-Plovers (Pluvialis dominica) on the tundra near Churchill, Manitoba, Canada, to assess how time budgets are influenced by environmental and body temperatures. Foraging time... more
We studied time budgets of precocial chicks of American Golden-Plovers (Pluvialis dominica) on the tundra near Churchill, Manitoba, Canada, to assess how time budgets
are influenced by environmental and body temperatures. Foraging time per day increased with increasing ambient temperatures and levels of solar radiation, as well as with age. This increase was due to an increase in the length of foraging bouts (i.e., the period of time in between two brooding bouts). The length of brooding bouts averaged 12 min, independent of ambient conditions or age. Body temperatures were lower under colder environmental
conditions and increased as the chicks grew older. Based on measurements of cooling rates of penned chicks, we determined that at the end of a foraging bout, body temperature never fell below 35.58C, which is high for a precocial chick. We suggest that in Churchill, American
Golden-Plover chicks are not limited in their foraging time by ambient conditions, and they can collect sufficient food in the short periods of foraging that are available to them
to sustain normal growth. By minimizing foraging bout length in favor of parental brooding, chicks may increase their digestive efficiency as well as save energy that would otherwise be expended on thermoregulation and locomotion.
are influenced by environmental and body temperatures. Foraging time per day increased with increasing ambient temperatures and levels of solar radiation, as well as with age. This increase was due to an increase in the length of foraging bouts (i.e., the period of time in between two brooding bouts). The length of brooding bouts averaged 12 min, independent of ambient conditions or age. Body temperatures were lower under colder environmental
conditions and increased as the chicks grew older. Based on measurements of cooling rates of penned chicks, we determined that at the end of a foraging bout, body temperature never fell below 35.58C, which is high for a precocial chick. We suggest that in Churchill, American
Golden-Plover chicks are not limited in their foraging time by ambient conditions, and they can collect sufficient food in the short periods of foraging that are available to them
to sustain normal growth. By minimizing foraging bout length in favor of parental brooding, chicks may increase their digestive efficiency as well as save energy that would otherwise be expended on thermoregulation and locomotion.
In captive red knots (Calidris canutus, Scolopacidae) showing a regulated body mass increase of 50% related to their migration from temperate staging sites to tundra breeding grounds, plasma corticosterone concentrations increased from... more
In captive red knots (Calidris canutus, Scolopacidae) showing a regulated body mass increase of 50% related to their migration from temperate staging sites to tundra breeding grounds, plasma corticosterone concentrations increased from less than 10 ng · ml−1 to levels as high as 30 ng · ml−1 when the energy storage for migration was complete. These birds did not fly, but concentrations dropped to very low levels (<5 ng · ml−1) as soon as the birds started their voluntary fasts to the low body masses preceding the early wing and body molts normally occurring after an unsuccessful breeding season. As the elevated levels of corticosterone are associated with stable body mass rather than with the preceding increase or subsequent decrease, it is suggested that a major role of corticosterone during the final stages just before departure may be to prepare birds for long-distance flights. Birds heading into the Arctic to breed face potentially arduous flights into unpredictable environmental and social conditions. Activation of the hypothalamic–pituitary–adrenal axis, as measured by elevated levels of corticosterone, may induce the suite of behavioral and metabolic changes necessary to negotiate these challenges successfully.
Birds daily maintain their plumage by applying waxes secreted from their uropygial gland. The preen wax coat probably keeps the feathers flexible and waterproof. Recent studies show that the chemical composition of preen wax of several... more
Birds daily maintain their plumage by applying waxes secreted from their uropygial gland. The preen wax coat probably keeps the feathers flexible and waterproof. Recent studies show that the chemical composition of preen wax of several shorebird species rapidly shifts from the usual monoester waxes to more complicated diester wax molecules in incubating individuals. In this article we present (preliminary) data of experiments performed to unravel the functional aspects of this shift.
Measurements of light reflection with a photospectrometer
showed that preen wax composition did not affect plumage coloration. Therefore, diesters probably have no function as
‘avian make-up’. We could not find evidence for an improved protection against abrasion of the wing feathers by diester wax. As incubating sandpipers create a microclimate that is
not only profitable for the hatching of eggs, but also for growth of bacteria, we are currently testing the idea that diester preen waxes offer better protection against these malicious bacteria. The data so far suggest that mono- and diester preen waxes inhibit the growth of feather-degrading bacteria equally well. During incubation sandpipers and their clutches are vulnerable to predation by especially mammalian predators. Because diesters are less volatile than monoester preen wax, they could be less easily detected by predators that use their sense of smell. A trained dog used in an
experiment indeed had more difficulty in locating diesters than monoesters, suggesting that ground-breeding birds that secrete diesters during incubation are selectively favoured
above birds that apply less olfactory cryptic monoester wax to their plumage.
Measurements of light reflection with a photospectrometer
showed that preen wax composition did not affect plumage coloration. Therefore, diesters probably have no function as
‘avian make-up’. We could not find evidence for an improved protection against abrasion of the wing feathers by diester wax. As incubating sandpipers create a microclimate that is
not only profitable for the hatching of eggs, but also for growth of bacteria, we are currently testing the idea that diester preen waxes offer better protection against these malicious bacteria. The data so far suggest that mono- and diester preen waxes inhibit the growth of feather-degrading bacteria equally well. During incubation sandpipers and their clutches are vulnerable to predation by especially mammalian predators. Because diesters are less volatile than monoester preen wax, they could be less easily detected by predators that use their sense of smell. A trained dog used in an
experiment indeed had more difficulty in locating diesters than monoesters, suggesting that ground-breeding birds that secrete diesters during incubation are selectively favoured
above birds that apply less olfactory cryptic monoester wax to their plumage.
Birds possess a preen (or uropygial) gland on their rump that secretes substances which are preened into the plumage, and which are probably essential for plumage maintenance. Secretions of the uropygial gland consist predominantly of... more
Birds possess a preen (or uropygial) gland on their rump that secretes substances which are preened into the plumage, and which are probably essential for plumage maintenance. Secretions of the uropygial gland consist predominantly
of wax-esters: fatty acids esterified to alcohols. These wax components vary in chain length and in degree and location of
branching of the carbon skeletons, resulting in complex mixtures of many different wax esters in preen gland secretions. We have found that shorebirds show pronounced seasonal changes in the composition of their preen waxes. Between arrival on and departure from breeding grounds, their usual monoester wax at winter quarters changes dramatically to a more complex diesterbased wax, which is maintained throughout the breeding season. The diesters have higher molecular weights and probably different physical properties than monoesters, and the secretion and use of diesters rather than monoesters may entail specific costs and benefits. We discuss how natural and sexual selection could explain the evolution of compositional shifts in preen waxes and outline possible approaches for future research.
of wax-esters: fatty acids esterified to alcohols. These wax components vary in chain length and in degree and location of
branching of the carbon skeletons, resulting in complex mixtures of many different wax esters in preen gland secretions. We have found that shorebirds show pronounced seasonal changes in the composition of their preen waxes. Between arrival on and departure from breeding grounds, their usual monoester wax at winter quarters changes dramatically to a more complex diesterbased wax, which is maintained throughout the breeding season. The diesters have higher molecular weights and probably different physical properties than monoesters, and the secretion and use of diesters rather than monoesters may entail specific costs and benefits. We discuss how natural and sexual selection could explain the evolution of compositional shifts in preen waxes and outline possible approaches for future research.
During the breeding season of 2008, bird populations were monitored in a 15.8 km2 area designated at Zackenberg Research Station in central Northeast Greenland. Results are presented and compared with those of previous seasons... more
During the breeding season of 2008, bird populations were monitored in a
15.8 km2 area designated at Zackenberg Research Station in central Northeast Greenland. Results are presented and compared with those of previous seasons (1995-2007). The breeding bird census revealed relatively high numbers of Sanderling (Calidris alba) and Dunlin (Calidris alpine) territories, whereas territories of Ruddy Turnstone (Arenaria interpres) were found in average numbers. However, only a few Ruddy Turnstones seemed to nest. The number of Red Knot (Calidris canutus) territories was around the average of the previous seasons. Despite the relatively late snow-melt, wader nest initiation in 2008 was average or a little later, and median first egg dates were also average in all four species. Wader nest success, however, was extremely low, and most nests suffered predation. Long-tailed Skua (Stercorarius longicaudus) territories were found in near-average numbers, and with an average median nest initiation date, but with a nest success well below average. Average numbers of Barnacle Goose (Branta leucopsis) broods were observed, and with a relatively high
mean brood size early in the season and low late in the season.
15.8 km2 area designated at Zackenberg Research Station in central Northeast Greenland. Results are presented and compared with those of previous seasons (1995-2007). The breeding bird census revealed relatively high numbers of Sanderling (Calidris alba) and Dunlin (Calidris alpine) territories, whereas territories of Ruddy Turnstone (Arenaria interpres) were found in average numbers. However, only a few Ruddy Turnstones seemed to nest. The number of Red Knot (Calidris canutus) territories was around the average of the previous seasons. Despite the relatively late snow-melt, wader nest initiation in 2008 was average or a little later, and median first egg dates were also average in all four species. Wader nest success, however, was extremely low, and most nests suffered predation. Long-tailed Skua (Stercorarius longicaudus) territories were found in near-average numbers, and with an average median nest initiation date, but with a nest success well below average. Average numbers of Barnacle Goose (Branta leucopsis) broods were observed, and with a relatively high
mean brood size early in the season and low late in the season.
Bird populations were monitored during the breeding season of 2007 in the 15.8 km2 designated bird census area at Zackenberg Research Station in central Northeast Greenland. The results are presented here and compared with the previous... more
Bird populations were monitored during the breeding season of 2007 in the
15.8 km2 designated bird census area at Zackenberg Research Station in central Northeast Greenland. The results are presented here and compared with the previous seasons 1995 to 2006. The breeding bird census revealed relatively high numbers of Sanderling Calidris alba and Dunlin Calidris alpina territories, whereas territories of Ruddy Turnstone Arenaria interpres were found in average numbers. Red Knot Calidris canutus territories were a
little above average in 2007. Long-tailed Skua Stercorarius longicaudus territories, with 15 pairs, were found in near-average numbers. Corresponding to the early snow-melt, wader nest initiation in 2007 was fairly early, and median first egg dates were before 16 June in all four species. For Ruddy Turnstone, 2007 was the earliest year in terms of median first egg dates recorded so far. Wader nest success, however, was extremely low, and most nests were depredated. The mean clutch size was 3.9. Long-tailed Skua nests were initiated early as well; average clutch size was 1.64 eggs per nest and success was just below average. High numbers
of Barnacle Goose Branta leucopsis broods were observed, but mean brood size was relatively low.
15.8 km2 designated bird census area at Zackenberg Research Station in central Northeast Greenland. The results are presented here and compared with the previous seasons 1995 to 2006. The breeding bird census revealed relatively high numbers of Sanderling Calidris alba and Dunlin Calidris alpina territories, whereas territories of Ruddy Turnstone Arenaria interpres were found in average numbers. Red Knot Calidris canutus territories were a
little above average in 2007. Long-tailed Skua Stercorarius longicaudus territories, with 15 pairs, were found in near-average numbers. Corresponding to the early snow-melt, wader nest initiation in 2007 was fairly early, and median first egg dates were before 16 June in all four species. For Ruddy Turnstone, 2007 was the earliest year in terms of median first egg dates recorded so far. Wader nest success, however, was extremely low, and most nests were depredated. The mean clutch size was 3.9. Long-tailed Skua nests were initiated early as well; average clutch size was 1.64 eggs per nest and success was just below average. High numbers
of Barnacle Goose Branta leucopsis broods were observed, but mean brood size was relatively low.