Using eggshell membranes as a DNA source for population genetic research

In the context of population genetic research, a faster and less invasive method of DNA sampling would allow large-scale assessments of genetic diversity and genetic differentiation with the help of volunteer observers. The aim of this study was to investigate the usefulness of eggshell membranes as a DNA source for population genetic research, by addressing eggshell membrane DNA quality, degeneration and cross-contamination. To this end, a comparison was made with blood-derived DNA samples. We have demonstrated 100% successful DNA extraction from post-hatched Black-tailed Godwit (Limosa limosa) eggshell membranes as well as from blood samples. Using 11 microsatellite loci, DNA amplification success was 99.1% for eggshell membranes and 97.7% for blood samples. Genetic information within eggshell membrane DNA in comparison to blood DNA was not affected (F-ST = -0.01735, P = 0.999) by degeneration or possible cross-contamination. Furthermore, neither degeneration nor cross-contamination was apparent in total genotypic comparison of eggshell membrane DNA and blood sample DNA. Our research clearly illustrates that eggshell membranes can be used for population genetic research

Distance doesn't matter: migration strategy in a seabird has no effect on survival or reproduction

Migrating animals show remarkable diversity in migration strategies, even between individuals from the same population. Migrating longer distances is usually expected to be costlier in terms of time, energy expenditure and risks with potential repercussions for subsequent stages within the annual cycle. Such costs are expected to be balanced by increased survival, for example due to higher quality wintering areas or lower energy expenditure at lower latitudes. We compared reproductive parameters and apparent survival of lesser black-backed gulls (Larus fuscus) breeding in The Netherlands, whose winter range extends from the UK to West Africa, resulting in one-way migration distances that differ by more than 4500 km. Individuals migrating furthest arrived later in the colony than shorter distance migrants, but still laid in synchrony with the colony and consequently had a shorter pre-laying period. This shorter pre-laying period affected neither egg volumes nor hatching success. We found no relationship between migration distance and apparent survival probability, corresponding with previous research showing that annual energy expenditure and distance travelled throughout the year is similar across migration strategies. Combined, our results indicate an equal fitness payoff across migration strategies, suggesting there is no strong selective pressure acting on migration strategy within this population

Does wintering north or south of the Sahara correlate with timing and breeding performance in black-tailed godwits?

Migrating long distances requires time and energy, and may interact with an individual’s performance during breeding. These seasonal interactions in migratory animals are best described in populations with disjunct nonbreeding distributions. The black-tailed godwit (Limosa limosa limosa), which breeds in agricultural grasslands in Western Europe, has such a disjunct nonbreeding distribution: The majority spend the nonbreeding season in West Africa, while a growing number winters north of the Sahara on the Iberian Peninsula. To test whether crossing the Sahara has an effect on breeding season phenology and reproductive parameters, we examined differences in the timing of arrival, breeding habitat quality, lay date, egg volume, and daily nest survival among godwits (154 females and 157 males), individually marked in a breeding area in the Netherlands for which wintering destination was known on the basis of resightings. We also examined whether individual repeatability in arrival date differed between birds wintering north or south of the Sahara. Contrary to expectation, godwits wintering south of the Sahara arrived two days earlier and initiated their clutch six days earlier than godwits wintering north of the Sahara. Arrival date was equally repeatable for both groups, and egg volume larger in birds wintering north of the Sahara. Despite these differences, we found no association between wintering location and the quality of breeding habitat or nest survival. This suggests that the crossing of an important ecological barrier and doubling of the migration distance, twice a year, do not have clear negative reproductive consequences for some long-distance migrants.Peer reviewe

High Migratory Survival and Highly Variable Migratory Behavior in Black-Tailed Godwits

Few studies have been able to directly measure the seasonal survival rates of migratory species or determine how variable the timing of migration is within individuals and across populations over multiple years. As such, it remains unclear how likely migration is to affect the population dynamics of migratory species and how capable migrants may be of responding to changing environmental conditions within their lifetimes. To address these questions, we used three types of tracking devices to track individual black-tailed godwits from the nominate subspecies (Limosa limosa limosa) throughout their annual cycles for up to 5 consecutive years. We found that godwits exhibit considerable inter- and intra-individual variation in their migratory behavior across years. We also found that godwits had generally high survival rates during migration, although survival was reduced during northward flights across the Sahara Desert. These patterns differ from those observed in most other migratory species, suggesting that migration may only be truly dangerous when crossing geographic barriers that lack emergency stopover sites and that the levels of phenotypic flexibility exhibited by some populations may enable them to rapidly respond to changing environmental conditions

Variation in egg size of Black-tailed Godwits

As is the case for most avian species, there is considerable variation in the egg size of Continental Black-tailed Godwits Limosa l. limosa breeding in The Netherlands. It is interesting that egg size has costs and benefits yet varies considerably at the population level. To better understand this variation in egg size, we tested its relationship to a suite of individual and environmental factors. We found that egg size can decrease up to 2.8% throughout a breeding season and that egg size increases with clutch size by 1.4% with each additional egg in the clutch. Female body mass and body size explained 5% of the total variation in egg size observed across the population. Furthermore, females wintering south of the Sahara laid 3% smaller eggs than those wintering north of the Sahara. We also found that egg size increases with age, which may indicate age-related differences in the endogenous and/or exogenous conditions of females. The variation in egg size was, however, mostly the result of consistent differences among individuals across years (repeatability = 0.60). A comparison of daughters with mothers suggested that most of this individual repeatability reflects heritable variation (heritability = 0.64). The actual individual traits that underlie this heritable variation among individuals remain mostly undetermined. Smaller eggs did have a slightly lower chance of hatching, but we found no relationship between egg size and chick survival. Finally, nest and chick survival were strongly correlated with lay date. Thus, in Black-tailed Godwits, lay date may actually reflect a female's endogenous and/or exogenous condition at the moment of egg-laying. This finding may be general across birds, since food supplementation experiments usually result in advanced laying and larger clutch sizes rather than in larger eggs

Warming springs and habitat alteration interact to impact timing of breeding and population dynamics in a migratory bird

In seasonal environments, increasing spring temperatures lead many taxa to advance the timing of reproduction. Species that do not may suffer lower fitness. We investigated why black-tailed godwits (Limosa limosa limosa), a ground-breeding agricultural grassland shorebird, have not advanced timing of reproduction during the last three decades in the face of climate change and human-induced habitat degradation. We used data from an 11-year field study to parameterize an Integral Projection Model to predict how spring temperature and habitat quality simultaneously influence the timing of reproduction and population dynamics. We found apparent selection for earlier laying, but not a correlation between the laying dates of parents and their offspring. Nevertheless, in warmer springs, laying dates of adults show a stronger positive correlation with laying date in previous springs than in cooler ones, and this leads us to predict a slight advance in the timing of reproduction if spring temperatures continue to increase. We also show that only in landscapes with low agricultural activity, the population can continue to act as a source. This study shows how climate change and declining habitat quality may enhance extinction risk

Geolocators lead to better measures of timing and renesting in black-tailed godwits and reveal the bias of traditional observational methods

Long-term population studies can identify changes in population dynamics over time. However, to realize meaningful conclusions, these studies rely on accurate measurements of individual traits and population characteristics. Here, we evaluate the accuracy of the observational methods used to measure reproductive traits in individually marked black-tailed godwits (Limosa limosa limosa). By comparing estimates from traditional methods with data obtained from light-level geolocators, we provide an accurate estimate of the likelihood of renesting in godwits and the repeatability of the lay dates of first clutches. From 2012 to 2018, we used periods of shading recorded on the light-level geolocators carried by 68 individual godwits to document their nesting behaviour. We then compared these estimates to those simultaneously obtained by our long-term observational study. We found that among recaptured geolocator-carrying godwits, all birds renested after a failed first clutch, regardless of the date of nest loss or the number of days already spent incubating. We also found that 43% of these godwits laid a second replacement clutch after a failed first replacement, and that 21% of these godwits renested after a hatched first clutch. However, the observational study correctly identified only 3% of the replacement clutches produced by geolocator-carrying individuals and designated as first clutches a number of nests that were actually replacement clutches. Additionally, on the basis of the observational study, the repeatability of lay date was 0.24 (95% CI 0.17-0.31), whereas it was 0.54 (95% CI 0.28-0.75) using geolocator-carrying individuals. We use examples from our own and other godwit studies to illustrate how the biases in our observational study discovered here may have affected the outcome of demographic estimates, individual-level comparisons, and the design, implementation and evaluation of conservation practices. These examples emphasize the importance of improving and validating field methodologies and show how the addition of new tools can be transformational

Patterns and processes in shorebird survival rates: a global review

Changes in demographic rates underpin changes in population size, and understanding demographic rates can greatly aid the design and development of strategies to maintain populations in the face of environmental changes. However, acquiring estimates of demographic parameters at relevant spatial scales is difficult. Measures of annual survival rates can be particularly challenging to obtain because large-scale, long-term tracking of individuals is difficult and the resulting data contain many inherent biases. In recent years, advances in both tracking and analytical techniques have meant that, for some taxonomic groups, sufficient numbers of survival estimates are available to allow variation within and among species to be explored. Here we review published estimates of annual adult survival rates in shorebird species across the globe, and construct models to explore the phylogenetic, geographical, seasonal and sex-based variation in survival rates. Models of 295 survival estimates from 56 species show that survival rates calculated from recoveries of dead individuals or from return rates of marked individuals are significantly lower than estimates from mark–recapture models. Survival rates also vary across flyways, largely as a consequence of differences in the genera that have been studied and the analytical methods used, with published estimates from the Americas and from smaller shorebirds (Actitis, Calidris and Charadrius spp.) tending to be underestimated. By incorporating the analytical method used to generate each estimate within a mixed model framework, we provide method-corrected species-specific and genus-specific adult annual survival estimates for 52 species of 15 genera