Assay optimisation and age-related baseline variation in biochemical markers in Lesser Black-backed gulls.

Free-ranging animals are often used as bioindicators of both short- and long-term changes in ecosystem health, mainly to detect the presence and effects of contaminants. Birds, and gulls in particular, have been used as bioindicators over a broad range of marine and terrestrial ecosystems. In this study, we standardise the conditions for the use of a suite of biochemical markers in non-destructive matrices of Lesser Black-backed Gull (Larus fuscus) to facilitate future biomonitoring of marine and terrestrial contaminants. We characterized cholinesterase (ChE) in plasma and optimized assay conditions for ChE activity as a marker of neurotoxic damage. Moreover, we quantified variation in activity of ChE, lactate dehydrogenase (LDH), glutathione-S-transferase (GST) and catalase (CAT) as well as variation ranges of lipid peroxidation (LPO), in free-ranging adults and captive chicks. The main ChE form present in plasma of both adults and chicks was butyrylcholinesterase (BChE) followed by acetylcholinesterase (AChE), whose relative proportion in plasma tended to decrease with increased chick age. LPO levels and GST activity in blood cells (BCs) decreased significantly with increasing chick age, while BChE and LDH activity in plasma were not age-dependent. CAT in BCs tended to decline non-significantly in older chicks. Results of this study underscore the importance of standardising assay conditions and assessing intrinsic baseline variation in biochemical markers, before biochemical quantification. Data presented here provide a foundation for future use of BChE and LDH activity in plasma, as well as oxidative stress markers (LPO, CAT and GST) in BCs, to monitor environmental stress effects in Lesser Black-backed gulls.

Simultaneous GPS-tracking of parents reveals a similar parental investment within pairs, but no immediate co-adjustment on a trip-to-trip basis.

BACKGROUND: Parental care benefits the offspring, but comes at a cost for each parent, which in biparental species gives rise to a conflict between partners regarding the within-pair distribution of care. Pair members could avoid exploitation by efficiently keeping track of each other's efforts and coordinating their efforts. Parents may, therefore, space their presence at the nest, which could also allow for permanent protection of the offspring. Additionally, they may respond to their partner's previous investment by co-adjusting their efforts on a trip-to-trip basis, resulting in overall similar parental activities within pairs. METHODS: We investigated the coordination of parental care measured as nest attendance and foraging effort in the Lesser black-backed gull (Larus fuscus), a species with long nest bouts that performs extended foraging trips out of sight of their partner. This was achieved by GPS-tracking both pair members simultaneously during the entire chick rearing period. RESULTS: We found that the timing of foraging trips (and hence nest attendance) was coordinated within gull pairs, as individuals left the colony only after their partner had returned. Parents did not match their partner's investment by actively co-adjusting their foraging efforts on a trip-by-trip basis. Yet, pair members were similar in their temporal and energetic investments during chick rearing. CONCLUSION: Balanced investment levels over a longer time frame suggest that a coordination of effort may not require permanent co-adjustment of the levels of care on a trip-to-trip basis, but may instead rather take place at an earlier stage in the reproductive attempt, or over integrated longer time intervals. Identifying the drivers and underlying processes of coordination will be one of the next necessary steps to fully understand parental cooperation in long-lived species.

Breeding habitat loss reveals limited foraging flexibility and increases foraging effort in a colonial breeding seabird.

BACKGROUND: Habitat loss can force animals to relocate to new areas, where they would need to adjust to an unfamiliar resource landscape and find new breeding sites. Relocation may be costly and could compromise reproduction. METHODS: Here, we explored how the Lesser black-backed gull (Larus fuscus), a colonial breeding seabird species with a wide ecological niche, responds to the loss of its breeding habitat. We investigated how individuals adjusted their foraging behaviour after relocating to another colony due to breeding site destruction, and whether there were any reproductive consequences in the first years after relocation. To this end, we compared offspring growth between resident individuals and individuals that recently relocated to the same colony due to breeding habitat loss. Using GPS-tracking, we further investigated the foraging behaviour of resident individuals in both colonies, as well as that of relocated individuals, as enhanced foraging effort could represent a potential driver of reproductive costs. RESULTS: We found negative consequences of relocation for offspring development, which were apparent when brood demand was experimentally increased. Recently relocated gulls travelled further distances for foraging than residents, as they often visited more distant foraging sites used by residents breeding in their natal colony as well as new areas outside the home range of the residents in the colony where they settled. CONCLUSIONS: Our results imply that relocated individuals did not yet optimally adapt to the new food landscape, which was unexpected, given the social information on foraging locations that may have been available from resident neighbours in their new breeding colony. Even though the short-term reproductive costs were comparatively low, we show that generalist species, such as the Lesser black-backed gull, may be more vulnerable to habitat loss than expected. Long term studies are needed to investigate how long individuals are affected by their relocation in order to better assess potential population effects of (breeding) habitat loss.

Mercury Uptake Affects the Development of Larus fuscus Chicks.

Current emission and mobilization rates of mercury (Hg) in the environment pose extensive threats to both wildlife and human health. Assessing the exposure risk and effects of Hg contamination in model species such as seabirds is essential to understand Hg risks at the population and ecosystem levels. The lesser black-backed gull (Larus fuscus), a generalist seabird species, is an excellent model species because it forages in both marine and terrestrial habitats, which in turn differ in their Hg exposure risk. To identify possible deleterious effects of Hg exposure on developing L. fuscus chicks, a dietary experiment was carried out and chicks were provided a marine, terrestrial, or mixed diet. The effects of embryonic and dietary Hg exposure on chick body condition and physiological state were assessed at different developmental stages until fledging age (30 d). Overall physiological condition was lower in chicks fed a predominantly marine diet, which coincided with higher Hg loads in blood and primary feathers. However, no effect of dietary uptake of Hg was observed on body condition or in terms of genotoxic damage. Body condition and genotoxic damage correlated instead with Hg exposure during embryonic development, which seems to indicate that embryonic exposure to Hg may result in carry-over effects on later chick development. Environ Toxicol Chem 2020;39:2008-2017. © 2020 SETAC.

Time and energy costs of different foraging choices in an avian generalist species.

BACKGROUND: Animals can obtain a higher foraging yield by optimizing energy expenditure or minimizing time costs. In this study, we assessed how individual variation in the relative use of marine and terrestrial foraging habitats relates to differences in the energy and time investments of an avian generalistic feeder (the Lesser Black-backed Gull, Larus fuscus), and how this changes during the course of the chick-rearing period. METHODS: We analyzed 5 years of GPS tracking data collected at the colony of Zeebrugge (Belgium). Cost proxies for energy expenditure (overall dynamic body acceleration) and time costs (trip durations and time spent away from the colony), together with trip frequency, were analyzed against the relative use of the marine and terrestrial habitats. RESULTS: The marine habitat was most often used by males and outside weekends, when fisheries are active. Marine trips implied higher energetic costs and lower time investments. As chicks became older, terrestrial trips became more prevalent, and trip frequency reached a peak towards 20 days after hatching of the first egg. Over a full chick rearing period, energy costs varied widely between individuals, but no trends were found across the marine foraging gradient. Conversely, a higher use of marine foraging implied lower overall amounts of time spent away from the colony. CONCLUSIONS: Foraging habitat choice was related to overall time costs incurred by gulls, but not to energy costs. The effect of chick age on foraging habitat choice and effort may be driven by energy expenditure constraints on the amount of marine foraging that can be performed. If time is less constraining to them, Lesser Black-backed Gulls may meet the increasing chick demand for food by switching from high to low energy demanding foraging strategies.

Recently-adopted foraging strategies constrain early chick development in a coastal breeding gull.

Human-mediated food sources offer possibilities for novel foraging strategies by opportunistic species. Yet, relative costs and benefits of alternative foraging strategies vary with the abundance, accessibility, predictability and nutritional value of anthropogenic food sources. The extent to which such strategies may ultimately alter fitness, can have important consequences for long-term population dynamics. Here, we studied the relationships between parental diet and early development in free-ranging, cross-fostered chicks and in captive-held, hand-raised chicks of Lesser Black-backed Gulls (Larus fuscus) breeding along the Belgian coast. This traditionally marine and intertidal foraging species is now increasingly taking advantage of human activities by foraging on terrestrial food sources in agricultural and urban environments. In accordance with such behavior, the proportion of terrestrial food in the diet of free-ranging chicks ranged between 4% and 80%, and consistent stable isotope signatures between age classes indicated that this variation was mainly due to between-parent variation in feeding strategies. A stronger terrestrial food signature in free-ranging chicks corresponded with slower chick development. However, no consistent differences in chick development were found when contrasting terrestrial and marine diets were provided ad libitum to hand-raised chicks. Results of this study hence suggest that terrestrial diets may lower reproductive success due to limitations in food quantity, rather than quality. Recent foraging niche expansion toward terrestrial resources may thus constitute a suboptimal alternative strategy to marine foraging for breeding Lesser Black-backed Gulls during the chick-rearing period.

High-resolution GPS tracking reveals sex differences in migratory behaviour and stopover habitat use in the Lesser Black-backed Gull Larus fuscus.

Sex-, size- or age-dependent variation in migration strategies in birds is generally expected to reflect differences in competitive abilities. Theoretical and empirical studies thereby focus on differences in wintering areas, by which individuals may benefit from avoiding food competition during winter or ensuring an early return and access to prime nesting sites in spring. Here, we use GPS tracking to assess sex- and size-related variation in the spatial behaviour of adult Lesser Black-backed Gulls (Larus fuscus) throughout their annual cycle. We did not find sex- or size-dependent differences in wintering area or the timing of spring migration. Instead, sexual differences occurred prior to, and during, autumn migration, when females strongly focussed on agricultural areas. Females exhibited a more protracted autumn migration strategy, hence spent more time on stopover sites and arrived 15 days later at their wintering areas, than males. This shift in habitat use and protracted autumn migration coincided with the timing of moult, which overlaps with chick rearing and migration. Our results suggest that this overlap between energy-demanding activities may lead females to perform a more prolonged autumn migration, which results in spatiotemporal differences in foraging habitat use between the sexes.

Long-term monitoring study of beached seabirds shows that chronic oil pollution in the southern North Sea has almost halted.

Trends in oil rates of beached seabirds reflect temporal and spatial patterns in chronic oil pollution at sea. We analysed a long-term dataset of systematic beached bird surveys along the Belgian North Sea coast during 1962-2015, where extreme high oil contamination rates and consequently high mortality rates of seabirds during the 1960s used to coincide with intensive ship traffic. In the 1960s, >90% of all swimming seabirds that washed ashore were contaminated with oil and estimated oil-induced mortality of seabirds was probably several times higher than natural mortality. More than 50years later oil rates of seabirds have dropped to historically low levels while shipping is still very intense, indicating that chronic oil pollution has significantly declined. The declining trend is discussed in the light of a series of legislative measures that were enacted in the North Sea region to reduce oil pollution.

Offspring Hg exposure relates to parental feeding strategies in a generalist bird with strong individual foraging specialization.

Generalist species can potentially exploit a wide variety of resources, but at the individual level they often show a certain degree of foraging specialization. Specific foraging strategies, however, may increase exposure to environmental contaminants that can alter the cost-benefit balance of consuming particular food items. The Lesser Black-backed Gull (Larus fuscus) is known to opportunistically feed on a wide range of marine and terrestrial prey that differ in contaminant load, such as mercury (Hg) that strongly biomagnifies through the aquatic food web. The hypothesis tested in this study were: i) a predominant use of marine prey by females during egg-formation and by both parents during chick rearing increases the exposure to Hg during embryonic development and chick growth, and ii) this affects parental investment in clutch volume, chick growth and body condition. Total Hg burden and isotopic signatures of carbon (δ13C) and nitrogen (δ15N) were determined for eggs, down feathers, and primary feathers of L. fuscus chicks collected at a coastal colony in Belgium. As expected, eggs and feathers of chicks from parents with a stable isotope signature that suggested a predominantly marine diet had higher levels of Hg. The use of marine resources by females during the egg-formation period positively correlated to maternal investment in egg size, though entailing the cost of increased Hg-concentrations which in turn negatively affected clutch volume. Furthermore, it is shown that the use of chick down feathers is a suitable matrix to non-lethally estimate Hg concentrations in eggs. Contrary to our expectations, no relationship between Hg exposure and chick growth or chick body condition was found, which may be due the low concentrations found. We conclude that currently Hg contamination does not constitute a risk for development and condition of L. fuscus offspring at the levels currently observed at the Belgian coast.

GPS tracking data of Lesser Black-backed Gulls and Herring Gulls breeding at the southern North Sea coast.

In this data paper, Bird tracking - GPS tracking of Lesser Black-backed Gulls and Herring Gulls breeding at the southern North Sea coast is described, a species occurrence dataset published by the Research Institute for Nature and Forest (INBO). The dataset (version 5.5) contains close to 2.5 million occurrences, recorded by 101 GPS trackers mounted on 75 Lesser Black-backed Gulls and 26 Herring Gulls breeding at the Belgian and Dutch coast. The trackers were developed by the University of Amsterdam Bird Tracking System (UvA-BiTS, http://www.uva-bits.nl). These automatically record and transmit bird movements, which allows us and others to study their habitat use and migration behaviour in great detail. Our bird tracking network is operational since 2013. It is funded for LifeWatch by the Hercules Foundation and maintained in collaboration with UvA-BiTS and the Flanders Marine Institute (VLIZ). The recorded data are periodically released in bulk as open data (http://dataset.inbo.be/bird-tracking-gull-occurrences), and are also accessible through CartoDB and the Global Biodiversity Information Facility (GBIF).

Age of first breeding interacts with pre- and post-recruitment experience in shaping breeding phenology in a long-lived gull.

Individual variation in timing of breeding is a key factor affecting adaptation to environmental change, yet our basic understanding of the causes of such individual variation is incomplete. This study tests several hypotheses for age-related variation in the breeding timing of Lesser Black-backed Gulls, based on a 13 year longitudinal data set that allows to decouple effects of age, previous prospecting behavior, and years of breeding experience on arrival timing at the colony. At the population level, age of first breeding was significantly associated with timing of arrival and survival, i.e. individuals tended to arrive later if they postponed their recruitment, and individuals recruiting at the age of 4 years survived best. However, up to 81% of the temporal variation in arrival dates was explained by within-individual effects. When excluding the pre-recruitment period, the effect of increasing age on advanced arrival was estimated at 11 days, with prior breeding experience accounting for a 7 days advance and postponed breeding for a 4 days delay. Overall, results of this study show that delayed age of first breeding can serve to advance arrival date (days after December 1(st)) in successive breeding seasons throughout an individual's lifetime, in large part due to the benefits of learning or experience gained during prospecting. However, prospecting and the associated delay in breeding also bear a survival cost, possibly because prospectors have been forced to delay through competition with breeders. More generally, results of this study set the stage for exploring integrated temporal shifts in phenology, resource allocation and reproductive strategies during individual lifecycles of long-lived migratory species.

Monitoring plastic ingestion by the northern fulmar Fulmarus glacialis in the North Sea.

The abundance of plastics in stomachs of northern fulmars from the North Sea is used in the OSPAR Ecological Quality Objective (EcoQO) for marine litter. The preliminary EcoQO defines acceptable ecological quality as the situation where no more than 10% of fulmars exceed a critical level of 0.1 g of plastic in the stomach. During 2003-2007, 95% of 1295 fulmars sampled in the North Sea had plastic in the stomach (on average 35 pieces weighing 0.31 g) and the critical level of 0.1 g of plastic was exceeded by 58% of birds, with regional variations ranging from 48 to 78%. Long term data for the Netherlands since the 1980s show a decrease of industrial, but an increase of user plastics, with shipping and fisheries as the main sources. The EcoQO is now also used as an indicator for Good Environmental Status in the European Marine Strategy Framework Directive.