Molecular characterization of European Pygorchis Looss, 1899.

Adult trematodes of the genus Pygorchis Looss, 1899 (Trematoda: Philophthalmidae) parasitize the cloaca of birds. The genus contains three species, all of which are rarely reported and molecular phylogenetics of which have not been applied. The absence of reference DNA sequences limit studies of their indistinct larval forms. Based on the materials that were obtained from birds of the Czech origin, we performed a molecular characterization of both currently known Pygorchis spp., which are known from the Palearctic, the type species Pygorchis affixus Looss, 1899 and Pygorchis alakolensis Zhatkanbaeva, 1967, and provided morphological description of the examined P. alakolensis specimen. We found that the two species were of similar dimensions; the only difference was in the position of testes and in the extent of vitelline follicles. However, the position of testes in P. affixus was variable, and approximately 10% of examined P. affixus individuals had testes positioned obliquely. The second feature that allows differential diagnostic, the extent of vitelline follicles, was more reproducible as the vitelline follicles of P. affixus did not extend beyond the intestinal caeca, or, in exceptional cases, they extended them at only one side. In the examined P. alakolensis individual, the testes were positioned obliquely, and the vitelline follicles extended beyond the intestinal caeca. We reported P. alakolensis for the first time from Europe; previously, it was known only from Central Asian lakes and rivers. We confirmed the classification of Pygorchis into Philophtalmidae.

Understanding the Social Dynamics of Breeding Phenology: Indirect Genetic Effects and Assortative Mating in a Long-Distance Migrant.

AbstractPhenological traits, such as the timing of reproduction, are often influenced by social interactions between paired individuals. Such partner effects may occur when pair members affect each other's prebreeding environment. Partner effects can be environmentally and/or genetically determined, and quantifying direct and indirect genetic effects is important for understanding the evolutionary dynamics of phenological traits. Here, using 26 years of data from a pedigreed population of a migratory seabird, the common tern (Sterna hirundo), we investigate male and female effects on female laying date. We find that female laying date harbors both genetic and environmental variation and is additionally influenced by the environmental and, to a lesser extent, genetic component of its mate. We demonstrate this partner effect to be largely explained by male arrival date. Interestingly, analyses of mating patterns with respect to arrival date show mating to be strongly assortative, and using simulations we show that assortative mating leads to overestimation of partner effects. Our study provides evidence for partner effects on breeding phenology in a long-distance migrant while uncovering the potential causal pathways underlying the observed effects and raising awareness for confounding effects resulting from assortative mating or other common environmental effects.

Contrasting heterozygosity-fitness correlations across life in a long-lived seabird.

Selection is a central force underlying evolutionary change and can vary in strength and direction, for example across time and space. The fitness consequences of individual genetic diversity have often been investigated by testing for multilocus heterozygosity-fitness correlations (HFCs), but few studies have been able to assess HFCs across life stages and in both sexes. Here, we test for HFCs using a 26-year longitudinal individual-based data set from a large population of a long-lived seabird (the common tern, Sterna hirundo), where 7,974 chicks and breeders of known age were genotyped at 15 microsatellite loci and sampled for life-history traits over the complete life cycle. Heterozygosity was not correlated with fledging or post-fledging prospecting probabilities, but was positively correlated with recruitment probability. For breeders, annual survival was not correlated with heterozygosity, but annual fledgling production was negatively correlated with heterozygosity in males and highest in intermediately heterozygous females. The contrasting HFCs among life stages and sexes indicate differential selective processes and emphasize the importance of assessing fitness consequences of traits over complete life histories.

Colony size affects nestling immune function: a cross-fostering experiment in a colonial waterbird.

Elevated transmission rate of pathogens and parasites is considered one of the major costs of sociality in birds. However, greater risk of infection in colonial birds might be compensated by specific immune adaptations. Here, we predicted that nestlings raised in larger colonies should invest more in their immune function. To test this hypothesis, we manipulated colony size and conduced cross-fostering experiment in a colonial waterbird, the common tern Sterna hirundo. Establishment of different size colonies under uniform environmental conditions was induced by providing large and small patches of attractive nesting area for terns (floating rafts). Then, pairs of clutches were swapped between large and small tern colonies, and skin-swelling response to phytohaemagglutinin (PHA) was assessed for nestlings from experimental and control broods. Contrary to our expectations, we found a negative effect of foster colony size on nestling PHA response (nestlings raised in the larger colony had lower PHA response). In addition, nestling PHA response correlated negatively with heterophil/lymphocyte ratio used as a measure of physiological stress. This suggested that low PHA response of nestlings raised in the larger colony could be mediated by an elevated level of social stress. We suggest that depression of immune function via social stress may constitute a strong selective pressure against large colony size in the common tern, and possibly in other colonial species. We also recommend that this largely overlooked cost of sociality should be considered in the further studies on the evolution and ecology of avian coloniality.

Reduced telomere length in offspring of old fathers in a long-lived seabird.

Evidence for transgenerational effects of senescence, whereby offspring from older parents have a reduced lifetime reproductive success, is increasing. Such effects could arise from compromised germline maintenance in old parents, potentially reflected in reduced telomere length in their offspring. We test the relationship between parental age and offspring early-life telomere length in a natural population of common terns and find a significant negative correlation between paternal age and offspring telomere length. Offspring telomere length is reduced by 35 base pairs for each additional year of paternal age. We find no correlation with maternal age. These results fit with the idea of compromised germline maintenance in males, whose germline stem cells require continued division.

Immigrants are attracted by local pre-breeders and recruits in a seabird colony.

Immigration is a major demographic factor shaping population dynamics. However, due to methodological difficulties, the extent of immigration and factors affecting immigration are insufficiently studied. This is also true for seabird colonies. We estimated annual immigration based on a long-term study of a colony of common terns Sterna hirundo marked with transponders, using a Bayesian integrated population model that links colony size and productivity with individual life histories. Strong annual fluctuations in the number of immigrants were found. To identify whether colony-specific covariates influenced immigration, we related the number of immigrants to various proxy variables for breeding site quality, specifically colony size, productivity, number of local subadults and local recruits. Numbers of local recruits and local subadults showed strong positive correlations with number of immigrants. We found that variation in immigration rate had strongly contributed to variation in colony growth rate, more so than variation in local recruitment or adult survival. Collectively, results suggest that immigration strongly affects colony growth rate, that the driving force behind immigration is natal dispersal and that immigrants were attracted by local recruits.

Low heritability of social phenotypes in a nonpasserine waterbird.

Most behavioral traits are known to be weakly heritable, possibly due to their extreme complexity and flexibility. Despite this general pattern, within-species variation in avian colony size choice has been reported to have a strong additive genetic component, but we are aware of no attempts to assess the heritability of avian sociality at the finer spatial scale. Here, we used an animal model and parent-offspring regression to quantify additive genetic variance in social phenotype (local nesting density) in a nonpasserine waterbird, the common tern Sterna hirundo. For this purpose, we used a novel experimental framework, where variation in the social environment was generated by providing birds with artificial patches of attractive nesting substrate that markedly varied in size. During 2011-2019, we collected data on social preferences for either low or high nesting density in over 250 individuals, either kin (mostly parent-offspring relationships) or non-kin recorded breeding multiple times across years. All heritability estimates of local nesting density were low (<0.10), irrespectively of fixed effects (sex and year) included in the models, data used in the modeling (all individuals vs. early recruits), or methodological approach (animal model vs. parent-offspring regression). We conclude that avian sociality, as measured at the local scale, may be much less heritable than colony size choice, as measured at the landscape level. Our study adds to the understanding of additive genetic variance in avian behavior, and it underlines a scale dependency in the heritability of behavioral traits.

Mercury bioaccumulation in three colonial seabird species in the Gulf of Maine.

The methylated form of mercury, MeHg, is a neurotoxin that bioaccumulates and biomagnifies through aquatic food webs, reaching high concentrations in top trophic species. Many seabird species are wide-ranging and feed on forage fish, so they can be used as sentinel species to assess the level of mercury in pelagic or coastal food webs because they integrate the signal from large areas and from lower trophic levels. The Gulf of Maine provides habitat for many seabirds, including endangered roseate terns (Sterna dougalii), common terns (Sterna hirundo), and the southernmost breeding population of black guillemots (Cepphus grylle). Hg levels were assessed in down of newly hatched chicks of three seabird species to determine pre-hatching Hg exposure. Stable isotopes (δ15N, δ13C) in down and chick contour feathers grown after hatching were used as indicators of adult female diet in the period before laying the egg (down) and pre-fledging chick diet (contour feathers). Black guillemot down THg concentrations were 10.07 ± 2.88 µg/g (mean ± 1SD), 5.5× higher than common tern down (1.82 ± 0.436 µg /g), and 7.4× higher than roseate tern down (1.37 ± 0.518 µg/g). Black guillemots also had higher down feather δ15N values (15.1 ± 0.52 ‰) compared to common (13.0 ± 0.72 ‰) or roseate terns (12.8 ± 0.25 ‰), and in black guillemot down feathers, higher Hg concentrations were correlated with δ15N, an indicator of trophic level. Repeated testing of the same tissue types across multiple years is needed to monitor THg exposure for seabirds in the Gulf of Maine; additionally, monitoring species composition and Hg presence in prey species of the black guillemot population would help to determine the source of high THg concentrations in this species.

Micro-evolutionary response of spring migration timing in a wild seabird.

In the context of rapid climate change, phenological advance is a key adaptation for which evidence is accumulating across taxa. Among vertebrates, phenotypic plasticity is known to underlie most of this phenological change, while evidence for micro-evolution is very limited and challenging to obtain. In this study, we quantified phenotypic and genetic trends in timing of spring migration using 8,032 dates of arrival at the breeding grounds obtained from observations on 1,715 individual common terns (Sterna hirundo) monitored across 27 years, and tested whether these trends were consistent with predictions of a micro-evolutionary response to selection. We observed a strong phenotypic advance of 9.3 days in arrival date, of which c. 5% was accounted for by an advance in breeding values. The Breeder's equation and Robertson's Secondary Theorem of Selection predicted qualitatively similar evolutionary responses to selection, and these theoretical predictions were largely consistent with our estimated genetic pattern. Overall, our study provides rare evidence for micro-evolution underlying (part of) an adaptive response to climate change in the wild, and illustrates how a combination of adaptive micro-evolution and phenotypic plasticity facilitated a shift towards earlier spring migration in this free-living population of common terns.

First Description of Mergibacter septicus Isolated from a Common Tern (Sterna hirundo) in Germany.

Mergibacter septicus (M. septicus), previously known as Bisgaard Taxon 40, is a recently described species within the Pasteurellaceae family. In this study, we present a M. septicus strain isolated from a common tern (Sterna hirundo) chick that died just after fledging from the Banter See in Wilhelmshaven, Germany. The recovered M. septicus strain underwent microbiological phenotypic characterization, followed by whole genome sequencing on Illumina and Nanopore platforms. Phenotypically, M. septicus 19Y0039 demonstrated resistance to colistin, cephalexin, clindamycin, oxacillin, and penicillin G. The genome analysis revealed a circular 1.8 Mbp chromosome without any extrachromosomal elements, containing 1690 coding DNA sequences. The majority of these coding genes were associated with translation, ribosomal structure and biogenesis, followed by RNA processing and modification, and transcription. Genetic analyses revealed that the German M. septicus strain 19Y0039 is related to the American strain M. septicus A25201T. Through BLAST alignment, twelve putative virulence genes previously identified in the M. septicus type strain A25201T were also found in the German strain. Additionally, 84 putative virulence genes distributed across nine categories, including immune modulation, effector delivery system, nutrition/metabolic factors, regulation, stress survival, adherence, biofilm, exotoxin, and motility, were also identified.

Distributing transmitters to maximize population-level representativeness in automated radio telemetry studies of animal movement.

Telemetry is a powerful and indispensable tool for evaluating wildlife movement and distribution patterns, particularly in systems where opportunities for direct observation are limited. However, the effort and expense required to track individuals often results in small sample sizes, which can lead to biased results if the sample of tracked individuals does not fully capture spatial, temporal, and individual variability within the target population. To better understand the influence of sampling design on results of automated radio telemetry studies, we conducted a retrospective power analysis of very high frequency (VHF) radio telemetry data from the Motus Wildlife Tracking System for two species of birds along the United States Atlantic coast: a shorebird, the piping plover (Charadrius melodus), and a nearshore seabird, the common tern (Sterna hirundo). We found that ~ 100-150 tracked individuals were required to identify 90% of locations known to be used by the tracked population, with 40-50 additional individuals required to include 95% of used locations. For any number of individuals, the percentage of stations included in the sample was higher for common terns than for piping plovers when tags were deployed within a single site and year. Percentages of stations included increased for piping plovers when birds were tagged over multiple sites and, to a lesser extent, years, and increased with average length of the tracking period. The probability that any given receiver station used by the population would be included in a subsample increased with the number of birds tracked, station proximity to a migratory stopover or staging site, number of receiving antennas per station, and percentage of the tracked population present. Our results provide general guidance for the number and distribution of tagged birds required to obtain representative VHF telemetry data, while also highlighting the importance of accounting for station network configuration and species-specific differences in behavior when designing automated radio telemetry studies to address specific research questions. Our results have broad applications to remotely track movements of small-bodied migratory wildlife in inaccessible habitats, including predicting and monitoring effects of offshore wind energy development.

Incidence of microplastic fiber ingestion by Common Terns (Sterna hirundo) and Roseate Terns (S. dougallii) breeding in the Northwestern Atlantic.

Ingestion of microplastics has been documented across marine species, but exposure remains sparsely described in many seabird species. We assess microplastic (between 0.2 and 5.0 mm) ingestion in two Northwestern Atantic - breeding species for which exposure to microplastics is entirely or largely undescribed: Common Terns (Sterna hirundo) and Roseate Terns (S. dougallii). Common Tern microplastic load did not vary between life stages (p = 0.590); microplastic load did differ in Common Tern adults breeding at two of three colonies explored (p = 0.002), with no other regional differences observed. Roseate Terns ingested significantly more microplastics than Common Terns (p = 0.007). Our results show that microplastic ingestion by terns varies regionally and interspecifically, but not by life stage, trends potentially explained by dietary differences. We provide the first quantification of microplastic fiber ingestion by terns in the Northwestern Atlantic and identify trophic dynamics related to microplastic ingestion, representing an important step toward understanding the risk of the pollutant to terns across regions, as well as toward the use of terns as potential bioindicators of microplastics.

Evolution of innate and adaptive immune genes in a non-model waterbird, the common tern.

Toll-like receptors (TLRs) and the Major Histocompatibility Complex (MHC) are the key pathogen-recognition genes of vertebrate immune system and they have a crucial role in the initiation of innate and adaptive immune response, respectively. Recent advancements in sequencing technology sparked research on highly duplicated MHC genes in non-model species, but TLR variation in natural vertebrate populations has remained little studied and comparisons of polymorphism across both TLRs and MHC are scarce. Here, we aimed to compare variation across innate (four TLR loci) and adaptive (MHC class I and class II) immune genes in a non-model avian species, the common tern Sterna hirundo. We detected relatively high allelic richness at TLR genes (9-48 alleles per locus), which was similar to or even higher than the estimated per locus allelic richness at the MHC (24-30 alleles at class I and 13-16 alleles at class II under uniform sample sizes). Despite this, the total number of MHC alleles across all duplicated loci (four class I and three class II) was much higher and MHC alleles showed greater sequence divergence than TLRs. Positive selection targeted relatively more sites at the MHC than TLRs, but the strength of selection (dN/dS ratios) at TLRs was higher when compared to MHC class I. There were also differences in the signature of positive selection and recombination (gene conversion) between MHC class I and II (stronger signature at class II), suggesting that mechanisms maintaining variation at the MHC may vary between both classes. Our study indicates that allelic richness of both innate and adaptive immune receptors may be maintained at relatively high levels in viable avian populations and we recommend a transition from the traditional gene-specific to multi-gene approach in studying molecular evolution of vertebrate immune system.

Presence of persistent organic pollutants in a breeding common tern (Sterna hirundo) population in Ireland.

Persistent organic pollutants (POPs) are chemical compounds of environmental concern due to their toxic, persistent nature and their ability to bio-accumulate in biological tissue. Seabirds, for often being at the top of the food web, have been used as monitors of environmental pollutants. Adverse effects caused by POPs have been reported in common terns (Sterna hirundo) since the 1970s. Egg shell thinning, embryo and hatchling deformities have been reported for this species. Environmental legislation, such as the Oslo-Paris Convention (OSPAR), has agreed on the monitoring of concentration of POPs in common terns. This study set out to investigate contemporary concentrations of polychlorinated biphenyls (PCBs), polycyclic aromatic hydrocarbons (PAHs), organochlorine pesticides (OCPs) and brominated flame retardants (BFRs) in common terns breeding in Ireland, along with congener profiles. Investigation was conducted in live (n = 15) and dead birds (n = 20) to test for the efficiency of different methodologies using preen oil and feathers versus liver and preen gland. Mean concentrations of POPs followed the order: PCB (36.48 ng/g ww feather) > PAH (30.01 ng/g ww feather) > OCP (13.36 ng/g ww feather) > BFR (1.98 ng/g ww feather) in live birds; and PAH (46.65 ng/g ww preen gland) > PCB (44.11 ng/g ww preen gland) > OCP (15.15 ng/g ww liver) > BFR (5.07 ng/g ww liver) in dead birds. Comparison of contaminant results with toxicity pre-established levels concluded that this population of common terns in Ireland is not at risk of anomalies caused by POPs. However, some levels are higher in comparison to the ones established by OSPAR's EcoQO and must be monitored periodically.

Age-related differences in nest defense in common terns: Relationship to other life-history parameters.

The Common Tern (Sterno hirundo) is a long-lived colonial nesting seabird. Previous studies have shown that chick growth and fledging success vary with age of the parental pair and with laying date, with older parents and those nesting earlier being more successful. This study investigated the dependence of breeding performance and one aspect of behavior, defense against conspecifics, on age and laying date. Nest defense behavior was evaluated by recording individual responses to a mirror placed 20 cm from the nest, simulating an unfamiliar intruder within the territory. Most study birds were of known age (3-21 years) from banding as chicks; they were divided into three groups: ≥12, 8-11 and ≤seven years. Responses to the mirror were examined during incubation and at the time of hatching. Older birds nested earlier than younger birds. Chicks reared by older parents gained mass more quickly and survived better than chicks of younger parents. Using a composite score reflecting both the intensity and duration of aggressive responses to the mirror, older birds responded more strongly than younger birds during incubation, but responses were similar at the time of hatching. Older birds reduced their aggressive responses between incubation and hatching, while younger birds increased their responses. We suggest that this contributes to the greater success of older birds, because younger birds expend more time and energy on territorial defense at a time when they need to feed chicks. Our findings are consistent with previous studies and show that Common Tern colonies are finely structured by age and laying date; older and earlier-nesting birds are superior to younger and later birds on several measures of performance. This study suggests that finely-tuned nest defense behavior is one component of the superior performance of old birds.

Comparative embryotoxicity of a pentabrominated diphenyl ether mixture to common terns (Sterna hirundo) and American kestrels (Falco sparverius).

Concentrations of polybrominated diphenyl ethers (PBDEs) in Forster's tern (Sterna forsteri) eggs from San Francisco Bay have been reported to range up to 63µgg(-1) lipid weight. This value exceeds the lowest-observed-adverse-effect level (1.8µgg(-1) egg wet weight; ∼32µg(-1) lipid weight) reported in an embryotoxicity study with American kestrels (Falco sparverius). As a surrogate for Forster's terns, common tern (Sterna hirundo) eggs were treated by air cell injection with corn oil vehicle (control) or a commercial penta-BDE formulation (DE-71) at nominal concentrations of 0.2, 2, and 20µgg(-1) egg. As a positive control, kestrel eggs received vehicle or 20µg DE-71g(-1) egg. In terns, there were no effects of DE-71 on embryonic survival, and pipping or hatching success; however, treated eggs hatched later (0.44d) than controls. Organ weights, organ-to-body weight ratios, and bone lengths did not differ, and histopathological observations were unremarkable. Several measures of hepatic oxidative stress in hatchling terns were not affected by DE-71, although there was some evidence of oxidative DNA damage (8-hydroxy-deoxyguanosine; 8-OH-dG). Although DE-71 did not impair pipping and hatching of kestrels, it did result in a delay in hatch, shorter humerus length, and reduced total thyroid weight. Concentrations of oxidized glutathione, reduced glutathione, thiobarbituric acid reactive substances, and 8-OH-dG in liver were greater in DE-71-treated kestrels compared to controls. Our findings suggest common tern embryos, and perhaps other tern species, are less sensitive to PBDEs than kestrel embryos.