Linking Mesoscale Spatial Variation in Methylmercury Production to Bioaccumulation in Tidal Marsh Food Webs.

Differences in sediment biogeochemistry among tidal marsh features with different hydrological and geomorphological characteristics, including marsh interiors, marsh edges, first-order channels, and third-order channels, can result in spatial variation in MeHg production and availability. To better understand the link between MeHg production in sediments and bioaccumulation in primary and secondary consumer invertebrates and fish, we characterized mesoscale spatial variation in sediment biogeochemistry and MeHg concentrations of sediments, water, and consumer tissues among marsh features. Our results indicated that marsh interiors had biogeochemical conditions, including greater concentrations of organic matter and sulfate reduction rates, that resulted in greater MeHg concentrations in sediments and surface water particulates from marsh interiors compared to other features. Tissue MeHg concentrations of consumers also differed among features, with greater concentrations from marsh edges and interiors compared to channels. This spatial mismatch of MeHg concentrations in sediments and water compared to those in consumers may have resulted from differences in behavior and physiology among consumers that influenced the spatial scale over which MeHg was integrated into tissues. Our results highlight the importance of sampling across a suite of marsh features and considering the behavioral and physiological traits of sentinel taxa for contaminant monitoring studies.

Reference genome of the black rail, Laterallus jamaicensis.

The black rail, Laterallus jamaicensis, is one of the most secretive and poorly understood birds in the Americas. Two of its five subspecies breed in North America: the Eastern black rail (L. j. jamaicensis), found primarily in the southern and mid-Atlantic states, and the California black rail (L. j. coturniculus), inhabiting California and Arizona, are recognized across the highly disjunct distribution. Population declines, due primarily to wetland loss and degradation, have resulted in conservation status listings for both subspecies. To help advance understanding of the phylogeography, biology, and ecology of this elusive species, we report the first reference genome assembly for the black rail, produced as part of the California Conservation Genomics Project (CCGP). We produced a de novo genome assembly using Pacific Biosciences HiFi long reads and Hi-C chromatin-proximity sequencing technology with an estimated sequencing error rate of 0.182%. The assembly consists of 964 scaffolds spanning 1.39 Gb, with a contig N50 of 7.4 Mb, scaffold N50 of 21.4 Mb, largest contig of 44.8 Mb, and largest scaffold of 101.2 Mb. The assembly has a high BUSCO completeness score of 96.8% and represents the first genome assembly available for the genus Laterallus. This genome assembly can help resolve questions about the complex evolutionary history of rails, assess black rail vagility and population connectivity, estimate effective population sizes, and evaluate the potential of rails for adaptive evolution in the face of growing threats from climate change, habitat loss and fragmentation, and disease.

Reference genome of the Virginia rail, Rallus limicola.

The Virginia rail, Rallus limicola, is a member of the family Rallidae, which also includes many other species of secretive and poorly studied wetland birds. It is recognized as a single species throughout its broad distribution in North America where it is exploited as a game bird, often with generous harvest limits, despite a lack of systematic population surveys and evidence of declines in many areas due to wetland loss and degradation. To help advance understanding of the phylogeography, biology, and ecology of this elusive species, we report the first reference genome assembly for the Virginia rail, produced as part of the California Conservation Genomics Project (CCGP). We produced a de novo genome assembly using Pacific Biosciences HiFi long reads and Hi-C chromatin-proximity sequencing technology with an estimated sequencing error rate of 0.191%. The assembly consists of 1,102 scaffolds spanning 1.39 Gb, with a contig N50 of 11.0 Mb, scaffold N50 of 25.3 Mb, largest contig of 45 Mb, and largest scaffold of 128.4 Mb. It has a high BUSCO completeness score of 96.9% and represents the first genome assembly available for the genus Rallus. This genome assembly will help resolve questions about the complex evolutionary history of rails and evaluate the potential of rails for adaptive evolution in the face of growing threats from climate change and habitat loss and fragmentation. It will also provide a valuable resource for rail conservation efforts by quantifying Virginia rail vagility, population connectivity, and effective population sizes.

Stability of patch-turnover relationships under equilibrium and nonequilibrium metapopulation dynamics driven by biogeography.

Two controversial tenets of metapopulation biology are whether patch quality and the surrounding matrix are more important to turnover (colonisation and extinction) than biogeography (patch area and isolation) and whether factors governing turnover during equilibrium also dominate nonequilibrium dynamics. We tested both tenets using 18 years of surveys for two secretive wetland birds, black and Virginia rails, during (1) a period of equilibrium with stable occupancy and (2) after drought and arrival of West Nile Virus (WNV), which resulted in WNV infections in rails, increased extinction and decreased colonisation probabilities modified by WNV, nonequilibrium dynamics for both species and occupancy decline for black rails. Area (primarily) and isolation (secondarily) drove turnover during both stable and unstable metapopulation dynamics, greatly exceeding the effects of patch quality and matrix conditions. Moreover, slopes between turnover and patch characteristics changed little between equilibrium and nonequilibrium, confirming the overriding influences of biogeographic factors on turnover.

Age- and sex-related dietary specialization facilitate seasonal resource partitioning in a migratory shorebird.

Dietary specialization is common in animals and has important implications for individual fitness, inter- and intraspecific competition, and the adaptive potential of a species. Diet composition can be influenced by age- and sex-related factors including an individual's morphology, social status, and acquired skills; however, specialization may only be necessary when competition is intensified by high population densities or increased energetic demands.To better understand the role of age- and sex-related dietary specialization in facilitating seasonal resource partitioning, we inferred the contribution of biofilm, microphytobenthos, and benthic invertebrates to the diets of western sandpipers (Calidris mauri) from different demographic groups during mid-winter (January/February) and at the onset of the breeding migration (April) using stable isotope mixing models. Western sandpipers are sexually dimorphic with females having significantly greater body mass and bill length than males.Diet composition differed between seasons and among demographic groups. In winter, prey consumption was similar among demographic groups, but, in spring, diet composition differed with bill length and body mass explaining 31% of the total variation in diet composition. Epifaunal invertebrates made up a greater proportion of the diet in males which had lesser mass and shorter bills than females. Consumption of Polychaeta increased with increasing bill length and was greatest in adult females. In contrast, consumption of microphytobenthos, thought to be an important food source for migrating sandpipers, increased with decreasing bill length and was greatest in juvenile males.Our results provide the first evidence that age- and sex-related dietary specialization in western sandpipers facilitate seasonal resource partitioning that could reduce competition during spring at the onset of the breeding migration.Our study underscores the importance of examining resource partitioning throughout the annual cycle to inform fitness and demographic models and facilitate conservation efforts.

Disentangling the effects of habitat biogeochemistry, food web structure, and diet composition on mercury bioaccumulation in a wetland bird.

Methylmercury (MeHg) is a globally pervasive contaminant with known toxicity to humans and wildlife. Several sources of variation can lead to spatial differences in MeHg bioaccumulation within a species including: biogeochemical processes that influence MeHg production and availability within an organism's home range; trophic positions of consumers and MeHg biomagnification efficiency in food webs; and individual prey preferences that influence diet composition. To better understand spatial variation in MeHg bioaccumulation within a species, we evaluated the effects of habitat biogeochemistry, food web structure, and diet composition in the wetland-obligate California black rail (Laterallus jamaicensis coturniculus) at three wetlands along the Petaluma River in northern San Francisco Bay, California, USA. The concentration of MeHg in sediments differed significantly among wetlands. We identified three sediment and porewater measurements that contributed significantly to a discriminant function explaining differences in habitat biogeochemistry among wetlands: the porewater concentration of ferrous iron, the percent organic matter, and the sediment MeHg concentration. Food web structure and biomagnification efficiency were similar among wetlands, with trophic magnification factors for MeHg ranging from 1.84 to 2.59. In addition, regurgitation samples indicated that black rails were dietary generalists with similar diets among wetlands (percent similarity indices > 70%). Given the similarities in diet composition, food web structure, and MeHg biomagnification efficiency among wetlands, we concluded that variation in habitat biogeochemistry and associated sediment MeHg production was the primary driver of differences in MeHg concentrations among black rails from different wetlands.

Validating dispersal distances inferred from autoregressive occupancy models with genetic parentage assignments.

Dispersal distances are commonly inferred from occupancy data but have rarely been validated. Estimating dispersal from occupancy data is further complicated by imperfect detection and the presence of unsurveyed patches. We compared dispersal distances inferred from seven years of occupancy data for 212 wetlands in a metapopulation of the secretive and threatened California black rail (Laterallus jamaicensis coturniculus) to distances between parent-offspring dyads identified with 16 microsatellites. We used a novel autoregressive multi-season occupancy model that accounted for both unsurveyed patches and imperfect detection to quantify patch isolation using buffer radius (BRM) and incidence function (IFM) connectivity measures at 15 scales (1-10, 15, 20, 25, and 30 km). Connectivity measures were then fit as colonization covariates in occupancy models to estimate a model-averaged dispersal distance. As predicted, colonization was more strongly related to connectivity at small spatial scales (<10 km). AIC weights were greatest at 7 km for BRM and at 4 km for IFM. Model-averaged dispersal distances (BRM = 7.46 km; IFM = 5.48 km) showed good agreement with the mean M(±SE) dispersal distance from 23 parent-offspring dyads (5.58 ± 1.92 km), indicating reasonably accurate mean dispersal distances can be inferred from occupancy data when isolation strongly affects colonization.

Inferring the timing of long-distance dispersal between Rail metapopulations using genetic and isotopic assignments.

The stochastic and infrequent nature of long-distance dispersal often makes it difficult to detect. We quantified the frequency, distance, and timing of long-distance dispersal in a nonmigratory, secretive wetland bird, the California Black Rail (Laterallus jamaicensis coturniculus), between an inland and a coastal metapopulation separated by greater than 100 km. Using 15 microsatellites in conjunction with stable carbon, nitrogen, and sulfur isotopes, we classified Rails as residents of their capture population, recent migrants that dispersed to their capture population less than one year before capture, established migrants that dispersed to their capture population more than one year before capture, and seasonal migrants that dispersed away from their capture population to forage, but returned the next season. Most Rails (195 of 204, or 95.6%) were classified as residents, but we detected two established migrants that had moved >100 km more than a year before capture. Seven Rails appeared to be seasonal migrants, but comparisons of feather isotope values with isotope values from wetland soils indicated that the isotope values in the feathers of these Rails likely resulted from natural environmental variation (e.g., source element effects) rather than long-distance dispersal of individuals. Thus, these seven Rails were most likely misassigned by isotopic population assignments due to small-scale variation in the isoscape. Using genetic data in conjunction with isotopic data allowed us to not only infer the timing of long-distance dispersal events, but to successfully track long-distance movements of nonmigratory Rails between metapopulations even when environmental variation of isotopes occurred across small spatial scales.

Genetic analyses of historic and modern marbled murrelets suggest decoupling of migration and gene flow after habitat fragmentation.

The dispersal of individuals among fragmented populations is generally thought to prevent genetic and demographic isolation, and ultimately reduce extinction risk. In this study, we show that a century of reduction in coastal old-growth forests, as well as a number of other environmental factors, has probably resulted in the genetic divergence of marbled murrelets (Brachyramphus marmoratus) in central California, despite the fact that 7 per cent of modern-sampled murrelets in this population were classified as migrants using genetic assignment tests. Genetic differentiation appears to persist because individuals dispersing from northern populations contributed relatively few young to the central California population, as indicated by the fact that migrants were much less likely to be members of parent-offspring pairs than residents (10.5% versus 45.4%). Moreover, a recent 1.4 per cent annual increase in the proportion of migrants in central California, without appreciable reproduction, may have masked an underlying decline in the resident population without resulting in demographic rescue. Our results emphasize the need to understand the behaviour of migrants and the extent to which they contribute offspring in order to determine whether dispersal results in gene flow and prevents declines in resident populations.

Characterizing dispersal patterns in a threatened seabird with limited genetic structure.

Genetic assignment methods provide an appealing approach for characterizing dispersal patterns on ecological time scales, but require sufficient genetic differentiation to accurately identify migrants and a large enough sample size of migrants to, for example, compare dispersal between sexes or age classes. We demonstrate that assignment methods can be rigorously used to characterize dispersal patterns in a marbled murrelet (Brachyramphus marmoratus) population from central California that numbers approximately 600 individuals and is only moderately differentiated (F(ST) approximately 0.03) from larger populations to the north. We used coalescent simulations to select a significance level that resulted in a low and approximately equal expected number of type I and II errors and then used this significance level to identify a population of origin for 589 individuals genotyped at 13 microsatellite loci. The proportion of migrants in central California was greatest during winter when 83% of individuals were classified as migrants compared to lower proportions during the breeding (6%) and post-breeding (8%) seasons. Dispersal was also biased toward young and female individuals, as is typical in birds. Migrants were rarely members of parent-offspring pairs, suggesting that they contributed few young to the central California population. A greater number of migrants than expected under equilibrium conditions, a lack of individuals with mixed ancestry, and a small number of potential source populations (two), likely allowed us to use assignment methods to rigorously characterize dispersal patterns for a population that was larger and less differentiated than typically thought required for the identification of migrants.

Characterizing source-sink dynamics with genetic parentage assignments.

Source-sink dynamics have been suggested to characterize the population structure of many species, but the prevalence of source-sink systems in nature is uncertain because of inherent challenges in estimating migration rates among populations. Migration rates are often difficult to estimate directly with demographic methods, and indirect genetic methods are subject to a variety of assumptions that are difficult to meet or to apply to evolutionary timescales. Furthermore, such methods cannot be rigorously applied to high-gene-flow species. Here, we employ genetic parentage assignments in conjunction with demographic simulations to infer the level of immigration into a putative sink population. We use individual-based demographic models to estimate expected distributions of parent-offspring dyads under competing sink and closed-population models. By comparing the actual number of parent-offspring dyads (identified from multilocus genetic profiles) in a random sample of individuals taken from a population to expectations under these two contrasting demographic models, it is possible to estimate the rate of immigration and test hypotheses related to the role of immigration on population processes on an ecological timescale. The difference in the expected number of parent-offspring dyads between the two population models was greatest when immigration into the sink population was high, indicating that unlike traditional population genetic inference models, the highest degree of statistical power is achieved for the approach presented here when migration rates are high. We used the proposed genetic parentage approach to demonstrate that a threatened population of Marbled Murrelets (Braclhyrarmphus marmotus) appears to be supplemented by a low level of immigration (approximately 2-6% annually) from other populations.