Haida Gwaii Archipelago Research Articles

Genomic changes underlying repeated niche shifts in an adaptive radiation.

In adaptive radiations, single lineages rapidly diversify by adapting to many new niches. Little is known yet about the genomic mechanisms involved, that is, the source of genetic variation or genomic architecture facilitating or constraining adaptive radiation. Here, we investigate genomic changes associated with repeated invasion of many different freshwater niches by threespine stickleback in the Haida Gwaii archipelago, Canada, by resequencing single genomes from one marine and 28 freshwater populations. We find 89 likely targets of parallel selection in the genome that are enriched for old standing genetic variation. In contrast to theoretical expectations, their genomic architecture is highly dispersed with little clustering. Candidate genes and genotype‐environment correlations match the three major environmental axes predation regime, light environment, and ecosystem size. In a niche space with these three dimensions, we find that the more divergent a new niche from the ancestral marine habitat, the more loci show signatures of parallel selection. Our findings suggest that the genomic architecture of parallel adaptation in adaptive radiation depends on the steepness of ecological gradients and the dimensionality of the niche space.

Population genomics of Sitka black-tailed deer supports invasive species management and ecological restoration on islands

Invasive mammals represent a critical threat to island biodiversity; eradications can result in ecological restoration yet may fail in the absence of key population parameters. Over-browsing by invasive Sitka black-tailed deer (Odocoileus hemionus sitkensis) is causing severe ecological and cultural impacts across the Haida Gwaii archipelago (Canada). Previous eradication attempts demonstrate forest regeneration upon deer removal, but reinvasion reverses conservation gains. Here we use restriction-site associated DNA sequencing (12,947 SNPs) to investigate connectivity and gene flow of invasive deer (n = 181) across 15 islands, revealing little structure throughout Haida Gwaii and identifying the large, central island of Moresby (>2600 km2) as the greatest source of migrants. As a result, the archipelago itself should be considered the primary eradication unit, with the exception of geographically isolated islands like SGang Gwaay. Thus, limiting eradications to isolated islands combined with controlled culling and enhanced biosecurity may be the most effective strategies for achieving ecological restoration goals.

Using Geolocator Data to Address Changes in Migration Patterns for Black Turnstone

AbstractBlack Turnstone is an obligate Pacific coast shorebird that is included as a “Species of High Concern” in both the U.S. and Alaska Shorebird Conservation Plans. Specific migration routes for this species are not well understood, which makes its recent disappearance at a major spring stopover site, northern Montague Island in Prince William Sound, Alaska, difficult to interpret. We tracked 23 Black Turnstones between breeding and wintering areas and examined migration timing, duration, and routes used. We identified two high-use regions during migration: 1) Cook Inlet/Shelikof Strait, Alaska, and 2) the Haida Gwaii Archipelago in British Columbia/Alexander Archipelago in southeastern Alaska. This second region was also an important wintering area. We found that northbound migration was longer than southbound (the reverse of what is often observed in shorebirds) and that staging behavior was primarily seen during northbound migration. No birds were tracked to northern Montague Island, and only a few individuals stopped anywhere in Prince William Sound. Alterations in patterns of spring herring spawn in Prince William Sound may be affecting the routes and stopovers used by Black Turnstones, and birds may be wintering farther north in recent decades due to warmer winter conditions. Additionally, the increasing availability and popularity of citizen science efforts like eBird has created a mechanism for disseminating observations from less accessible parts of the Black Turnstone range, a fact which may confound our understanding of whether migration routes for this species have changed over the last 30 years.

Report of new lobsters (Crustacea, Decapoda) from the Lower Cretaceous (Albian) of Haida Gwaii Archipelago, Canada

Report of new lobsters (Crustacea, Decapoda) from the Lower Cretaceous (Albian) of Haida Gwaii Archipelago, Canada

Deer exclusion unveils abiotic filtering in forest understorey plant assemblages.

The role of deer (family Cervidae) in ecosystem functioning has traditionally been neglected by forest ecologists due to the animal's scarcity in most parts of the northern hemisphere. However, the dramatic rebound in deer populations throughout the 20th century has brought deer browsing to the forefront of forest ecological questioning. Today there is ample evidence that deer affect tree regeneration, understorey plant and animal diversity, and even litter decomposition. However, the mechanisms underlying the effects of deer on forest ecosystems remain unclear. Among others, the relative role of abiotic factors versus biotic interactions (e.g. herbivory) in shaping plant assemblages remains largely unknown. We used a large-scale experiment with exclosures distributed along abiotic gradients to understand the role of black-tailed deer (Odocoileus hemionus sitchensis) on the forest understorey on the Haida Gwaii archipelago (western Canada), a unique context where most of the key ecological effects of deer presence have already been intensively studied. Our results demonstrate that 20 years of deer exclusion resulted in a clear increase in vascular plant richness, diversity and cover, and caused a decline in bryophyte cover. Exclusion also unveiled abiotic (i.e. soil water availability and fertility) filtering of plant assemblages that would otherwise have been masked by the impact of abundant deer populations. However, deer exclusion did not lead to an increase in beta diversity, probably because some remnant species had a competitive advantage to regrow after decades of over browsing. We demonstrated that long-term herbivory by deer can be a dominant factor structuring understorey plant communities that overwhelms abiotic factors. However, while exclosures prove useful to assess the overall effects of large herbivores, the results from our studies at broader scales on the Haida Gwaii archipelago suggest that exclosure experiments should be used cautiously when inferring the mechanisms at work.

Global origins of invasive brown rats (Rattus norvegicus) in the Haida Gwaii archipelago

Brown rats (Rattus norvegicus) have commensally spread from northern China and Mongolia to become among the most invasive species on the planet. Understanding the proximate source(s) of invasion can inform biosecurity plans and eradication strategies for preventing or mitigating impacts to native biodiversity. The Haida Gwaii archipelago, located off the coast of British Columbia, Canada, is a significant nesting site for 1.5 million seabirds across 12 species, half of which are now threatened by brown rats. Local knowledge points to a European origin in the late 1800’s to early 1900’s, though the true source(s) and firm date(s) of invasion remain unknown. To fill these knowledge gaps, we analyzed genotypic data (16,598 SNPs) for 280 brown rats sampled throughout Haida Gwaii relative to a published global database of potential source populations. Principle component analysis and population assignment tests supported multiple potential invasion sources from Europe and North America. Likewise, demographic modelling best supported two invasions into the islands. The first invasion likely occurred in the early 1900’s into the south-central archipelago from Western Europe followed by a more recent invasion in the early 2000’s from Vancouver, British Columbia, into northern Haida Gwaii. The northern invasion of Haida Gwaii could also be indicative of contemporary gene flow between Haida Gwaii and the mainland, representing a significant biosecurity risk. Our results will inform management strategies for invasive rats in Haida Gwaii and serve as a guide for studies in other isolated systems worldwide.

Rattus population genomics across the Haida Gwaii archipelago provides a framework for guiding invasive species management.

Invasive species have led to precipitous declines in biodiversity, especially in island systems. Brown (Rattus norvegicus) and black rats (R. rattus) are among the most invasive animals on the planet, with eradication being the primary tool for established island populations. The need for increased research for defining eradication units and monitoring outcomes has been highlighted as a means to maximize success. Haida Gwaii is an archipelago ~100 km off the northern coast of British Columbia, Canada, that hosts globally significant breeding populations of seabirds that are at risk due to invasive rats. Here, we paired sampling of brown (n = 287) and black (n = 291) rats across the Haida Gwaii archipelago with genotyping by sequencing (10,770–27,686 SNPs) to investigate patterns of population connectivity and infer levels/direction of gene flow among invasive rat populations in Haida Gwaii. We reconstructed three regional clusters for both species (north, central and south), with proximate populations within regions being largely more related than those that were more distant, consistent with predictions from island biogeography theory. Population assignment of recently detected individuals post‐eradication on Faraday, Murchison and the Bischof Islands revealed all were re‐invaders from Lyell Island, rather than being on‐island survivors. Based on these results, we identified six eradication units constituting single or clusters of islands that would limit the potential for reinvasion, some of which will need to be combined with biosecurity measures. Overall, our results highlight the importance of targeted research prior to conducting eradications and demonstrate a framework for applying population genomics for guiding invasive species management in island systems.

Spatial, sexual, and rapid temporal differentiation in neuromast expression on lateral plates of Haida Gwaii threespine stickleback (Gasterosteusaculeatus)

Lateral lines, a major sensory modality in fishes, are diverse among taxa, but their intraspecific variation has received limited attention. We examined numbers of superficial neuromasts on the buttressing lateral plates (LP) of 1910 threespine stickleback (Gasterosteus aculeatus Linnaeus, 1758) from 26 ecologically and morphologically diverse populations on the Haida Gwaii archipelago, western Canada. Extending from previous studies, we predicted that (i) highly stained dystrophic localities would have threespine stickleback with elevated numbers of neuromasts per plate due to a greater reliance on non-visual sensory modalities and (ii) that LP count and neuromast numbers per plate would functionally covary with predatory assemblage. We found that there were no differences in neuromast count across major habitats (marine, lake, stream), but clear-water populations and those with predatory fish had significantly more neuromasts per plate than most populations in highly stained dystrophic lakes, the effects being accentuated on the first buttressing plate (LP4). We also report the first evidence that neuromast counts per plate are sexually dimorphic, with males having a greater density of neuromasts in most populations. Two transplant experiments between ecologically opposite habitats indicate that within 12 generations, neuromast counts per plate can rapidly shift in response to a change in habitat.

Seismic induced flow disruption of Gandll K'in Gwaay.yaay thermal springs, Gwaii Haanas National Park Reserve, Canada

The October 28, 2012 magnitude 7.8 Haida Gwaii earthquake disrupted flow of the only thermal springs in the Haida Gwaii archipelago of western Canada. Springs of the Gandll K'in Gwaay.yaay geothermal system ceased discharge at existing outlets and spring pools drained empty. Subsequent visits to the remote site documented return of flow at the lowest elevation discharge points, although at a greatly reduced discharge rate. Over time thermal water discharge was renewed at higher elevations and the total discharge rate increased.To understand better how seismic activity affected the spring flow, at a site ∼30 km distant from the epicentre, a study was initiated to inform development of a conceptual model of the thermal system. Stable isotope data show that thermal waters discharging at Gandll K'in Gwaay.yaay originate in deep circulation of meteoric waters, where they are heated by the normal increase in ground temperature with depth. Geothermal gradients in the region are relatively low, and aqueous geothermometry suggests that circulation depths of the system are ∼3.6 km. There is no significant difference in overall water geochemistry from before and after the earthquake, either suggesting that the flow path was clogged, or that changes in water pressure in the recharge zone have reduced the overall system drive. We propose a conceptual model, suggesting that the earthquake induced a drop in the water table of the recharge zone, reducing the driving force of the flow system, leading to flow cessation. As the water table returned back to normal elevations the spring system has begun to return to pre-earthquake discharge patterns. This interpretation is consistent with traditional knowledge of the site, were oral history records previous earthquake induced flow cessations and subsequent returns of spring flow.

Experimental evidence for rapid genomic adaptation to a new niche in an adaptive radiation.

A substantial part of biodiversity is thought to have arisen from adaptive radiations in which one lineage rapidly diversified into multiple lineages adapted to many different niches. However, selection and drift reduce genetic variation during adaptation to new niches and may thus prevent or slow down further niche shifts. We tested whether rapid adaptation is still possible from a highly derived ecotype in the adaptive radiation of threespine stickleback on the Haida Gwaii archipelago, Western Canada. In a 19-years selection experiment, we let giant stickleback from a large blackwater lake evolve in a small clearwater pond without vertebrate predators. 56 whole genomes from the experiment and 26 natural populations revealed that adaptive genomic change was rapid in many small genomic regions and encompassed 75% of the adaptive genomic change between 12,000 years old ecotypes. Adaptive genomic change was as fast as phenotypic change in defence and trophic morphology and both were largely parallel between the short-term selection experiment and long-term natural adaptive radiation. Our results show that functionally relevant standing genetic variation can persist in derived adaptive radiation members, allowing adaptive radiations to unfold very rapidly.

Levels of fecal glucocorticoid metabolites do not reflect environmental contrasts across islands in black-tailed deer (Odocoileus hemionus sitkensis) populations

Animals face stressful situations to which they can respond by mounting a physiological response. Few studies have compared the relative effects of two or more stressors on this response. We compared how low food abundance and hunting affected levels of fecal glucocorticoid metabolites (FGM), an indicator of stress, in Sitka black-tailed deer (Odocoileus hemionus sitkensis) on the Haida Gwaii archipelago (Canada). We monitored monthly FGM levels over a year on three islands: on two, there was no hunting but deer were exposed to increased risk of severe food depletion; and on one, deer had access to abundant food but were exposed to a few days of hunting each year. Based on the context of the study, we tentatively predicted that FGM levels would be higher in low food abundance/safe islands. We also predicted that FGM levels would be higher in winter when food is rarer, particularly in low food abundance/safe islands. The three deer populations presented similar average FGM levels and seasonal variations. Our predictions were therefore not supported. Our results rather suggested that environmental contrasts, perceived by us as large (increased risk of starvation on ELI and Kunga islands) or associated with differences in animal behavior (human avoidance on Reef island), did not lead to increased stress responses. We discuss plausible explanations, including the down-regulation of the stress response in depleted environments and the lack of stress response to low hunting pressure when behavioral responses to risk are unlikely to be costly.

Early Albian (Early Cretaceous) douvilleiceratid ammonites from Haida Gwaii, British Columbia, Canada

AbstractThe early Albian to mid-Albian cosmopolitan genusDouvilleicerasis represented in the Haida Gwaii archipelago of western British Columbia by five species,D.mammillatum(Schlotheim),D.offarcinatum(White),D.scabrosumCasey,D.spiniferum(Whiteaves), andD. aff.spiniferum(Whiteaves). Specimens of one of these taxa,D.spiniferum, are particularly abundant on Haida Gwaii and the species is discussed with respect to its morphological variability and ontogenetic development. The important morphological features for taxonomic criteria of the genusDouvilleicerasare the mode of tuberculation, the pattern of ribbing, and the proportions of the shell in the middle growth stage.

Corrigendum: Short-term effects of hunting on naïve black-tailed deer (Odocoileus hemionus sitkensis): behavioural response and consequences on vegetation growth

Hunting is commonly used to reduce overabundant deer populations that are of socioeconomic and ecological concerns. Recently, it has been suggested that “hunting for fear” might help maximize nonconsumptive effects of hunting and their cascading impacts. We investigated how a predator-free black-tailed deer (Odocoileus hemionus sitkensis Merriam, 1898) population introduced to the Haida Gwaii archipelago (Canada) responded to short-term hunting for fear. We conducted a hunt that minimized killing and maximized scaring on an island where some deer were marked. Between control and hunted sites, we compared deer use of bait stations and of shoreline areas (i.e., an open and risky area that provided marine subsidies). We also compared the browsing pressure and growth of two grasses and two shrubs. Hunting for fear had no effect on the overall use of bait stations and shorelines. However, in the area exposed to hunting, unmarked deer, which were assumed to be less tolerant of human disturbance, avoided bait st...

Thermal regime, predation danger and the early marine exit of sockeye salmon Oncorhynchus nerka.

Marine exit timing of sockeye salmon Oncorhynchus nerka populations on the Haida Gwaii Archipelago, British Columbia, Canada, is described, with specific focus on Copper Creek. Marine exit in Copper Creek occurs > 130 days prior to spawning, one of the longest adult freshwater residence periods recorded for any O. nerka population. Copper Creek presents an easy upstream migration, with mild water temperatures (7 to 14° C), short distance (13·1 km) and low elevation gain (41 m) to the lake where fish hold prior to spawning. An energetic model estimates that <1% of the initial energy reserve is required for upstream migration, compared with 62% for lake holding and 38% for reproductive development. Historical records suggest that it is unlikely that water temperature in any of the O.nerka streams in Haida Gwaii has ever exceeded the presumed temperature threshold (19° C) for early marine exit. Although it is not impossible that the thermal tolerance of Copper Creek O.nerka is very low, the data presented here appear inconsistent with thermal avoidance as an explanation for the early marine exit timing in Copper Creek and in three other populations on the archipelago with early marine exit.

Short-term effects of hunting on naïve black-tailed deer (Odocoileus hemionus sitkensis): behavioural response and consequences on vegetation growth

Hunting is commonly used to reduce overabundant deer populations that are of socioeconomic and ecological concerns. Recently, it has been suggested that “hunting for fear” might help maximize nonconsumptive effects of hunting and their cascading impacts. We investigated how a predator-free black-tailed deer (Odocoileus hemionus sitkensis Merriam, 1898) population introduced to the Haida Gwaii archipelago (Canada) responded to short-term hunting for fear. We conducted a hunt that minimized killing and maximized scaring on an island where some deer were marked. Between control and hunted sites, we compared deer use of bait stations and of shoreline areas (i.e., an open and risky area that provided marine subsidies). We also compared the browsing pressure and growth of two grasses and two shrubs. Hunting for fear had no effect on the overall use of bait stations and shorelines. However, in the area exposed to hunting, unmarked deer, which were assumed to be less tolerant of human disturbance, avoided bait stations at the outset of hunting. We concluded that individuals perceive and respond to risk differently. Furthermore, two of the four plant species were less likely to be browsed and had better growth in the experimental area than in the control area, suggesting an indirect effect of hunting on plants mediated by deer behaviour.

Understanding the paradox of deer persisting at high abundance in heavily browsed habitats

In the context of remarkable increases in many deer populations observed in temperate forests, it is critical to better understand the processes sustaining abundant populations despite dramatic declines in the vegetation they feed on. When natural predation and hunting levels are too low to control deer populations, a resource‐driven negative feedback is expected. Such a feedback assumes that the remaining resources do not match the energy requirements of a current herbivore population, thereby limiting herbivore abundance. Here we take advantage of a well‐documented, long‐term study of abundant predator‐free populations of black‐tailed deer Odocoileus hemionus sitkensis on the Haida Gwaii archipelago (Canada) to assess the ability of a heavily browsed forest habitat to sustain abundant deer populations. For two deer populations, we: 1) compared the energy provided by various resource pools to the energy required by deer; and 2) identified what components of the environment contributed most to support them. Qualitatively, our results are robust to the many assumptions and uncertainties and identify the resources currently available that allow these abundant deer populations to meet their energy needs despite the apparent paucity in resources. Resources are provided by a flux of hardly visible plant tissue produced by perennial species highly tolerant of herbivory and able to survive via underground structures (e.g. rhizomes), and by subsidies provided by canopy trees or by plants in refuges (i.e. litterfall and seed bank). We discuss the possibility of a resource‐driven feedback that may ultimately occur in the long term as a result of changes in recruitment, productivity and fertility of plants. The possible lack of resource‐driven feedback in the short or medium term should be considered by managers when assessing the need for active deer population control in situations without carnivores or hunting.

A better world for bryophytes? A rare and overlooked case of positive community-wide effects of browsing by overabundant deer

During the twentieth century, populations of several deer species (Cervidae) increased dramatically in temperate and boreal forests worldwide, leading to major changes in forest plant and animal communities. The effect of deer overabundance on understory vegetation has been documented repeatedly. In situations of severe browsing pressure, even the least palatable vascular plants were negatively affected. However, deer impact on bryophytes has been greatly under-investigated despite their key role in ecosystem functioning and their high conservation profile. Taking advantage of a unique situation involving adjacent islands with and without deer that resulted from the introduction of black-tailed deer (Odocoileus hemionus) to the Haida Gwaii archipelago (British Columbia, Canada) we explored the response of the bryophyte community to unregulated browsing. We compared species density, cover, and diversity between small islands never colonized by deer and small islands with prolonged deer presence. We took a novel approach that combined direct observations of deer foraging with sampling of their impact on the vegetation. We show that even in situations of severe browsing pressure deer totally avoided bryophytes. Contrary to what is observed for vascular plants (even for tolerant species such as graminoids), species density, cover, and diversity of bryophytes were higher on the islands with deer. We attribute this pattern of higher bryophyte prevalence to reduced competition with vascular plants, especially for light.

Phylogeography and adaptation genetics of stickleback from theHaidaGwaii archipelago revealed using genome‐wide single nucleotide polymorphism genotyping

Threespine stickleback populations are model systems for studying adaptive evolution and the underlying genetics. In lakes on the Haida Gwaii archipelago (off western Canada), stickleback have undergone a remarkable local radiation and show phenotypic diversity matching that seen throughout the species distribution. To provide a historical context for this radiation, we surveyed genetic variation at >1000 single nucleotide polymorphism (SNP) loci in stickleback from over 100 populations. SNPs included markers evenly distributed throughout genome and candidate SNPs tagging adaptive genomic regions. Based on evenly distributed SNPs, the phylogeographic pattern differs substantially from the disjunct pattern previously observed between two highly divergent mtDNA lineages. The SNP tree instead shows extensive within watershed population clustering and different watersheds separated by short branches deep in the tree. These data are consistent with separate colonizations of most watersheds, despite underlying genetic connections between some independent drainages. This supports previous suppositions that morphological diversity observed between watersheds has been shaped independently, with populations exhibiting complete loss of lateral plates and giant size each occurring in several distinct clades. Throughout the archipelago, we see repeated selection of SNPs tagging candidate freshwater adaptive variants at several genomic regions differentiated between marine–freshwater populations on a global scale (e.g. EDA, Na/K ATPase). In estuarine sites, both marine and freshwater allelic variants were commonly detected. We also found typically marine alleles present in a few freshwater lakes, especially those with completely plated morphology. These results provide a general model for postglacial colonization of freshwater habitat by sticklebacks and illustrate the tremendous potential of genome-wide SNP data sets hold for resolving patterns and processes underlying recent adaptive divergences.

Importance for forest plant communities of refuges protecting from deer browsing

There is growing evidence that the increase of wild ungulates worldwide is responsible of strong deleterious impacts on various component of forest biodiversity (tree and shrub regeneration, insects, songbirds). Plant communities are particularly affected by overbrowsing, and overabundant deer are increasingly recognized as a major factor of decline in understory plant diversity in temperate and boreal forest ecosystems.In grassland ecosystems, refuges from herbivores have been shown to provide suitable habitat for plants sensitive to browsing and grazing, and to allow the conservation of rare plant species. In the present study we analyze if such refuges can maintain representative samples of forest plant communities exposed to strong browsing pressure by deer. For this we used the unique situation offered by the presence, side by side, on the Haida Gwaii archipelago of forested islands colonized or not by introduced deer.We compared plant assemblages on rocky outcrop to assemblages found in the adjacent field-layer in order (1) to assess, on islands without deer, the potential of refuges to be representative of the local field-layer communities and (2), on islands colonized by deer for over 60years, to analyze how far plant assemblages on rocky outcrops are representative of un-browsed field-layer communities and can serve as bioassays for field-layer plant communities in the absence of unbrowsed reference sites. We did this for forest-interior field-layer plant communities as well as for the forest edge plant communities found along the shorelines. We used refuges on treefall mounds to assess the role refuges can play as sources of propagules in two understory shrubs and ferns.Our results indicate that, in presence of deer, plant species density and plant cover are dramatically higher in refuges than in the adjacent field-layer plots. The comparison of these refuge communities to the reference state provided by the field-layer on islands without deer indicated that refuges maintain a representative part of the unbrowsed plant community, although with differences in the cover percentage in some plants. Some typical plants are more abundant in the refuges and, more sobering, six field-layer species are only poorly present in the rocky habitat. Despite these differences and their small size, refuges shelter a representative part of the understory and forest edge vegetation of the studied sites and could serve as a bioassay of deer overbrowsing in situations lacking a reference state.

Prolonged life span among endemicGasterosteuspopulations

Throughout their circumboreal coastal distribution, the threespine stickleback ( Gasterosteus aculeatus L., 1758) typically reproduce at 1 or 2 years of age (second or third summer) and die during the year of the reproductive cycle. Extending from a previous study on the Haida Gwaii archipelago, western Canada, that identified an exceptionally long life span (8 years) in a population of large-bodied threespine stickleback, we use pelvic spine annuli to examine age of the five largest adult stickleback of 12 additional populations comprising five populations with average-sized adults (45–60 mm standard length (SL)) and seven populations with large-bodied adult stickleback (&gt;75 mm SL). Each of the small-bodied populations had a maximum age of 1 or 2 years typical for the taxon. Among the large-bodied populations, which also reached adult size in the 2nd year, adult stickleback in the populations ranged from 3 to 6 years, indicating extended longevity. Low productivity habitats and refuge against gape-limited piscivores, each of which theoretically predicts reduced rate of senescence, are associated with the greatest longevity among these populations. These data combined with the recent full genome sequence for stickleback provide opportunities for locating genetic markers for extended longevity.