Fragmentation effects on an endangered species across a gradient from the interior to edge of its range.

Understanding how habitat fragmentation affects individual species is complicated by challenges associated with quantifying species-specific habitat and spatial variability in fragmentation effects within a species' range. We aggregated a 29-year breeding survey data set for the endangered marbled murrelet (Brachyramphus marmoratus) from >42,000 forest sites throughout the Pacific Northwest (Oregon, Washington, and northern California) of the United States. We built a species distribution model (SDM) in which occupied sites were linked with Landsat imagery to quantify murrelet-specific habitat and then used occupancy models to test the hypotheses that fragmentation negatively affects murrelet breeding distribution and that these effects are amplified with distance from the marine foraging habitat toward the edge of the species' nesting range. Murrelet habitat declined in the Pacific Northwest by 20% since 1988, whereas the proportion of habitat comprising edges increased by 17%, indicating increased fragmentation. Furthermore, fragmentation of murrelet habitat at landscape scales (within 2 km of survey stations) negatively affected occupancy of potential breeding sites, and these effects were amplified near the range edge. On the coast, the odds of occupancy decreased by 37% (95% confidence interval [CI] -54 to 12) for each 10% increase in edge habitat (i.e., fragmentation), but at the range edge (88 km inland) these odds decreased by 99% (95% CI 98 to 99). Conversely, odds of murrelet occupancy increased by 31% (95% CI 14 to 52) for each 10% increase in local edge habitat (within 100 m of survey stations). Avoidance of fragmentation at broad scales but use of locally fragmented habitat with reduced quality may help explain the lack of murrelet population recovery. Further, our results emphasize that fragmentation effects can be nuanced, scale dependent, and geographically variable. Awareness of these nuances is critical for developing landscape-level conservation strategies for species experiencing broad-scale habitat loss and fragmentation.

Efectos de la fragmentación sobre las especies en peligro a lo largo de un gradiente desde el interior hasta el borde de su distribución Resumen Es complicado entender el efecto de la fragmentación del hábitat sobre las especies individuales debido a los retos asociados con la cuantificación de hábitats específicos por especie y la variabilidad espacial de los efectos de la fragmentación dentro de la distribución de la especie. Combinamos los datos de un censo reproductivo realizado durante 29 años para el mérgulo jaspeado (Brachyramphus marmoratus) de >42,000 sitios boscosos a lo largo del noroeste del Pacífico (Oregón, Washington, y el norte de California, EE. UU.). Construimos un modelo de distribución de especie (MDE) en el cual los sitios ocupados estuvieron vinculados con imágenes de Landsat para cuantificar el hábitat específico del mérgulo y después usamos los modelos de ocupación para comprobar la hipótesis de que la fragmentación afecta negativamente la distribución reproductiva de la especie y que estos efectos se amplifican con la distancia entre el hábitat de forrajeo marino y el borde de la distribución de anidación de la especie. El hábitat del mérgulo declinó en la zona en un 20% a partir de 1988, mientras que la proporción de hábitat que comprende bordes incrementó en un 17%, lo que indica un aumento en la fragmentación. Además, la fragmentación del hábitat del mérgulo a escala de paisaje (a de 2 km de las estaciones de censo) afectó negativamente a la ocupación de sitios potenciales de reproducción y estos efectos se amplificaron cerca del borde de la distribución. La probabilidad de ocupación disminuyó en un 37% (95% IC -54 a 12) por cada 10% de incremento en el hábitat de borde (es decir, fragmentación) en la costa, pero en el borde de la distribución (88 km tierra adentro), esta probabilidad disminuyó en un 99% (95% IC 98 a 99). De forma contraria, la probabilidad de ocupación incrementó en un 31% (95% IC 14 a 52) por cada 10% de incremento en el hábitat de borde local (a 100 m de las estaciones de censo). La evasión de la fragmentación a gran escala y el uso de hábitats con calidad reducida y fragmentados a nivel local podría explicar la falta de recuperación poblacional del mérgulo. Más allá, nuestros resultados resaltan que los efectos de la fragmentación pueden estar matizados, depender de la escala y tener variación geográfica. Es importante tener conciencia de estos matices para desarrollar estrategias de conservación a nivel paisaje para las especies que experimentan fragmentación y pérdida del hábitat a gran escala.

Cumulative effects of piscivorous colonial waterbirds on juvenile salmonids: A multi predator-prey species evaluation.

We investigated the cumulative effects of predation by piscivorous colonial waterbirds on the survival of multiple salmonid (Oncorhynchus spp.) populations listed under the U.S. Endangered Species Act (ESA) and determined what proportion of all sources of fish mortality (1 -survival) were due to birds in the Columbia River basin, USA. Anadromous juvenile salmonids (smolts) were exposed to predation by Caspian terns (Hydroprogne caspia), double-crested cormorants (Nannopterum auritum), California gulls (Larus californicus), and ring-billed gulls (L. delawarensis), birds known to consume both live and dead fish. Avian consumption and survival probabilities (proportion of available fish consumed or alive) were estimated for steelhead trout (O. mykiss), yearling Chinook salmon (O. tshawytscha), sub-yearling Chinook salmon, and sockeye salmon (O. nerka) during out-migration from the lower Snake River to the Pacific Ocean during an 11-year study period (2008-2018). Results indicated that probabilities of avian consumption varied greatly across salmonid populations, bird species, colony location, river reach, and year. Cumulative consumption probabilities (consumption by birds from all colonies combined) were consistently the highest for steelhead, with annual estimates ranging from 0.22 (95% credible interval = 0.20-0.26) to 0.51 (0.43-0.60) of available smolts. The cumulative effects of avian consumption were significantly lower for yearling and sub-yearling Chinook salmon, with consumption probabilities ranging annually from 0.04 (0.02-0.07) to 0.10 (0.07-0.15) and from 0.06 (0.3-0.09) to 0.15 (0.10-0.23), respectively. Avian consumption probabilities for sockeye salmon smolts was generally higher than for Chinook salmon smolts, but lower than for steelhead smolts, ranging annually from 0.08 (0.03-0.22) to 0.25 (0.14-0.44). Although annual consumption probabilities for birds from certain colonies were more than 0.20 of available smolts, probabilities from other colonies were less than 0.01 of available smolts, indicating that not all colonies of birds posed a substantial risk to smolt mortality. Consumption probabilities were lowest for small colonies and for colonies located a considerable distance from the Snake and Columbia rivers. Total mortality attributed to avian consumption was relatively small for Chinook salmon (less than 10%) but was the single greatest source of mortality for steelhead (greater than 50%) in all years evaluated. Results suggest that the potential benefits to salmonid populations of managing birds to reduce smolt mortality would vary widely depending on the salmonid population, the species of bird, and the size and location of the breeding colony.

Measuring the additive effects of predation on prey survival across spatial scales.

The degree to which predation is an additive vs. compensatory source of mortality is fundamental to understanding the effects of predation on prey populations and evaluating the efficacy of predator management actions. In the Columbia River basin, USA, predation by Caspian Terns (Hydroprogne caspia) on U.S. Endangered Species Act (ESA)-listed juvenile salmonids (smolts; Oncorhynchus spp.) has led to predator management actions to reduce predation; however, the assumption that reduced predation translates into greater salmonid survival, either within the life stage where predation occurs or across their lifetime, has remained untested. To address this critical uncertainty, we analyzed a long-term (2008-2018) mark-recapture-recovery data set of ESA-listed steelhead trout (O. mykiss) that were tagged (n = 78,409) and subsequently exposed to predation during smolt out-migration through multiple river reaches (spatial scales), jointly estimating weekly probabilities of steelhead survival, mortality due to bird predation, and mortality due to other causes. This concurrent estimation across time-stratified cohorts allowed for the direct measurement of the strength, magnitude, and direction of relationships between survival and Caspian Tern predation. Estimates of Tern predation on steelhead were substantial in most years, with cumulative annual estimates ranging from 0.075 (95% creditable interval = 0.058-0.099) to 0.375 (0.290-0.461). Increases in Tern predation probabilities were associated with statistically significant decreases in steelhead survival probabilities in all evaluated years and salmonid life stages (smolt out-migration and smolt-to-adult returns). Results provide novel evidence that predation by Caspian Terns may have been a super-additive source of mortality during the smolt life stage and a partially additive source of mortality to the adult life stage. Annual estimates of the difference between observed survival and baseline survival (i.e., in the absence of Tern predation) ranged from 0.052 (0.017-0.103) to 0.314 (0.172-0.459) during the steelhead smolt life stage and from 0.011 (0.001-0.029) to 0.049 (0.025-0.078) to the adult life stage. The estimated levels of compensation have important implications for predator management actions aimed at increasing the survival of endangered salmonids, and the modeling approach developed herein provides a framework to directly quantify the impacts of source-specific mortality factors on prey populations.

Disturbance of a rare seabird by ship-based tourism in a marine protected area.

Managers of marine protected areas (MPAs) must often seek ways to allow for visitation while minimizing impacts to the resources they are intended to protect. Using shipboard observers, we quantified the "zone of disturbance" for Kittlitz's and marbled murrelets (Brachyramphus brevirostris and B. marmoratus) exposed to large cruise ships traveling through Glacier Bay National Park, one of the largest MPAs in North America. In the upper reaches of Glacier Bay, where Kittlitz's murrelets predominated, binary logistic regression models predicted that 61% of all murrelets within 850 m perpendicular distance of a cruise ship were disturbed (defined as flushing or diving), whereas in the lower reaches, where marbled murrelets predominated, this percentage increased to 72%. Using survival analysis, murrelets in both reaches were found to react at greater distances when ships approached indirectly, presumably because of the ship's larger profile, suggesting murrelets responded to visual rather than audio cues. No management-relevant covariates (e.g., ship velocity, route distance from shore) were found to be important predictors of disturbance, as distance from ship to murrelet accounted for > 90% of the explained variation in murrelet response. Utilizing previously published murrelet density estimates from Glacier Bay, and applying an average empirical disturbance probability (68%) out to 850 m from a cruise ship's typical route, we estimated that a minimum of 9.8-19.6% of all murrelets in Glacier Bay are disturbed per ship entry. Whether these disturbance levels are inconsistent with Park management objectives, which include conserving wildlife as well as providing opportunities for visitation, depends in large part on whether disturbance events caused by cruise ships have impacts on murrelet fitness, which remains uncertain.

Wintering North Pacific black-legged kittiwakes balance spatial flexibility and consistency.

BACKGROUND: Marine environments are inherently dynamic, yet marine predators are often long-lived and employ strategies where consistency, individual specialization, routine migrations, and spatial memory are key components to their foraging and life-history strategies. Intrinsic determinates of animal movements are linked to physiological and life-history traits (e.g. sex, colony, experience), while extrinsic influences occur as the result of an animal's interactions with either other animals or the environment (e.g. prey availability, weather, competition). Knowledge of the factors affecting animal movements is critical to understand energetic bottlenecks and population dynamics. Here, we attempt to understand the interaction of some of these factors on the winter distributions of a surface-feeding seabird in the North Pacific. Between 2008 and 2011, we tracked 99 black-legged kittiwakes breeding at St. Paul and St. George in the Pribilof Islands, Alaska using geolocation loggers. We tested for colony and sex differences in winter distributions, and individual spatial fidelity over two consecutive winters of 17 individuals. Then we linked tracking data to associated environmental conditions as proxies of prey availability (e.g. sea surface temperature, mesoscale eddies, chlorophyll a, and wind) to understand their influence on kittiwake space use at an ocean basin scale. RESULTS: Black-legged kittiwakes from both Pribilof Islands primarily wintered in pelagic sub-arctic waters, however, distributions spanned seven ecoregions of the North Pacific. There was a high degree of similarity in area use of birds from the two closely situated colonies and between sexes. Birds tracked for two consecutive years showed higher fidelity to wintering areas than occurred at random. Annual changes were apparent, as distributions were further north in 2009/10 than 2008/09 or 2010/11. This occurred because 70 % of birds remained in the Bering Sea in the fall of 2009, which corresponded with lower October sea surface temperatures than the other two years. CONCLUSIONS: Although individuals returned to wintering areas in consecutive years, our results suggest that under current conditions individual black-legged kittiwakes have a high capacity to alter winter distributions.

Body size affects individual winter foraging strategies of thick-billed murres in the Bering Sea.

Foraging and migration often require different energetic and movement strategies. Though not readily apparent, constraints during one phase might influence the foraging strategies observed in another. For marine birds that fly and dive, body size constraints likely present a trade-off between foraging ability and migration as smaller bodies reduce flight costs, whereas larger bodies are advantageous for diving deeper. This study examines individual wintering strategies of deep diving thick-billed murres (Uria lomvia) breeding at three colonies in the south-eastern Bering Sea: St Paul, St George and Bogoslof. These colonies, arranged north to south, are located such that breeding birds forage in a gradient from shelf to deep-water habitats. We used geolocation time-depth recorders and stable isotopes from feathers to determine differences in foraging behaviour and diet of murres during three non-breeding periods, 2008-2011. Body size was quantified by a principal component analysis (wing, culmen, head+bill and tarsus length). A hierarchical cluster analysis identified winter foraging strategies based on individual movement, diving behaviour and diet (inferred from stable isotopes). Structural body size differed by breeding island. Larger birds from St Paul had higher wing loading than smaller birds from St George. Larger birds, mainly from St Paul, dove to deeper depths, spent more time in the Bering Sea, and likely consumed higher trophic-level prey in late winter. Three winter foraging strategies were identified. The main strategy, employed by small birds from all three breeding colonies in the first 2 years, was characterized by high residency areas in the North Pacific south of the Aleutians and nocturnal diving. In contrast, 31% of birds from St Paul remained in the Bering Sea and foraged mainly during the day, apparently feeding on higher trophic-level prey. Throat feather stable isotopes indicated that individuals exhibited flexibility in the use of this colony-specific foraging strategy. The third strategy only occurred in 2010/2011, when birds dove more and deeper, suggesting limited prey resources. Foraging strategies partitioned with respect to annual differences, presumably in response to shifts in distribution of prey, and were linked to body size. The presence of a colony-specific wintering strategy suggests the potential for overwinter survival differences between these populations.

Foraging responses of black-legged kittiwakes to prolonged food-shortages around colonies on the Bering Sea shelf.

We hypothesized that changes in southeastern Bering Sea foraging conditions for black-legged kittiwakes (Rissa tridactyla) have caused shifts in habitat use with direct implications for population trends. To test this, we compared at-sea distribution, breeding performance, and nutritional stress of kittiwakes in three years (2008-2010) at two sites in the Pribilof Islands, where the population has either declined (St. Paul) or remained stable (St. George). Foraging conditions were assessed from changes in (1) bird diets, (2) the biomass and distribution of juvenile pollock (Theragra chalcogramma) in 2008 and 2009, and (3) eddy kinetic energy (EKE; considered to be a proxy for oceanic prey availability). In years when biomass of juvenile pollock was low and patchily distributed in shelf regions, kittiwake diets included little or no neritic prey and a much higher occurrence of oceanic prey (e.g. myctophids). Birds from both islands foraged on the nearby shelves, or made substantially longer-distance trips overnight to the basin. Here, feeding was more nocturnal and crepuscular than on the shelf, and often occurred near anticyclonic, or inside cyclonic eddies. As expected from colony location, birds from St. Paul used neritic waters more frequently, whereas birds from St. George typically foraged in oceanic waters. Despite these distinctive foraging patterns, there were no significant differences between colonies in chick feeding rates or fledging success. High EKE in 2010 coincided with a 63% increase in use of the basin by birds from St. Paul compared with 2008 when EKE was low. Nonetheless, adult nutritional stress, which was relatively high across years at both colonies, peaked in birds from St. Paul in 2010. Diminishing food resources in nearby shelf habitats may have contributed to kittiwake population declines at St Paul, possibly driven by increased adult mortality or breeding desertion due to high foraging effort and nutritional stress.

Transcription profiling in environmental diagnostics: health assessments in Columbia River basin steelhead (Oncorhynchus mykiss).

The health condition of out-migrating juvenile salmonids can influence migration success. Physical damage, pathogenic infection, contaminant exposure, and immune system status can affect survival probability. The present study is part of a wider investigation of out-migration success in juvenile steelhead (Oncorhynchus mykiss) and focuses on the application of molecular profiling to assess sublethal effects of environmental stressors in field-collected fish. We used a suite of genes in O. mykiss to specifically assess responses that could be directly related to steelhead health condition during out-migration. These biomarkers were used on juvenile steelhead captured in the Snake River, a tributary of the Columbia River, in Washington, USA, and were applied on gill and anterior head kidney tissue to assess immune system responses, pathogen-defense (NRAMP, Mx, CXC), general stress (HSP70), metal-binding (metallothionein-A), and xenobiotic metabolism (Cyp1a1) utilizing quantitative polymerase chain reaction (PCR) technology. Upon capture, fish were ranked according to visual external physical conditions into good, fair, poor, and bad categories; gills and kidney tissues were then dissected and preserved for gene analyses. Transcription responses were tissue-specific for gill and anterior head kidney with less significant responses in gill tissue than in kidney. Significant differences between the condition ranks were attributed to NRAMP, MX, CXC, and Cyp1a1 responses. Gene profiling correlated gene expression with pathogen presence, and results indicated that gene profiling can be a useful tool for identifying specific pathogen types responsible for disease. Principal component analysis (PCA) further correlated these responses with specific health condition categories, strongly differentiating good, poor, and bad condition ranks. We conclude that molecular profiling is an informative and useful tool that could be applied to indicate and monitor numerous population-level parameters of management interest.

Use of fatty acid analysis to determine dispersal of caspian terns in the Columbia River Basin, USA.

Lethal control, which has been used to reduce local abundances of animals in conflict with humans or with endangered species, may not achieve management goals if animal movement is not considered. In populations with emigration and immigration, lethal control may induce compensatory immigration, if the source of attraction remains unchanged. Within the Columbia River Basin (Washington, U.S.A.), avian predators forage at dams because dams tend to reduce rates of emigration of juvenile salmonids (Oncorhynchus spp.), artificially concentrating these prey. We used differences in fatty acid profiles between Caspian Terns (Hydroprogne caspia) at coastal and inland breeding colonies and terns culled by a lethal control program at a mid-Columbia River dam to infer dispersal patterns. We modeled the rate of loss of fatty acid biomarkers, which are fatty acids that can be traced to a single prey species or groups of species, to infer whether and when terns foraging at dams had emigrated from the coast. Nonmetric multidimensional scaling showed that coastal terns had high levels of C(20) and C(22) monounsaturated fatty acids, whereas fatty acids of inland breeders were high in C18:3n3, C20:4n6, and C22:5n3. Models of the rate of loss of fatty acid showed that approximately 60% of the terns collected at Rock Island Dam were unlikely to have bred successfully at local (inland) sites, suggesting that terns foraging at dams come from an extensive area. Fatty acid biomarkers may provide accurate information about patterns of dispersal in animal populations and may be extremely valuable in cases where populations differ demonstrably in prey base.

Wind, waves, and wing loading: morphological specialization may limit range expansion of endangered albatrosses.

Among the varied adaptations for avian flight, the morphological traits allowing large-bodied albatrosses to capitalize on wind and wave energy for efficient long-distance flight are unparalleled. Consequently, the biogeographic distribution of most albatrosses is limited to the windiest oceanic regions on earth; however, exceptions exist. Species breeding in the North and Central Pacific Ocean (Phoebastria spp.) inhabit regions of lower wind speed and wave height than southern hemisphere genera, and have large intrageneric variation in body size and aerodynamic performance. Here, we test the hypothesis that regional wind and wave regimes explain observed differences in Phoebastria albatross morphology and we compare their aerodynamic performance to representatives from the other three genera of this globally distributed avian family. In the North and Central Pacific, two species (short-tailed P. albatrus and waved P. irrorata) are markedly larger, yet have the smallest breeding ranges near highly productive coastal upwelling systems. Short-tailed albatrosses, however, have 60% higher wing loading (weight per area of lift) compared to waved albatrosses. Indeed, calculated aerodynamic performance of waved albatrosses, the only tropical albatross species, is more similar to those of their smaller congeners (black-footed P. nigripes and Laysan P. immutabilis), which have relatively low wing loading and much larger foraging ranges that include central oceanic gyres of relatively low productivity. Globally, the aerodynamic performance of short-tailed and waved albatrosses are most anomalous for their body sizes, yet consistent with wind regimes within their breeding season foraging ranges. Our results are the first to integrate global wind and wave patterns with albatross aerodynamics, thereby identifying morphological specialization that may explain limited breeding ranges of two endangered albatross species. These results are further relevant to understanding past and potentially predicting future distributional limits of albatrosses globally, particularly with respect to climate change effects on basin-scale and regional wind fields.

Response of pigeon guillemots to variable abundance of high-lipid and low-lipid prey.

Populations of the pigeon guillemot (Cepphus columba) and other piscivores have been in decline for several decades in the Gulf of Alaska and Bering Sea, and a decline in abundance of lipid-rich schooling fishes is hypothesized as the major cause. We tested this hypothesis by studying the breeding biology of pigeon guillemots during 1995-1999 while simultaneously measuring prey abundance with beach seines and bottom trawls. Our study area (Kachemak Bay, Alaska) comprises two oceanographically distinct areas. Populations of a lipid-rich schooling fish, Pacific sand lance (Ammodytes hexapterus), were higher in the warmer Inner Bay than in the colder Outer Bay, and sand lance abundance was higher during warm years. Populations of low-lipid content demersal fishes were similar between areas. Chick survival to age 15 days was 47% higher in the Inner Bay (high-lipid diet) than in the Outer Bay (low-lipid diet), and estimated reproductive success (chicks fledged nest-1) was 62% higher in the Inner Bay than in the Outer Bay. Chick provisioning rate (kJ chick-1 h-1) increased with the proportion of sand lance in the diet (r 2=0.21), as did growth rate (g day-1) of younger (beta) chicks in two-chick broods (r 2=0.14). Pigeon guillemots in the Inner Bay switched to demersal prey during years of below-average sand lance abundance, and these birds reacted to 38-fold interannual changes in sand lance abundance with reductions in beta chick growth rates, with no decline in beta chick survival. In contrast, the proportion of nests experiencing brood reduction in the Outer Bay (demersal diet) increased >300% during years of below-average demersal abundance, although demersal fish abundance varied only 4-fold among years. Our results support the hypothesis that recovery of pigeon guillemot populations from the effects of the Exxon Valdez oil spill is limited by availability of lipid-rich prey.