Paul W. Collins

Pleistocene to historic shifts in bald eagle diets on the Channel Islands, California

Studies of current interactions among species, their prey, and environmental factors are essential for mitigating immediate threats to population viability, but the true range of behavioral and ecological flexibility can be determined only through research on deeper timescales. Ecological data spanning centuries to millennia provide important contextual information for long-term management strategies, especially for species that now are living in relict populations. Here we use a variety of methods to reconstruct bald eagle diets and local abundance of their potential prey on the Channel Islands from the late Pleistocene to the time when the last breeding pairs disappeared from the islands in the mid-20th century. Faunal and isotopic analysis of bald eagles shows that seabirds were important prey for immature/adult eagles for millennia before the eagles’ local extirpation. In historic times (A.D. 1850–1950), however, isotopic and faunal data show that breeding bald eagles provisioned their chicks with introduced ungulates (e.g., sheep), which were locally present in high densities. Today, bald eagles are the focus of an extensive conservation program designed to restore a stable breeding population to the Channel Islands, but native and nonnative prey sources that were important for bald eagles in the past are either diminished (e.g., seabirds) or have been eradicated (e.g., introduced ungulates). In the absence of sufficient resources, a growing bald eagle population on the Channel Islands could expand its prey base to include carrion from local pinniped colonies, exert predation pressure on a recovering seabird population, and possibly prey on endangered island foxes.

Mitochondrial genomes suggest rapid evolution of dwarf California Channel Islands foxes (Urocyon littoralis).

Island endemics are typically differentiated from their mainland progenitors in behavior, morphology, and genetics, often resulting from long-term evolutionary change. To examine mechanisms for the origins of island endemism, we present a phylogeographic analysis of whole mitochondrial genomes from the endangered island fox (Urocyon littoralis), endemic to California’s Channel Islands, and mainland gray foxes (U. cinereoargenteus). Previous genetic studies suggested that foxes first appeared on the islands >16,000 years ago, before human arrival (~13,000 cal BP), while archaeological and paleontological data supported a colonization >7000 cal BP. Our results are consistent with initial fox colonization of the northern islands probably by rafting or human introduction ~9200–7100 years ago, followed quickly by human translocation of foxes from the northern to southern Channel Islands. Mitogenomes indicate that island foxes are monophyletic and most closely related to gray foxes from northern California that likely experienced a Holocene climate-induced range shift. Our data document rapid morphological evolution of island foxes (in ~2000 years or less). Despite evidence for bottlenecks, island foxes have generated and maintained multiple mitochondrial haplotypes. This study highlights the intertwined evolutionary history of island foxes and humans, and illustrates a new approach for investigating the evolutionary histories of other island endemics.

Proactive Conservation Management of an Island-endemic Bird Species in the Face of Global Change

Biodiversity conservation in an era of global change and scarce funding benefits from approaches that simultaneously solve multiple problems. Here, we discuss conservation management of the island scrub-jay (Aphelocoma insularis), the only island-endemic passerine species in the continental United States, which is currently restricted to 250-square-kilometer Santa Cruz Island, California. Although the species is not listed as threatened by state or federal agencies, its viability is nonetheless threatened on multiple fronts. We discuss management actions that could reduce extinction risk, including vaccination, captive propagation, biosecurity measures, and establishing a second free-living population on a neighboring island. Establishing a second population on Santa Rosa Island may have the added benefit of accelerating the restoration and enhancing the resilience of that islands currently highly degraded ecosystem. The proactive management framework for island scrub-jays presented here illustrates how strategies for species protection, ecosystem restoration, and adaptation to and mitigation of climate change can converge into an integrated solution.

Does the Order of Invasive Species Removal Matter? The Case of the Eagle and the Pig

Background Invasive species are recognized as a primary driver of native species endangerment and their removal is often a key component of a conservation strategy. Removing invasive species is not always a straightforward task, however, especially when they interact with other species in complex ways to negatively influence native species. Because unintended consequences may arise if all invasive species cannot be removed simultaneously, the order of their removal is of paramount importance to ecological restoration. In the mid-1990s, three subspecies of the island fox Urocyon littoralis were driven to near extinction on the northern California Channel Islands owing to heightened predation by golden eagles Aquila chrysaetos. Eagles were lured to the islands by an abundant supply of feral pigs Sus scrofa and through the process of apparent competition pigs indirectly facilitated the decline in foxes. As a consequence, both pigs and eagles had to be removed to recover the critically endangered fox. Complete removal of pigs was problematic: removing pigs first could force eagles to concentrate on the remaining foxes, increasing their probability of extinction. Removing eagles first was difficult: eagles are not easily captured and lethal removal was politically distasteful. Methodology/Principal Findings Using prey remains collected from eagle nests both before and after the eradication of pigs, we show that one pair of eagles that eluded capture did indeed focus more on foxes. These results support the premise that if the threat of eagle predation had not been mitigated prior to pig removal, fox extinction would have been a more likely outcome. Conclusions/Significance If complete eradication of all interacting invasive species is not possible, the order in which they are removed requires careful consideration. If overlooked, unexpected consequences may result that could impede restoration.

Next-generation sequencing workflow for assembly of nonmodel mitogenomes exemplified with North Pacific albatrosses (Phoebastria spp.)

Use of complete mitochondrial genomes (mitogenomes) can greatly increase the resolution achievable in phylogeographic and historical demographic studies. Using next‐generation sequencing methods, it is now feasible to efficiently sequence mitogenomes of large numbers of individuals once a reference mitogenome is available. However, assembling the initial mitogenomes of nonmodel organisms can present challenges, for example, in birds, where mtDNA is often subject to gene rearrangements and duplications. We developed a workflow based on Illumina paired‐end, whole‐genome shotgun sequencing, which we used to generate complete 19‐kilobase mitogenomes for each of three species of North Pacific albatross, a group of birds known to carry a tandem duplication. Although this duplication had been described previously, our procedure did not depend on this prior knowledge, nor did it require a closely related reference mitogenome (e.g. a mammalian mitogenome was sufficient). We employed an iterative process including de novo assembly, reference‐guided assembly and gap closing, which enabled us to detect duplications, determine gene order and identify sequence for primer positioning to resolve any mitogenome ambiguity (via minimal targeted Sanger sequencing). We present full mtDNA annotations, including 22 tRNAs, 2 rRNAs, 13 protein‐coding genes, a control region and a duplicated feature for all three species. Pairwise comparisons supported previous hypotheses regarding the phylogenetic relationships within this group and occurrence of a shared tandem duplication. The resulting mitogenome sequences will enable rapid, high‐throughput NGS mitogenome sequencing of North Pacific albatrosses via direct reference‐guided assembly. Moreover, our approach to assembling mitogenomes should be applicable to any taxon.

Foraging ecology of a reintroduced population of breeding Bald Eagles on the Channel Islands, California, USA, inferred from prey remains and stable isotope analysis

ABSTRACT Successful management of reintroduced populations requires recognizing that ecological conditions may have changed between extirpation and reintroduction. For example, characterizing dietary patterns of generalist apex predators in the past and present can help to define how their functional role may change as translocated populations grow. We identified prey remains collected from Bald Eagle (Haliaeetus leucocephalus) nests and used carbon (δ13C) and nitrogen (δ15N) stable isotope analysis to quantify diet composition of the recently reintroduced Bald Eagle population on the Channel Islands off southern California, USA. We collected >6,000 prey items from recently occupied nests on Santa Catalina, Santa Rosa, Santa Cruz, and Anacapa islands in 2010 and 2011. Prey identification and stable isotope analysis yielded similar results and showed that eagles on Santa Catalina Island consumed a high proportion (~60%) of marine fish and a lower proportion (25–30%) of seabirds, while their counterparts on the Northern Channel Islands consumed equal proportions (~40–45%) of these prey types. Terrestrial resource use was low with the exception of eagles from one nest on Santa Catalina Island, where eagles primarily consumed ground squirrels and freshwater fish. We suggest that a combination of natural and anthropogenic factors is responsible for the interisland differences in Bald Eagle diet. Bald Eagle interactions with a robust recreational fishery off Santa Catalina Island may enhance access to fish species that are not available to eagles on the Northern Channel Islands, where the availability of breeding seabirds is far greater. The proportion of seabirds consumed by eagles on the Northern Channel Islands today is similar to that consumed by eagles from this region historically and prehistorically. This suggests that the restoration of breeding seabirds on the Channel Islands will benefit the long-term viability of eagle populations in the northern archipelago.

Late Quaternary Chorus Frog (Pseudacris) from the Channel Islands, California

Abstract Fossil and subfossil remains of the vertebrate faunas from the northern Channel Islands, southern California, have been studied for many decades. Continued interest has focused on skeletal remains of birds, rodents, and mammoths from archaeological and paleontological localities, but considerably less attention has been placed on the detailed description of the herpetofauna (salamanders, anurans [frogs and toads], lizards, and snakes) on the Channel Islands. We present descriptions of an ilium of an anuran from Santa Rosa Island (Larramendy North; radiocarbon dating at least 13,393 calibrated years ago) and two tibiofibulae San Miguel Island (Daisy Cave) dating from earliest and middle late Holocene layers. We identify the fossil ilium as Pseudacris sp. (chorus frog): 1) it is the lowest level that skeletal morphology permits us to attempt, 2) realizing that it appears morphologically closest to P. regilla, and 3) yet realizing that not all species of Pseudacris and Hyla have been directly compared or are understood. The extant amphibian fauna on these islands is depauperate. The remains presented here represent the first description of a fossil anuran from the northern Channel Islands. It is now understood that a chorus frog lived on glacial-age Santarosae Island, yet it is not understood when its distribution was reduced to just the present two largest islands, Santa Rosa and Santa Cruz.

Reintroduction of Historically Extirpated Taxa on the California Channel Islands

Abstract. Most invasive alien vertebrate populations on the Channel Islands of California have been eradicated over the past 30 years. Unfortunately, removal of these introduced herbivores or predators came too late for some native flora and fauna, and numerous populations are now extinct. Here, we describe a systematic approach to reintroducing extirpated native taxa as a means for rebuilding natural communities and enhancing the resiliency of island ecosystems. Reintroduction efforts typically focus on a single species or site. In contrast, we propose that if reintroduction is a shared conservation goal of managers across the islands, the associated planning, implementation, and monitoring should be conducted as a cross-island initiative for the archipelago. A coordinated effort based on best practices in reintroduction biology could accrue programmatic efficiencies and economies of scale, more quickly advance ecosystem and species conservation goals, and create unique opportunities to test hypotheses in basic and applied ecology and evolution. The philosophical and technical approaches developed through this program may apply to other island and mainland systems and could be adapted to develop conservation strategies for species that may be candidates for assisted colonization in the face of climate change.

Development and characterization of 15 polymorphic microsatellite markers for North Pacific albatrosses using paired-end Illumina shotgun sequencing

All three species of North Pacific albatross are vulnerable or near threatened (IUCN 2013) yet microsatellite markers to study their population characteristics are lacking. We employed 250-bp paired-end whole genome shotgun sequencing on an Illumina MiSeq platform to discover microsatellite markers. We selected 16 candidate loci for screening in 36 Black-footed (Phoebastria nigripes), 12 Laysan (P. immutabilis), and 3 Short-tailed (P. albatrus) albatrosses from which we characterized 15 markers.