Christina L. Boser

Adaptive divergence despite strong genetic drift: genomic analysis of the evolutionary mechanisms causing genetic differentiation in the island fox (Urocyon littoralis)

The evolutionary mechanisms generating the tremendous biodiversity of islands have long fascinated evolutionary biologists. Genetic drift and divergent selection are predicted to be strong on islands and both could drive population divergence and speciation. Alternatively, strong genetic drift may preclude adaptation. We conducted a genomic analysis to test the roles of genetic drift and divergent selection in causing genetic differentiation among populations of the island fox (Urocyon littoralis). This species consists of six subspecies, each of which occupies a different California Channel Island. Analysis of 5293 SNP loci generated using Restriction‐site Associated DNA (RAD) sequencing found support for genetic drift as the dominant evolutionary mechanism driving population divergence among island fox populations. In particular, populations had exceptionally low genetic variation, small Ne (range = 2.1–89.7; median = 19.4), and significant genetic signatures of bottlenecks. Moreover, islands with the lowest genetic variation (and, by inference, the strongest historical genetic drift) were most genetically differentiated from mainland grey foxes, and vice versa, indicating genetic drift drives genome‐wide divergence. Nonetheless, outlier tests identified 3.6–6.6% of loci as high FST outliers, suggesting that despite strong genetic drift, divergent selection contributes to population divergence. Patterns of similarity among populations based on high FST outliers mirrored patterns based on morphology, providing additional evidence that outliers reflect adaptive divergence. Extremely low genetic variation and small Ne in some island fox populations, particularly on San Nicolas Island, suggest that they may be vulnerable to fixation of deleterious alleles, decreased fitness and reduced adaptive potential.

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.

Floral visitation by the Argentine ant reduces bee visitation and plant seed set

Ants often visit flowers, but have only seldom been documented to provide effective pollination services. Floral visitation by ants can also compromise plant reproduction in situations where ants interfere with more effective pollinators. Introduced ants may be especially likely to reduce plant reproductive success through floral visitation, but existing experimental studies have found little support for this hypothesis. Here, we combine experimental and observational approaches to examine the importance of floral visitation by the nonnative Argentine ant (Linepithema humile) on plant species native to Santa Cruz Island, California, USA. First, we determine how L. humile affects floral visitor diversity, bee visitation rates, and levels of pollen limitation for the common, focal plant species island morning glory (Calystegia macrostegia ssp. macrostegia). Second, we assess the broader ecological consequences of floral visitation by L. humile by comparing floral visitation networks between invaded and uninvaded sites. The Argentine ant and native ants both visited island morning glory flowers, but L. humile was much more likely to behave aggressively towards other floral visitors and to be the sole floral occupant. The presence of L. humile in morning glory flowers reduced floral visitor diversity, decreased rates of bee visitation, and increased levels of pollen limitation. Network comparisons between invaded and uninvaded. sites revealed differences in both network structure and species-level attributes. In. invaded sites, floral visitors were observed on fewer plant species, ants had a higher per-plant interaction strength relative to that of other visitors, and interaction strengths between bees and plants were weaker. These results illustrate that introduced ants can negatively affect plant reproduction and potentially disrupt pollination services at an ecosystem scale.

Argentine Ant Management in Conservation Areas: Results of a Pilot Study

Abstract. Argentine ants (Linepithema humile) have invaded many areas of conservation concern, including half of the California Channel Islands. On Santa Cruz Island, the species has invaded approximately 2% of the island, and the infestations are expanding. Argentine ants displace many other invertebrates, and their expansion throughout the island could lead to the extirpation of native invertebrate species and the disruption of key ecological processes (e.g., plant-pollinator interactions and seed dispersal). We describe a treatment protocol to manage or eliminate Argentine ants on Santa Cruz Island developed by The Nature Conservancy and the National Park Service, in collaboration with academic and pest control specialists. We combined low-concentration toxicant baits with efficient dispersal methods to treat landscape-scale Argentine ant infestations in rugged terrain and dense vegetation with minimal impact to nontarget species. From May to October 2012, we applied our baiting protocol within 2 study sites, totaling 7.8 ha on Santa Cruz Island. In May 2013, one year post treatment, we observed >99% reduction in Argentine ant activity in treatment plots compared to untreated plots, using 2 different monitoring techniques. While further testing and monitoring is needed, these results suggest this protocol may be an effective tool to eliminate Argentine ant infestations from this type of habitat and terrain.

Laboratory and Field Evaluations of Polyacrylamide Hydrogel Baits Against Argentine Ants (Hymenoptera: Formicidae)

ABSTRACT The development of effective baits to control the Argentine ant, Linepithema humile (Mayr), has been problematic because foragers prefer sweet liquids, while many toxicants are insoluble in water and liquid baits are generally difficult to deliver. The incorporation of thiamethoxam and sucrose solutions into a water-absorbing polyacrylamide hydrogel provides a unique and novel carrier and method of application for liquid baits. Formulations of thiamethoxam affected the size of the hydrogels, and sucrose solutions containing 0.0003% technical thiamethoxam provided hydrogels as large as those made with 25% sucrose solution or deionized water. Concentrations of thiamethoxam as low as 0.000075% in the hydrogels provided 50% kill of workers within 3 d in a laboratory setting. In small colony studies, baiting with 0.00015 and 0.000075% thiamethoxam hydrogels provided 100% mortality of workers and queens within 8 d. An enzyme-linked immunosorbent assay indicated that thiamethoxam was absorbed into the interior of the polyacrylamide matrix. The water loss rates of the hydrogels were dependent upon the relative humidity. Polyacrylamide hydrogels with >50% water loss were less attractive to ants. Field studies in highly infested areas indicated that concentrations of 0.0006 or 0.0018% thiamethoxam were more effective than 0.00015%. Hydrogels may provide a cost-effective alternative to providing aqueous baits to control Argentine ants.

Testing the effects of ant invasions on non-ant arthropods with high-resolution taxonomic data

Invasions give rise to a wide range of ecological effects. Many invasions proceed without noticeable impacts on the resident biota, whereas others shift species composition and even alter ecosystem function. Ant invasions generate a broad spectrum of ecological effects, but controversy surrounds the extent of these impacts, especially with regard to how other arthropods are affected. This uncertainty in part results from the widespread use of low-resolution taxonomic data, which can mask the presence of other introduced species and make it difficult to isolate the effects of ant invasions on native species. Here, we use high-resolution taxonomic data to examine the effects of Argentine ant invasions on arthropods on Santa Cruz Island, California. We sampled arthropods in eight pairs of invaded and uninvaded plots and then collaborated with taxonomic experts to identify taxa in four focal groups: spiders, bark lice, beetles, and ants. Spiders, bark lice, and beetles made up ~40% of the 9868 non-ant arthropod individuals sampled; the majority of focal group arthropods were putatively native taxa. Although our results indicate strong negative effects of the Argentine ant on native ants, as is well documented, invaded and uninvaded plots did not differ with respect to the richness, abundance, or species composition of spiders, bark lice, and beetles. One common, introduced species of bark louse was more common in uninvaded plots than in invaded plots, and including this species into our analyses changed the relationship between bark louse richness vs. L. humile abundance from no relationship to a significant negative relationship. This case illustrates how failure to differentiate native and introduced taxa can lead to erroneous conclusions about the effects of ant invasions. Our results caution against unqualified assertions about the effects of ant invasions on non-ant arthropods, and more generally demonstrate that accurate assessments of invasion impacts depend on adequate information about species identity.

On the Fast Track to Recovery: Island Foxes on the Northern Channel Islands

Abstract. The island fox (Urocyon littoralis) represents an unusual case of a species that achieved virtual recovery a mere 15 years after population declines were first discovered. Island fox subspecies on San Miguel, Santa Rosa, and Santa Cruz islands declined precipitously in the mid-1990s due to predation by Golden Eagles (Aquila chrysaetos), which had not historically bred on the islands. In 2008, a 10-year period of recovery action implementation ended. The recovery program had included captive breeding and reintroduction of island foxes and capture and relocation of Golden Eagles. Free-ranging fox populations have been monitored to assess recovery of each subspecies and to detect potential threats of disease and predation. Monitoring included (1) annual grid trapping to allow estimation of annual population size via capture-mark-recapture methods and (2) systematic surveillance of radio-collared foxes to allow estimation of mortality rates and causes. A comprehensive demographic modeling effort produced a population recovery tool that uses adult mortality and population size estimates from the monitoring programs to estimate extinction risks for each fox population. The tool allows managers to assess when threats are sufficiently mitigated to consider populations acceptably safe from extinction. Population monitoring indicates that island foxes on the northern Channel Islands have increased up to 30-fold from population lows and that annual survival has been 90% or better in most years. The San Miguel and Santa Cruz subspecies have approached or reached predecline population levels, and application of the recovery tool indicates they will be biologically recovered by 2013. Biological recovery of the Santa Rosa subspecies, hindered by predation which caused lower survival in 2010, will occur by 2017.

Strategies for Biosecurity on a Nearshore Island in California

Abstract. Islands provide refuge for many rare and endemic species but are especially vulnerable to invasion by nonnative species. Invasive alien species are a major factor in the imperilment and extinction of island biota. Biosecurity protocols are designed to prevent or quickly detect the transport of harmful nonnative species, with the goal of eliminating the high economic cost of invasive species removal and the biological cost of damage caused by nonnative organisms. Effective biosecurity protocols require a balanced approach to on-island monitoring, off-island surveillance and prevention practices, rapid response, and educational outreach. Here we use the biosecurity program on Santa Cruz Island, California, to illustrate how risk evaluation, program priorities, and funding constraints intersect to define programmatic scope. Santa Cruz Island land managers have chosen to invest in early detection programs such as remote camera trapping, off-island prevention and education, and rapid-response planning for rats and in on-island biosecurity to prevent the spread of the most harmful plant species. We suggest that biosecurity efforts will be more effective—as well as cost effective—as an archipelago-wide initiative than as a single-island program. A newly formed collaboration with managers of other California Islands is designed to enhance visibility of the biosecurity initiative and attract new funding sources. With the economy afforded by collaboration, we will expand our program and prioritize annual audits, augment educational programs, measure project success, and increase compliance with and effectiveness of biosecurity protocols.

Protocols for Argentine ant eradication in conservation areas

The Argentine ant (Linepithema humile) is a widespread, abundant and ecologically disruptive invader that is present throughout major portions of coastal California and on half of the California Channel Islands. On Santa Cruz Island, the Argentine ant had invaded about 2% of the islands area in four distinct locations as of 2012. Given the negative ecological effects resulting from Argentine ant invasions, we sought to develop a cost‐effective method of eradication. Here, we describe the results of large‐scale, field‐tested methods for Argentine ant eradication and post‐treatment detection. Our eradication protocol employs a novel toxicant‐delivery system: an aqueous solution of sucrose and 6 ppm of thiamethoxam mixed with hydrating polyacrylamide beads. Ants feed on the solution present on the beads surface for about 24 h after which time bead dehydration prevents feeding. We distributed hydrated beads by helicopter over 74 ha of infested areas plus a 50‐m buffer on 14 occasions between June 2013 and September 2014. Treatments reduced Argentine ant activity to subdetectable levels within four months. In 2014, we conducted a high‐intensity detection protocol using lures (n = 55 363) in areas treated in 2013. This effort did not detect Argentine ants. In 2015, we conducted a medium‐intensity detection protocol using lures (n = 2250) in areas treated in 2013 and 2014 but not searched in 2014; this sampling effort did not detect Argentine ant activity except for a single remnant infestation (c. 0.3 ha in area), which was retreated in 2015. The cost of treatments was approximately

Aphid‐tending ants on introduced fennel: can resources derived from non‐native plants alter the trophic position of higher‐order consumers?

1400 per ha; this cost is comparable to other ant eradication efforts. The cost of our preferred detection method, which used lures spaced every 10 m, was