Population structure of loggerhead shrikes in the California Channel Islands

The loggerhead shrike (Lanius ludovicianus), a songbird that hunts like a small raptor, maintains breeding populations on seven of the eight California Channel Islands. One of the two subspecies, L. l. anthonyi, was described as having breeding populations on six of the islands while a second subspecies, L. l. mearnsi, was described as being endemic to San Clemente Island. Previous genetic studies have demonstrated that the San Clemente Island loggerhead shrike is well differentiated genetically from both L. l. anthonyi and mainland populations, despite the fact that birds from outside the population are regular visitors to the island. Those studies, however, did not include a comparison between San Clemente Island shrikes and the breeding population on Santa Catalina Island, the closest island to San Clemente. Here we use mitochondrial control region sequences and nuclear microsatellites to investigate the population structure of loggerhead shrikes in the Channel Islands. We confirm the genetic distinctiveness of the San Clemente Island loggerhead shrike and, using Bayesian clustering analysis, demonstrate the presence and infer the source of the nonbreeding visitors. Our results indicate that Channel Island loggerhead shrikes comprise three distinct genetic clusters that inhabit: (i) San Clemente Island, (ii) Santa Catalina Island and (iii) the Northern Channel Islands and nearby mainland; they do not support a recent suggestion that all Channel Island loggerhead shrikes should be managed as a single entity.     

Typological thinking and the conservation of subspecies: the case of the San Clemente Island loggerhead shrike

Abstract.  Hybridization with closely related taxa poses a significant threat to endangered subspecies (e.g. outbreeding depression, inbreeding) and confounds efforts to manage and conserve these taxa through a loss of taxonomic identity, in part because of the practical necessity of defining subspecies in a typological manner. We examined nine morphological characters in 167 post-juvenile museum specimens to determine if loggerhead shrikes Lanius ludovicianus Linnaeus 1766 on San Clemente Island (off the coast of California) remain diagnosable as L. l. mearnsi Ridgway (1903); an island endemic listed as endangered by the United States Fish and Wildlife Service. Four recent shrike specimens from the island were compared to historical specimens using a bivariate scatter plot and a discriminant function (the latter was used to classify recent specimens post hoc). The few recent specimens were not diagnosable as L. l. mearnsi , but instead appear to be intergrades between L. l. mearnsi and L. l. anthonyi Mearns 1898 (the subspecies endemic to Santa Cruz, Santa Catalina, Santa Rosa and Anacapa islands), and are perhaps closer to pure anthonyi . Our data and the species' natural history and distribution suggest that shrikes currently on San Clemente Island are the result of genetic 'swamping' of mearnsi by anthonyi . Under a necessarily typological definition of a subspecies, it is evident that mearnsi is probably no longer diagnosable. However, we conclude that protection of the entire Channel Islands population of the loggerhead shrike would be the best management strategy, as the species has declined drastically throughout the islands.     

Microsatellite variation and microevolution in the critically endangered San Clemente Island loggerhead shrike (Lanius ludovicianus mearnsi)

Polymorphic nuclear microsatellite loci were used to characterize genetic variation in contemporary and historic populations of the San Clemente Island loggerhead shrike (Lanius ludovicianus mearnsi), an endangered bird with a current population of 30 individuals that is endemic to to one of the California Channel Islands. We also compared the population of the shrike with two contemporary populations of the still abundant subspecies, L. l. gambeli, which live 120 km away on the adjacent mainland. The current population of L. l. mearnsi has 60 per cent of the genetic variation of the mainland shrike populations and is strongly differentiated from them. Comparison of living birds with 19 birds collected in 1915 shows that most of the variation within the island population was lost before the recent 90 per cent decline in population size, and the 20 per cent decrease in variation this century is probably attributable to genetic drift. Mitochondrial DNA control region sequence data from 80 year old specimens show that there may have been limited introgression to L. l. mearnsi, this century, from another island subspecies, L. l. anthonyi, found in the northern Channel Islands. Today, gene flow between L. l. mearnsi and mainland L. l. gambel is very low, even though a few mainland birds visit the island annually. The island subspecies population has evolved sufficient genetic independence to justify ongoing conservation efforts to counter demographic collapse and genetic erosion; the course of genetic erosion can now be monitored non-invasively, as demonstrated by this study, based on DNA amplified from feathers.     

Genetic differences between the endangered San Clemente Island loggerhead shrike Lanius ludovicianus mearnsi and two neighbouring subspecies demonstrated by mtDNA control region and cytochrome b sequence variation

We investigated mtDNA sequence variation in five populations of the loggerhead shrike Lanius ludovicianus , representing four subspecies, including the San Clemente loggerhead shrike L. l. mearnsi , a critically endangered California Channel Island endemic. Variability in 200 bp of control region and 200 bp of cytochrome b was extremely low, and defined four haplotypes. Strong structure was apparent among all three southern Californian subspecies, including L. l. mearnsi , with one haplotype predominating in each subspecies. Although potential levels of gene flow between L. l. mearnsi and neighbouring populations are low, mtDNA data support field observations that some shrikes visit the island during winter but do not stay to breed, and suggest that these birds come from the mainland. The similarity in haplotypes between populations from Saskatchewan, Canada and those in southern California suggests post-glacial northern range expansion of the species. Our results confirm the evolutionary distinctiveness of L. l. mearnsi and justify continuing efforts for its conservation.     

Genetic Divergence of an Avian Endemic on the Californian Channel Islands

The Californian Channel Islands are near–shore islands with high levels of endemism, but extensive habitat loss has contributed to the decline or extinction of several endemic taxa. A key parameter for understanding patterns of endemism and demography in island populations is the magnitude of inter–island dispersal. This paper estimates the extent of migration and genetic differentiation in three extant and two extinct populations of Channel Island song sparrows (Melospiza melodia graminea). Inter–island differentiation was substantial (G''''_ST: 0.14–0.37), with San Miguel Island having the highest genetic divergence and lowest migration rates. Santa Rosa and Santa Cruz Island populations were less diverged with higher migration rates. Genetic signals of past population declines were detected in all of the extant populations. The Channel Island populations were significantly diverged from mainland populations of M. m. heermanni (G''''_ST: 0.30–0.64). Ten mtDNA haplotypes were recovered across the extant and extinct Channel Island population samples. Two of the ten haplotypes were shared between the Northern and Southern Channel Islands, with one of these haplotypes being detected on the Californian mainland. Our results suggest that there is little contemporary migration between islands, consistent with early explanations of avian biogeography in the Channel Islands, and that song sparrow populations on the northern Channel Islands are demographically independent.     

The population genetics of nonmigratory Allen’s Hummingbird (Selasphorus sasin sedentarius) following a recent mainland colonization

Allen''s Hummingbird comprises two subspecies, one migratory (Selasphorus sasin sasin) and one nonmigratory (S. s. sedentarius). The nonmigratory subspecies, previously endemic to the California Channel Islands, apparently colonized the California mainland on the Palos Verdes Peninsula some time before 1970 and now breeds throughout coastal southern California. We sequenced and compared populations of mainland nonmigratory Allen''s Hummingbird to Channel Island populations from Santa Catalina, San Clemente, and Santa Cruz Island. We found no evidence of founder effects on the mainland population. Values of nucleotide diversity on the mainland were higher than on the Channel Islands. There were low levels of divergence between the Channel Islands and the mainland, and Santa Cruz Island was the most genetically distinct. Ecological niche models showed that rainfall and temperature variables on the Channel Islands are similar in the Los Angeles basin and predicted continued expansion of nonmigratory Allen''s Hummingbird north along the coast and inland. We also reviewed previous genetic studies of vertebrate species found on the Channel Islands and mainland and showed that broad conclusions regarding island–mainland patterns remain elusive. Challenges include the idiosyncratic nature of colonization itself as well as the lack of a comprehensive approach that incorporates similar markers and sampling strategies across taxa, which, within the context of a comparative study of island–mainland relationships, may lead to inconsistent results.     

Epidemic Development and Virulence in 1995–1998 of Puccinia coronata, a Potential Biocontrol Agent of Wild Oats on San Clemente Island

The biology of islands differs from that of large land masses in having less complex ecosystems. Introduced exotic weeds are often a major threat to fragile island ecosystems because of their expansion into habitats previously occupied by endemic species. San Clemente Island, 120 km off the California coastline, is an example of this process in which numerous exotic weed species have been introduced and some are endangering the native flora. Crown rust of oats caused by Puccinia coronata f.sp. avenae was investigated as a potential biocontrol agent against two wild oat species, Avena barbata and Avena fatua, introduced on San Clemente Island. Epidemiology and virulence of this rust were studied. The island was surveyed from 1995 to 1998 for occurrence of P. coronata on wild oats. Wild oats were found sprouting in the northern part of the island shortly after autumn rainfall and subsequently covered the main grasslands of the island. The rust also appeared first on the northern part of the island and progressively spread south. However, disease severities in the south were considerably lower than those in the north. Diverse virulence types, although related to Californian and Mexican forms, were detected among the isolates. The potential use of P. coronata as an augmentative biocontrol agent for wild oat species on San Clemente Island is discussed.     

Host islands within the California Northern Channel Islands create fine-scale genetic structure in two sympatric species of the symbiotic ectomycorrhizal fungus Rhizopogon

We have examined fine-scale genetic structure of the symbiotic ectomycorrhizal fungi Rhizopogon occidentalis and R. vulgaris on two of the California Channel Islands using five and six microsatellite loci, respectively. Both Rhizopogon species are sympatric on Santa Cruz and Santa Rosa Islands and are ectomycorrhizal with bishop pine (Pinus muricata) on both islands or Santa Rosa Island Torrey pine (P. torreyana ssp. insularis) on Santa Rosa. The combination of disjunct pine host distributions and geographic barriers within and among the islands have created highly structured Rhizopogon populations over very short distances (8.5 km on Santa Cruz Island; F(ST) = 0.258, F(ST) = 0.056, R. occidentalis and R. vulgaris, respectively). Both species show similar patterns of genetic differentiation as a result of limited dispersal between host populations as revealed by a significant isolation by distance relationship (r = 0.69, P < 0.04; r = 0.93, P < 0.001, R. occidentalis and R. vulgaris, respectively) and Bayesian clustering analyses, and is most likely a function of the small foraging range of the few mammals that disperse Rhizopogon on these islands and the enormous spore bank characteristic of Rhizopogon species.     

Biochemical and hematologic reference intervals for the endangered island fox (Urocyon littoralis)

Hematologic and serum biochemical data collected must be interpreted by comparison with normal reference intervals generated from healthy animals, within a similar population, because many blood parameters are influenced by diet, environment, and stress. Species-specific reference intervals for the endangered island fox (Urocyon littoralis) are not available. We reviewed hematology and serum biochemistry panels from 280 island foxes sampled from 1999-2008 and established normal reference intervals from clinically healthy foxes using a nonparametric approach. Blood parameters were analyzed for differences in age, sex, island of origin, and captivity status. Alkaline phosphatase, alanine aminotransferase, aspartate aminotransferase, and creatine kinase activities, as well as calcium and phosphorus concentrations, were significantly higher in juveniles than in adults, but total protein and globulin concentration was lower for juveniles than for adults. Lymphocyte and eosinophil counts, and blood urea nitrogen (BUN) concentration, in foxes from the northern Channel islands of California, USA (Santa Cruz, Santa Rosa, and San Miguel) were higher when compared with foxes from Santa Catalina Island to the south. Higher lymphocyte and eosinophil numbers in the northern island foxes may be associated with increased levels of parasitism on the northern islands. Differences in BUN concentration in both free-ranging and captive foxes may reflect dietary differences among islands. Although aggressive conservation programs have been enacted, island foxes are still susceptible to infectious and neoplastic diseases and, potentially, to toxins. Island fox species-specific reference intervals will enable managers and veterinarians to better care for sick and injured foxes and will contribute to future population health monitoring.     

Predicting release success of captive‐reared loggerhead shrikes (Lanius ludovicianus) using pre‐release behavior

We assessed whether behavioral markers could be used to evaluate pair compatibility and predict pair bond success of captive‐reared San Clemente loggerhead shrikes (Lanius ludovicianus mearnsi) released into the wild. Potential breeding pairs of shrikes were introduced at the Zoological Society of San Diego's captive‐breeding facility and then moved to release cages located in suitable but unoccupied habitat. Courting pairs were affected negatively by the disturbance of translocation to a new location and generally needed a few days to reinitiate pair bonding in the release enclosures. We separated and returned pairs to captivity when intra‐pair aggression or cessation of all courtship behavior occurred; all other pairs were released into the wild. The rate of nest approaches was the best marker to predict a successful release into the wild (i.e., pairs that remained near the release site and attempted to breed). Additionally, all experienced breeding pairs (i.e., pairs with males and females with prior captive breeding experience) exhibiting nesting behavior were successful, although previous experience alone does not ensure post‐release breeding. Results from this study indicate the importance of assessing behaviors of individuals paired for population augmentation. In using behavioral cues, identifying pairs with a low probability of success is possible, and replacing these pairs with individuals that have a higher likelihood of post‐release success can occur. This strategy will be important to efficiently restore imperiled populations of endangered species while working within temporal and financial constraints. Zoo Biol 0:1–12, 2005. © 2005 Wiley‐Liss, Inc.     

Porotic hyperostosis in a marine-dependent California Indian population

A maize-based iron- and protein-deficient diet is commonly cited as the most important cause of porotic hyperostosis among American Indian agriculturalists. An alternative to this maize dependence hypothesis is suggested by the analysis of 432 crania from the nonagricultural, fish-dependent population of the Channel Island area of southern California. Cribra orbitalia, a form of porotic hyperostosis associated with iron deficiency anemia, is just as common among these fisherpeople, whose diet was rich in iron and essential amino acids, as it is among maize-dependent agriculturalists. Northern Channel Island crania have much more cribra orbitalia than those from the California mainland. The highest incidence is on San Miguel, a small geographically isolated island with a shortage of fresh water and terrestrial resources. The Indians who lived on Santa Cruz, the largest of the northern Channel Islands with the greatest diversity of terrestrial plants and animals, have less cribra orbitalia than those who lived on Santa Rosa or San Miguel Island. This geographical distribution appears to be explained by island-mainland and interisland differences in water contamination, exposure to fish-borne parasites, and nutritional adequacy of the diet. The prevalence of porotic hyperostosis in a population with a heavy dietary dependence on marine resources shows that among prehistoric American Indians, this condition is not always associated with an iron- and protein-deficient diet of cultigens. It seems likely that high nutrient losses associated with diarrheal disease are often more significant in the etiology of porotic hyperostosis than a low dietary intake of essential nutrients.     

110 years of Avipoxvirus in the Galapagos Islands

The role of disease in regulating populations is controversial, partly owing to the absence of good disease records in historic wildlife populations. We examined birds collected in the Galapagos Islands between 1891 and 1906 that are currently held at the California Academy of Sciences and the Zoologisches Staatssammlung Muenchen, including 3973 specimens representing species from two well-studied families of endemic passerine birds: finches and mockingbirds. Beginning with samples collected in 1899, we observed cutaneous lesions consistent with Avipoxvirus on 226 (6.3%) specimens. Histopathology and viral genotyping of 59 candidate tissue samples from six islands showed that 21 (35.6%) were positive for Avipoxvirus, while alternative diagnoses for some of those testing negative by both methods were feather follicle cysts, non-specific dermatitis, or post mortem fungal colonization. Positive specimens were significantly nonrandomly distributed among islands both for mockingbirds (San Cristobal vs. Espanola, Santa Fe and Santa Cruz) and for finches (San Cristobal and Isabela vs. Santa Cruz and Floreana), and overall highly significantly distributed toward islands that were inhabited by humans (San Cristobal, Isabela, Floreana) vs. uninhabited at the time of collection (Santa Cruz, Santa Fe, Espanola), with only one positive individual on an uninhabited island. Eleven of the positive specimens sequenced successfully were identical at four diagnostic sites to the two canarypox variants previously described in contemporary Galapagos passerines. We conclude that this virus was introduced late in 1890's and was dispersed among islands by a variety of mechanisms, including regular human movements among colonized islands. At present, this disease represents an ongoing threat to the birds on the Galapagos Islands.     

Origin and dispersion pathways of guava in the Galapagos Islands inferred through genetics and historical records

Guava (Psidium guajava) is an aggressive invasive plant in the Galapagos Islands. Determining its provenance and genetic diversity could explain its adaptability and spread, and how this relates to past human activities. With this purpose, we analyzed 11 SSR markers in guava individuals from Isabela, Santa Cruz, San Cristobal, and Floreana islands in the Galapagos, as well as from mainland Ecuador. The mainland guava population appeared genetically differentiated from the Galapagos populations, with higher genetic diversity levels found in the former. We consistently found that the Central Highlands region of mainland Ecuador is one of the most likely origins of the Galapagos populations. Moreover, the guavas from Isabela and Floreana show a potential genetic input from southern mainland Ecuador, while the population from San Cristobal would be linked to the coastal mainland regions. Interestingly, the proposed origins for the Galapagos guava coincide with the first human settlings of the archipelago. Through approximate Bayesian computation, we propose a model where San Cristobal was the first island to be colonized by guava from the mainland, and then, it would have spread to Floreana and finally to Santa Cruz; Isabela would have been seeded from Floreana. An independent trajectory could also have contributed to the invasion of Floreana and Isabela. The pathway shown in our model agrees with the human colonization history of the different islands in the Galapagos. Our model, in conjunction with the clustering patterns of the individuals (based on genetic distances), suggests that guava introduction history in the Galapagos archipelago was driven by either a single event or a series of introduction events in rapid succession. We thus show that genetic analyses supported by historical sources can be used to track the arrival and spread of invasive species in novel habitats and the potential role of human activities in such processes.     

Genetic structure of black abalone (Haliotis cracherodii) populations in the California islands and central California coast: Impacts of larval dispersal and decimation from withering syndrome

The genetic structure of black abalone populations in the southern California Islands and central California coast was investigated by protein electrophoresis. Detailed sampling of San Nicolas Island (SN) permitted investigation of microgeographic genetic differentiation among local geomorphological features. In addition, temporal genetic differentiation was assessed by comparing juveniles and adults at three islands, San Miguel (SM), Santa Cruz (SC) and San Nicolas (SN). Mainland and island locations were genetically differentiated based on allele frequency differences and the presence of private alleles in some island populations. Although microgeographic genetic structure among sites on SN was weak and not statistically significant, heterozygosity varied among sites, with diversity decreasing from west to east. In addition, investigation among cohorts showed that adults were genetically differentiated among island locations, whereas no differences among juveniles were detected. Genetic differentiation between adult and juvenile abalones was detected at SC but not SM or SN. These data are generally consistent with local recruitment augmented by relatively more gene flow among island populations than among island and mainland populations, and possible selection acting on immigrant recruits.     

Recent origin and adaptive diversification of <Emphasis Type="Italic">Ainsliaea</Emphasis> (Asteraceae) in the Ryukyu Islands: molecular phylogenetic inference using nuclear microsatellite markers

We investigated the phylogeny and phylogeography of four closely related Ainsliaea species (Asteraceae) on the continental Ryukyu Islands of eastern Asia, which consist of two flood-adapted “rheophyte” and two non-rheophyte (inland) species, based on 12 nuclear microsatellite loci. Phylogenetic analyses using 420 individuals from 26 populations showed that rheophytic A. linearis and A. oblonga are genetically distinct. Each species was clustered with the inland species that occur on the same islands, suggesting a different ancestry for the two rheophytes that evolved independently by local adaptation to flooded habitats. The results from the neighbor-joining clustering and principal coordinate analysis (PCoA) indicate that the southern populations of A. macroclinidioides are distinct lineages and ancestral to the northern populations as well as the other diverse species complex in the Ryukyus. These results suggest a pattern of colonization initially from the Asian mainland to the southern islands, followed by the northern islands via land bridges generated during the Quaternary glaciations. After isolation from southern populations, species radiation and regional differentiation within the northern clade occurred possibly via local adaptation and/or geographic isolation of the subdivided island bridge.     

Parallel habitat specialization within the wolf spider genus Hogna from the Galápagos

Within most island archipelagos, such as the Galápagos, similar ecological gradients are found on geographically isolated islands. Species radiations in response to these ecological gradients may follow different scenarios being (i) a single habitat specialization event followed by secondary colonization of each ecotype on the different islands or (ii) repeated and parallel habitat specialization on each island separately. This latter scenario has been considered less likely as gene flow might hamper such ecotypic differentiation. At least for the Galápagos, the extent to which this process is involved in species radiations remains yet poorly understood. Within the wolf spider genus Hogna, seven species are described that can be divided into three different ecotypes based on general morphology and habitat preference i.e. species that inhabit the pampa vegetation in the highlands, species that occur in coastal dry habitats and one generalist species. Comparison of the species phylogeny based on one mitochondrial (COI) and one nuclear (28S) gene fragment convincingly demonstrates that ‘pampa’ and ‘coastal dry’ species evolved in parallel on the islands Santa Cruz and San Cristóbal. Despite the observation that allozymes analysis indicated that each species forms a distinct genetic cluster, phylogenetic divergence within these species complexes was very low and paraphyletic and most likely due to hybridization rather than incomplete lineage sorting, as demonstrated for the Santa Cruz species complex. This suggests that within‐island speciation occurred under low levels of gene flow. Species phylogeny in general did not follow the progression of island emergence as a molecular clock analysis suggested that island endemic species may have diverged after as well as before the emergence of the islands. This represents the first clear example of parallel and within‐island speciation because of habitat specialization on the Galápagos and that such divergence most likely occurred under historic gene flow.     

Persistence of antipredator behavior in an island population of California quail

Island populations may provide unique insights into the evolution and persistence of antipredator behavior. If antipredator behavior is costly and islands have reduced predation risk, then we expect the reduction or loss of antipredator behavior on islands. However, if even a single predator remains, the multipredator hypothesis predicts that antipredator behaviors will be conserved. We compared the flight initiation distances (FID) of California quail (Callipepla californica) on Santa Catalina Island (a location with reduced predation pressure) with quail on the mainland. We found no differences in FID between mainland and island quail. However, despite employing consistent testing methods, the starting distance from which quail were approached was significantly reduced for quail studied on the island when compared with quail studied on the mainland. Our results are consistent with the multipredator hypothesis because, while the island population had substantially fewer predators, some predators remained and some antipredator behavior persisted.     

A new species of White‐eye Zosterops and notes on other birds from Vanikoro,Solomon Islands

A new species of white‐eye, the Vanikoro White‐eye Zosterops gibbsi, is described from the island of Vanikoro (= Vanikolo) in the Santa Cruz Islands (= Temotu Province) within the Solomon Islands. It differs from the geographically closest white‐eye, the Santa Cruz White‐eye Zosterops sanctaecrucis, by a number of features including a much longer bill, and different leg‐ and eye‐ring colour. This is the second bird species endemic to Vanikoro; the neighbouring Nendo Island supports three endemic species. Although the conservation status of this species appears to be secure, the Santa Cruz Islands are very poorly known. Despite supporting several globally threatened species, the Islands at present are not protected by any conservation activity.     

ALLOZYME DIFFERENTIATION AND GENETIC STRUCTURE IN ISLAND AND MAINLAND JAPANESE POPULATIONS OF CAMPANULA PUNCTATA (CAMPANULACEAE)

Allozyme variation was investigated in 17 Japanese populations of Campanula punctata, ten from the Izu Islands and seven in the mainland (Honshu). The data indicate that there are two groups, a mainland group and an island one, and that the systematically problematic Oshima Island (northernmost Izu island) populations are closely related to those of the other islands. Nei's genetic identity values among islands and among mainland populations were 0.95 and 0.97, respectively, while the value between island and mainland populations was 0.84, suggesting that the island populations are an independent species. Total genetic variation was nearly the same among island and mainland populations. However, the apportionment of variation within and among populations was considerably different; 14% of gene diversity exists among mainland populations, while 31% of the diversity exists among island populations. Mean outcrossing rates of self-incompatible mainland and Oshima populations are 0.62–0.79, supporting xenogamy; those in self-compatible island populations are 0.37–0.57 in the northern islands, indicating a mixed mating system, and 0.16–0.25 in southern ones, indicating dominant inbreeding. Total genetic diversity in each island population decreased with distance from the mainland. Genetic and geological data suggest that the ancestors of insular populations were founded on northern islands in a relatively ancient period and that they dispersed progressively to the southern ones. Chromosome number (2n = 34) and isozyme numbers indicate gene duplications in this species, which suggests it is an ancient polyploid.