Fumio Sato

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.

First Detection of Rickettsia in Soft‐Bodied Ticks Associated with Seabirds, Japan

Rickettsia was first detected in seabird soft‐bodied ticks, Carios capensis and C. sawaii in Japan. According to sequence analysis, Rickettsia in Japan was identical to Rickettsia scc31 in C. capensis in the U.S.A. This suggested that an environmental circulation had consisted among microorganisms, ticks and long distance migratory seabirds around the Pacific Ocean.

Competence of a migratory bird, red-bellied thrush (Turdus chrysolaus), as an avian reservoir for the Lyme disease spirochetes in Japan.

To evaluate the competence of migratory birds as reservoirs for the Lyme disease spirochetes, we examined two species of migrants, Red-bellied thrush (Turdus chrysolaus) and Black-faced bunting (Emberiza spodocephala) in Nemuro, the northern part of Japan. Spirochetes were found in four individual birds out of 11 T. chrysolaus, three isolates were detected from the skins and the other one was obtained from the liver. No spirochete was found to be infected in 20 E. spodocephala. As far as we know, this is the first record of direct detection of the spirochetes from migratory birds in Japan. The spirochetes were also isolated from immature ixodid ticks, Ixodes persulcatus, fed on those species of birds. The spirochetes were transmitted trans stadially to the next stage, when infected ticks molted. All of the isolates from birds and ticks were identified as Borrelia garinii by our ribotyping and flagellin gene sequence analyses. Our results strongly suggest that the migratory birds are reservoirs in the transmission of the Lyme disease spirochetes in Japan.

Relapsing fever spirochete in seabird tick, Japan.

To the Editor: Tick-borne relapsing fever (TBRF) is caused by infection with spirochetes belonging to the genus Borrelia. We previously reported a human case of febrile illness suspected to be TBRF on the basis of serologic examination results; the vector most likely was a genus Carios tick that had fed on a seabird colony (1). However, surveillance of ticks in the area did not identify Borrelia spp. in any of the Carios ticks sampled (2). In 2007 and 2008, a borreliosis investigation was conducted on Kutsujima Island (35.71′N, 135.44′E) because a bird-associated tick, genus Carios, inhabits this island. During the investigation, 77 Carios ticks (55 nymphs, 11 adult males, and 11 adult females) were collected from colonies of seabirds: Swinhoes storm petrel (Oceanodroma monorhis) and streaked shearwater (Calonectris leucomelas). Identification of tick species as C. sawaii was based on tick morphology and rrs gene sequence analysis of the tick mitochondrion DNA (2). Total DNA was extracted from the ticks by using a DNeasy Tissue Kit (QIAGEN, Germantown, MD, USA). For the detection of Borrelia DNA, PCR designed was based on the flagellin gene (flaB) according to Sato et al. (3). To check for contamination and amplicon carryover, we used blank tubes as a negative control for each experiment. Of 77 C. sawaii ticks that were positive by PCR of tick genes (2), 25 (14 nymphs, 6 adult males, 5 adult females) were positive for Borrelia DNA by PCR of flaB. n nTo characterize the Borrelia spp., we sequenced amplified fragments of the flaB gene and the 16S ribosomal RNA (16SrRNA) gene of Borrelia spp. in a tick and compared the results with those of representative Borrelia spp. The primers BflaPBU and BflaPCR (3) for flaB and the 4 PCR primers (Technical Appendix) for 16SrRNA were used for direct sequencing and/or amplification. DNA sequence (GenBank accession no. {type:entrez-nucleotide,attrs:{text:AB491928,term_id:225703023,term_text:AB491928}}AB491928) of a 294-bp amplified fragment of flaB showed the following nucleotide similarities with those of Borrelia spp.: B. turicatae (98.98%), B. parkeri (98.30%), Borrelia sp. Carios spiro-1 (98.64%), and Borrelia sp. Carios spiro-2 (98.30%). DNA sequence (GenBank accession no. {type:entrez-nucleotide,attrs:{text:AB491930,term_id:225703027,term_text:AB491930}}AB491930) of a 1,490-bp amplified fragment of 16SrRNA showed the following nucleotide similarities with those of Borrelia spp.: B. turicatae (99.60%), B. parkeri (99.53%), and Borrelia sp. Carios spiro-2 (99.45%). Borrelia sp. Carios spiro-1 and Carios spiro-2, which were recently identified in C. kelleyi in the United States, have been classified into TBRF Borrelia (4,5). The Borrelia sp. found in this study, designated as Borrelia sp. K64, was closely related to B. turicatae but was distinct from other TBRF Borrelia spp. (Technical Appendix). n nTo observe Borrelia spp. in tick tissues, we performed an indirect fluorescence assay (IFA) according to methods described by Fisher et al. (6), with minor modifications. A tick that was negative by PCRs of flab and 16SrRNA was used as a negative control. The IFA of the tick salivary gland and midgut was conducted by using acetone for fixation, goat anti-Borrelia sp. polyclonal immunoglobulin (Ig) G (1:100; KPL, Inc., Gaithersburg, MD, USA) as the primary antibody, and Alexa fluor 488-labeled rabbit antigoat IgG (1:200, Invitrogen, Carlsbad, CA, USA) as the secondary antibody. Our analysis showed a spirochete, which was stained by anti-Borrelia spp. antibody, in salivary gland and midgut tissue (Technical Appendix). However, no spirochetes were detected by IFA in the negative control (data not shown). n nWe also attempted to isolate Borrelia spp. from tick specimens by using Barbour-Stoenner-Kelly medium (7). The motility of Borrelia-like organisms in the medium was initially observed by using dark-field microscopy. The Borrelia-like organisms were identified as Borrelia sp. K64 by sequencing of PCR-amplified fragments of flaB and 16SrRNA genes from the cultured medium. However, these Borrelia organisms were found for only 2 weeks after inoculation (data not shown). n nThe vertebrate reservoir hosts of TBRF Borrelia are usually rodents but can be a variety of other animals (8). Although competence as a reservoir has not been determined for birds, infection of an owl with a TBRF Borrelia sp. has been reported (9). The vertebrate host of the spirochete has not yet been determined. Given our results, it is possible that seabirds are potential vertebrate hosts for Borrelia spp. n nIn Japan, relapsing fever is a neglected infectious disease because it was not reported during 1956–1998 (10). In this study, we detected a Borrelia sp. in C. sawaii, and the spirochete we characterized is closely related to B. turicatae. Although the human health implications of infections caused by Borrelia spp. are not yet known, the findings from this study should contribute to the epidemiologic investigation of TBRF in Japan.

Morphological and genomic comparisons of Hawaiian and Japanese Black-footed Albatrosses (Phoebastria nigripes) using double digest RADseq: implications for conservation.

Evaluating the genetic and demographic independence of populations of threatened species is important for determining appropriate conservation measures, but different technologies can yield different conclusions. Despite multiple studies, the taxonomic status and extent of gene flow between the main breeding populations of Black‐footed Albatross (Phoebastria nigripes), a Near‐Threatened philopatric seabird, are still controversial. Here, we employ double digest RADseq to quantify the extent of genomewide divergence and gene flow in this species. Our genomewide data set of 9760 loci containing 3455 single nucleotide polymorphisms yielded estimates of genetic diversity and gene flow that were generally robust across seven different filtering and sampling protocols and suggest a low level of genomic variation (θ per site = ~0.00002–0.00028), with estimates of effective population size (Ne = ~500–15 881) falling far below current census size. Genetic differentiation was small but detectable between Japan and Hawaii (FST ≈ 0.038–0.049), with no FST outliers. Additionally, using museum specimens, we found that effect sizes of morphological differences by sex or population rarely exceeded 4%. These patterns suggest that the Hawaiian and Japanese populations exhibit small but significant differences and should be considered separate management units, although the evolutionary and adaptive consequences of this differentiation remain to be identified.

Translocation and hand-rearing of the short-tailed albatross Phoebastria albatrus : early indicators of success for species conservation and island restoration

Many endemic species, particularly those on remote islands, have been driven to extinction or near extinction by anthropogenic influences. The short-tailed albatross Phoebastria albatrus once numbered in the millions but was thought to be extinct by the mid 20th century. Albatrosses, of the family Diomedeidae, are among the most threatened birds globally as a result of commercial exploitation, introduced predators, and mortality in commercial fisheries. We applied an experimental approach over 5 years to evaluate the translocation and hand-rearing of albatross chicks by comparing growth, physiological health indices, post-fledging survival, and migration patterns with a control group of naturally reared chicks in the source population. Hand-reared chicks had comparable or superior health and similar rates of immediate post-fledging mortality (15%), with mortality strongly female-biased in both groups. Hand-reared birds had longer post-fledging drift periods before attaining sustained flight (also female-biased) but comparable, albeit somewhat wider ranging, migration patterns to naturally reared chicks during their first 6 months at sea. Recruitment to the translocation site of a breeding pair that included a hand-reared bird occurred within 5 years of the first translocation. Success will ultimately depend on continued recruitment and breeding over the coming decades, given delayed breeding in these long-lived species. The results to date, however, have exceeded initial expectations and can inform potential reintroductions of other long-lived, migratory avian species with strong natal philopatry, and reintroductions of native species to former breeding islands.

First Record of Leptospira borgpetersenii Isolation in the Amami Islands, Japan

In 2003, a Leptospira survey was performed on Yoroshima Island of the Amami Islands located in the southwestern part of Japan. Seven Leptospira strains were isolated from the field rat Rattus rattus, which were identified as L. borgpetersenii by flaB sequencing, 16S rDNA sequencing and gyrB sequencing, and serovar Javanica was determined by a microscopic agglutination test. NotI‐long restriction fragment analysis indicated that these isolates were genetically indistinguishable from an isolate from the Okinawa Islands. The present results suggest that L. borgpetersenii is migrating into the Amami Islands in Japan.

Translocation and hand-rearing techniques for establishing a colony of threatened albatross

Summary Many breeding colonies of Procellariiformes have been threatened with extinction. Chick translocation has been shown to be an effective method for establishing new “safer” colonies of burrow-nesting species, but techniques for surface-nesting species have not been fully developed. The entire breeding population of the threatened Short-tailed Albatross Phoebastoria albatrus is restricted to two sites, Torishima Island and the Senkaku Islands, and neither site is secure due to volcanic activity or political instability. The Short-tailed Albatross Recovery Team has recommended facilitating the recovery of this species by establishing at least one additional colony through the translocation and hand-rearing of chicks at a safe historical breeding site. To evaluate the feasibility of this approach, we hand-reared 10 post-guard phase chicks of two related species in 2006–2007: Laysan Albatross P. immutabilis translocated from Midway Atoll to Kaua’i Island, Hawai’i and Black-footed Albatross P. nigripes translocated from a nearby islet in the Ogasawara (Bonin) Islands to Mukojima Island, Japan. In these pilot studies, 40% of Laysan Albatross chicks and 90% of Black-footed Albatross chicks fledged successfully. Following this groundwork, 40 post-guard phase Short-tailed Albatross chicks were translocated from Torishima Island to Mukojima Island in February 2008–2010 and hand-reared to fledging. Their fledging success has been 100% in all three years. Fledging body sizes were similar or greater in hand-reared chicks at the release site than parent-reared chicks on Torishima Island. There were significant differences in levels of some blood chemistry parameters between pre-fledging hand-reared and parent-reared chicks. The techniques developed in our studies have broad-reaching implications for the future conservation of threatened populations of other surface-nesting seabirds.

Satellite tracking of migrating Whooper Swans Cygnus cygnus wintering in Japan.

Abstract n We satellite-tracked Whooper Swans Cygnus cygnus wintering in northern Japan to document their migration routes and timing, and to identify breeding areas. From 47 swans that we marked at Lake Izunuma-Uchinuma, Miyagi Prefecture, northeast Honshu, and at Lake Kussharo, east Hokkaido, we observed 57 spring and 33 autumn migrations from 2009–2012. In spring, swans migrated north along Sakhalin Island from eastern Hokkaido using stopovers in Sakhalin, at the mouth of the Amur River and in northern coastal areas of the Sea of Okhotsk. They ultimately reached molting/breedmg areas along the Indigirka River and the lower Kolyma River in northern Russia. In autumn, the swans basically reversed the spring migration routes. We identified northern Honshu, eastern Hokkaido, coastal areas in Sakhalin, the lower Amur River and northern coastal areas of the Sea of Okhotsk as the most frequent stopover sites, and the middle reaches of the Indigirka and the lower Kolyma River as presumed breeding sites. Our results are helpful in understanding the distribution of the breeding and stopover sites of Whooper Swans wintering in Japan and in identifying their major migration habitats. Our findings contribute to understanding the potential transmission process of avian influenza viruses potentially carried by swans, and provide information necessary to conserve Whooper Swans in East Asia.

Genetic structure of the endangered red-crowned cranes in Hokkaido, Japan and conservation implications

The red-crowned crane in Japan was once considered extinct due to hunting and habitat destruction in late nineteenth century; however, in 1926, a small group of cranes was rediscovered in the Kushiro Mire in eastern Hokkaido. Since then, various conservation efforts, including artificial feeding during winter, hunting prohibition, and habitat conservation, have increased the population size to >1400 by 2012. Despite such a successful population recovery, the genetic characteristics of the population have not been fully explored. To ensure the long-term persistence and evolutionary potential of cranes, accurate knowledge of the spatial distribution of genetic variation and its underlying causes are necessary. We assessed their genetic structure using 12 polymorphic microsatellite loci and inferred the mechanisms shaping the observed structure. Among the three regional groups in Hokkaido, we found generally low pairwise FST values and no significant differences in genetic diversity, probably because of the population expansion in the recent past. In contrast, spatial autocorrelation analysis revealed a significant positive kinship at the short distance (0–15xa0km) and negative kinship at the long distance (155–205xa0km), showing a pattern of isolation by distance. The presence of isolation by distance on a small spatial scale despite the species’ strong flight ability is probably explained by the recolonization process and restricted dispersal due to natal philopatry in a non-equilibrium condition. Cranes in Hokkaido do not appear to be a panmictic (random mating) population; however they can be considered a single population without genetic discontinuity (i.e. a single management unit). Our findings confirm the importance of considering natal philopatry when developing management strategies such as dispersing cranes into unoccupied areas.