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George H. Balazs

Publications and source records attributed to George H. Balazs.

At least 19 recordsLinked to original sources

Global tracking of marine megafauna space use reveals how to achieve conservation targets

The recent Kunming-Montreal Global Biodiversity Framework (GBF) sets ambitious goals but no clear pathway for how zero loss of important biodiversity areas and halting human-induced extinction of threatened species will be achieved. We assembled a multi-taxa tracking dataset (11 million geopositions from 15,845 tracked individuals across 121 species) to provide a global assessment of space use of highly mobile marine megafauna, showing that 63% of the area that they cover is used 80% of the time as important migratory corridors or residence areas. The GBF 30% threshold (Target 3) will be insufficient for marine megafauna’s effective conservation, leaving important areas exposed to major anthropogenic threats. Coupling area protection with mitigation strategies (e.g., fishing regulation, wildlife-traffic separation) will be essential to reach international goals and conserve biodiversity.

Science

Three decades of stranding data reveal insights into endangered hawksbill sea turtles in Hawai‘i

Hawksbill sea turtles Eretmochelys imbricata inhabiting the Hawaiian Islands are extremely rare and listed as endangered under the US Endangered Species Act. The paucity of data on basic hawksbill ecology continues to hinder effective management of the species. We analyzed stranding data collected between 1984 and 2018 to gain insights into the distribution, demography, and conservation challenges facing hawksbills in Hawai‘i. In doing so, we present a comprehensive description of the population across developmental stages and rank threats that may be impeding their successful recovery. Over the >30 yr data set, we recorded a total of only 111 juvenile and adult hawksbill stranding events. Interactions with nearshore recreational fishing gear were documented for a large proportion (48.6%) of stranding events in the Hawaiian Islands, identifying this as the primary management challenge for the species. Stranding events were biased towards females (female to male sex ratio of 4.8:1.0), which may be indicative of the population as a whole. Even though the majority of hawksbills nest on the islands of Hawai‘i Moloka‘i, and Maui, the greatest number of juvenile to adult strandings was found to be on the island of Oahu (n = 47). Temporal distribution of the majority of adult hawksbill strandings (72.2%) occurred during a 4 mo period between June and September. We discuss these and other findings that help identify future research and conservation efforts to mitigate anthropogenic threats in Hawai‘i for this enigmatic population.

Hawaii

Characterization of halogenated organic compounds in pelagic sharks and sea turtles using a nontargeted approach

Halogenated organic compounds (HOCs) in marine species collected from the Atlantic Ocean [3 shortfin mako ( Isurus oxyrinchus ) and 1 porbeagle ( Lamna nasus )], and 12 sea turtles collected from the Pacific Ocean [3 loggerhead ( Caretta caretta ), 3 green ( Chelonia mydas ), 3 olive ridley ( Lepidochelys olivacea ), and 3 hawksbill ( Eretmochelys imbricata )] were analyzed with a nontargeted analytical method using two-dimensional gas chromatography coupled to high-resolution time-of-flight mass spectrometry. Sharks and sea turtles had distinct HOC profiles. Halogenated methoxyphenols (halo-MeOPs) were the most abundant compound class identified in sea turtle livers, while polychlorinated biphenyls (PCBs) were the most abundant in shark livers. In addition to legacy contaminants and halo-MeOPs, a total of 110 nontargeted/novel HOCs (NHOCs) were observed in the shark livers. Shortfin mako collected from the northern Gulf of Mexico contained the largest number (89) and most diverse structural classes of NHOCs. Among all NHOCs, a group of compounds with the elemental composition C 14 H 12– n Cl n ( n = 5–8) exhibited the highest concentrations, followed by chlorocarbazoles and tris(chlorophenyl) methanes (TCPMs). Using nontargeted workflows, a variety of known and unknown HOCs were observed, which demonstrate the need to develop more complete chemical profiles in the marine environment.

Environmental Science & Technology

Species and population specific gene expression in blood transcriptomes of marine turtles

Background Transcriptomic data has demonstrated utility to advance the study of physiological diversity and organisms’ responses to environmental stressors. However, a lack of genomic resources and challenges associated with collecting high-quality RNA can limit its application for many wild populations. Minimally invasive blood sampling combined with de novo transcriptomic approaches has great potential to alleviate these barriers. Here, we advance these goals for marine turtles by generating high quality de novo blood transcriptome assemblies to characterize functional diversity and compare global transcriptional profiles between tissues, species, and foraging aggregations. Results We generated high quality blood transcriptome assemblies for hawksbill ( Eretmochelys imbricata ) , loggerhead ( Caretta caretta ), green ( Chelonia mydas ), and leatherback ( Dermochelys coriacea ) turtles. The functional diversity in assembled blood transcriptomes was comparable to those from more traditionally sampled tissues. A total of 31.3% of orthogroups identified were present in all four species, representing a core set of conserved genes expressed in blood and shared across marine turtle species. We observed strong species-specific expression of these genes, as well as distinct transcriptomic profiles between green turtle foraging aggregations that inhabit areas of greater or lesser anthropogenic disturbance. Conclusions Obtaining global gene expression data through non-lethal, minimally invasive sampling can greatly expand the applications of RNA-sequencing in protected long-lived species such as marine turtles. The distinct differences in gene expression signatures between species and foraging aggregations provide insight into the functional genomics underlying the diversity in this ancient vertebrate lineage. The transcriptomic resources generated here can be used in further studies examining the evolutionary ecology and anthropogenic impacts on marine turtles.

BMC Genomics

Sea turtles across the North Pacific are exposed to perfluoroalkyl substances

Perfluorinated alkyl substances (PFASs) are global, persistent, and toxic contaminants. We assessed PFAS concentrations in green ( Chelonia mydas ) and hawksbill ( Eretmochelys imbricata ) turtles from the North Pacific. Fifteen compounds were quantified via liquid chromatography tandem mass spectrometry from 62 green turtle and 6 hawksbill plasma samples from Hawai’i, Palmyra Atoll, and the Northern Marianas Islands. Plasma from 14 green turtles severely afflicted with fibropapillomatosis, and eggs from 12 Hawaiian hawksbill nests from 7 females were analyzed. Perfluorooctane sulfonate (PFOS) predominated in green turtle plasma; perfluorononanoic acid (PFNA) predominated in hawksbill tissues. Concentrations were greater in hawksbill than green turtle plasma (p < 0.05), related to trophic differences. Green turtle plasma PFOS concentrations were related to human populations from highest to lowest: Hawai’i, Marianas, Palmyra. Influence on fibropapillomatosis was not evident. PFASs were maternally transferred to hawksbill eggs, with decreasing concentrations with distance from airports and with clutch order from one female. A risk assessment of PFOS showed concern for immunosuppression in Kailua green turtles and alarming concern for hawksbill developmental toxicity. Perfluoroundecanoic (PFUnA) and perfluorotridecanoic (PFTriA) acid levels were correlated with reduced emergence success (p < 0.05). Studies to further examine PFAS effects on sea turtle development would be beneficial.

Hawaii

A novel host-adapted strain of Salmonella Typhimurium causes disease in olive ridley turtles (Lepidochelys olivacea) in the Pacific.

Salmonella spp. are frequently shed by wildlife including turtles, but S. enterica subsp. enterica serovar Typhimurium or lesions associated with Salmonella are rare in turtles. Between 1996 and 2016, we necropsied 127 apparently healthy pelagic olive ridley turtles ( Lepidochelys olivacea ) that died from drowning bycatch in fisheries and 44 live or freshly dead stranded turtles from the west coast of North and Central America and Hawaii. Seven % (9/127) of pelagic and 47% (21/44) of stranded turtles had renal granulomas associated with S. Typhimurium. Stranded animals were 12 times more likely than pelagic animals to have Salmonella -induced nephritis suggesting that Salmonella may have been a contributing cause of stranding. S. Typhimurium was the only Salmonella serovar detected in L. olivacea , and phylogenetic analysis from whole genome sequencing showed that the isolates from L. olivacea formed a single clade distinct from other S. Typhimurium. Molecular clock analysis revealed that this novel clade may have originated as recently as a few decades ago. The phylogenetic lineage leading to this group is enriched for non-synonymous changes within the genomic area of Salmonella pathogenicity island 1 suggesting that these genes are important for host adaptation.

California, Hawaii, Oregon, Washington

Validation of ATR FT-IR to identify polymers of plastic marine debris, including those ingested by marine organisms

Polymer identification of plastic marine debris can help identify its sources, degradation, and fate. We optimized and validated a fast, simple, and accessible technique, attenuated total reflectance Fourier transform infrared spectroscopy (ATR FT-IR), to identify polymers contained in plastic ingested by sea turtles . Spectra of consumer good items with known resin identification codes #1–6 and several #7 plastics were compared to standard and raw manufactured polymers. High temperature size exclusion chromatography measurements confirmed ATR FT-IR could differentiate these polymers. High-density (HDPE) and low-density polyethylene (LDPE) discrimination is challenging but a clear step-by-step guide is provided that identified 78% of ingested PE samples. The optimal cleaning methods consisted of wiping ingested pieces with water or cutting. Of 828 ingested plastics pieces from 50 Pacific sea turtles, 96% were identified by ATR FT-IR as HDPE, LDPE, unknown PE, polypropylene (PP), PE and PP mixtures, polystyrene , polyvinyl chloride , and nylon.

Marine Pollution Bulletin

Investigation of plastic debris ingestion by four species of sea turtles collected as bycatch in pelagic Pacific longline fisheries

Ingestion of marine debris is an established threat to sea turtles. The amount, type, color and location of ingested plastics in the gastrointestinal tracts of 55 sea turtles from Pacific longline fisheries from 2012 to 2016 were quantified, and compared across species, turtle length, body condition, sex, capture location, season and year. Six approaches for quantifying amounts of ingested plastic strongly correlated with one another and included: number of pieces, mass, volume and surface area of plastics, ratio of plastic mass to body mass, and percentage of the mass of gut contents consisting of plastic. All olive ridley (n = 37), 90% of green (n = 10), 80% of loggerhead (n = 5) and 0% of leatherback (n = 3) turtles had ingested plastic; green turtles ingested significantly more than olive ridleys. Most debris was in the large intestines. No adverse health impacts (intestinal lesions, blockage, or poor body condition) due directly to plastic ingestion were noted.

Marine Pollution Bulletin

Persistent organic pollutants in fat of three species of Pacific pelagic longline caught sea turtles: Accumulation in relation to ingested plastic marine debris

In addition to eating contaminated prey, sea turtles may be exposed to persistent organic pollutants (POPs) from ingesting plastic debris that has absorbed these chemicals. Given the limited knowledge about POPs in pelagic sea turtles and how plastic ingestion influences POP exposure, our objectives were to: 1) provide baseline contaminant levels of three species of pelagic Pacific sea turtles; and 2) assess trends of contaminant levels in relation to species, sex, length, body condition and capture location. In addition, we hypothesized that if ingesting plastic is a significant source of POP exposure, then the amount of ingested plastic may be correlated to POP concentrations accumulated in fat. To address our objectives we compared POP concentrations in fat samples to previously described amounts of ingested plastic from the same turtles. Fat samples from 25 Pacific pelagic sea turtles [2 loggerhead ( Caretta caretta ), 6 green ( Chelonia mydas ) and 17 olive ridley ( Lepidochelys olivacea ) turtles] were analyzed for 81 polychlorinated biphenyls (PCBs), 20 organochlorine pesticides, and 35 brominated flame-retardants. The olive ridley and loggerhead turtles had higher ΣDDTs (dichlorodiphenyltrichloroethane and metabolites) than ΣPCBs, at a ratio similar to biota measured in the South China Sea and southern California. Green turtles had a ratio close to 1:1. These pelagic turtles had lower POP levels than previously reported in nearshore turtles. POP concentrations were unrelated to the amounts of ingested plastic in olive ridleys, suggesting that their exposure to POPs is mainly through prey. In green turtles, concentrations of ΣPCBs were positively correlated with the number of plastic pieces ingested, but these findings were confounded by covariance with body condition index (BCI). Green turtles with a higher BCI had eaten more plastic and also had higher POPs. Taken together, our findings suggest that sea turtles accumulate most POPs through their prey rather than marine debris.

Science of the Total Environment

In-vitro replication of Chelonid herpesvirus 5 in organotypic skin cultures from Hawaiian green turtles (Chelonia mydas)

Fibropapillomatosis (FP) is a tumor disease of marine turtles associated with Chelonid herpesvirus 5 (ChHV5) that has historically been refractory to growth in tissue culture. Here, we show for the first time de novo formation of ChHV5-positive intranuclear inclusions in cultured green turtle cells, which is indicative for active lytic replication of the virus. The minimal requirements to achieve lytic replication in cultured cells included 1) either in-vitro culturing of ChHV5-positive tumor biopsies (plugs) or organotypic cultures (rafts) consisting of ChHV5-positive turtle fibroblasts in collagen rafts seeded with turtle keratinocytes and 2) keratinocyte maturation induced by raising raft or biopsy cultures to the air-liquid interface. Virus growth was confirmed by detailed electron microscopic studies revealing intranuclear sun-shaped capsid factories, tubules, various stages of capsid formation, nuclear export by budding into the perinuclear space, tegumentation, and envelopment to complete de novo virus production. Membrane synthesis was also observed as a sign for active viral replication. Interestingly, cytoplasmic particles became associated with keratin filaments, a feature not seen in conventional monolayer cell cultures where most studies of herpesvirus replication have been performed. Our findings draw a rich and realistic picture of ChHV5 replication in cells derived from its natural host and may be crucial not only to better understand ChHV5 circulation but also to eventually complete Koch's postulates for FP. Moreover, the principles described here may serve as model to culture other viruses that are resistant to replication in conventional cell culture.

Hawai'i

Identification of Chelonid herpesvirus 5 (ChHV5) in endangered green turtles (Chelonia mydas) with fibropapillomatosis in Asia

Fibropapillomatosis (FP), a debilitating tumor disease of sea turtles, was first identified in green turtles [ Chelonia mydas (Linnaeus, 1758)] in Florida in 1938. In recent decades, FP has been observed globally and is an emerging panzootic disease in sea turtles. However, few reports of FP in Asia exist. Here, we provide the first evidence of Chelonid herpesvirus 5 (ChHV5) DNA associated with FP in endangered green turtles from Taiwan, through molecular characterization, phylogenetic analysis, and histopathological examination. In our study, ChHV5 was successfully detected by PCR in the FP tumor lesions of green turtles. The sequences were found to be consistent with those of tumor-inducing viruses shown to affect sea turtles in the other parts of the world. ChHV5 RNA from the FP tissues was further detected by RT-PCR, indicating active replication of the viruses inside FP tumors. In addition to the molecular evidence of ChHV5 in FP, epidermal intranuclear inclusions were identified in tumor lesions upon histopathological examination. This further suggests that ChHV5 should be in a transcriptionally active (i.e., non-latent) state in FP tumors of affected green turtles. The phylogenetic tree revealed that ChHV5 from the green turtles in Taiwan were closest to the ChHV5 from Hawaii, Puerto Rico, and Sao Tome. For conservation of endangered sea turtles, ChHV5 should be considered an emerging virus, which threatens sea turtles in marine waters in Asia.

Bulletin of Marine Science

Validation of ultrasound as a noninvasive tool to measure subcutaneous fat depth in leatherback sea turtles ( Dermochelys coriacea )

Leatherback turtles ( Dermochelys coriacea ) undergo substantial cyclical changes in body condition between foraging and nesting. Ultrasonography has been used to measure subcutaneous fat as an indicator of body condition in many species but has not been applied in sea turtles. To validate this technique in leatherback turtles, ultrasound images were obtained from 36 live-captured and dead-stranded immature and adult turtles from foraging and nesting areas in the Pacific and Atlantic oceans. Ultrasound measurements were compared with direct measurements from surgical biopsy or necropsy. Tissue architecture was confirmed histologically in a subset of turtles. The dorsal shoulder region provided the best site for differentiation of tissues. Maximum fat depth values with the front flipper in a neutral (45&ndash;90&deg;) position demonstrated good correlation with direct measurements. Ultrasound-derived fat measurements may be used in the future for quantitative assessment of body condition as an index of health in this critically endangered species.

Journal of Zoo and Wildlife Medicine

Green turtles ( Chelonia mydas ) have novel asymmetrical antibodies

Igs in vertebrates comprise equally sized H and L chains, with exceptions such as H chain&ndash;only Abs in camels or natural Ag receptors in sharks. In Reptilia, Igs are known as IgYs. Using immunoassays with isotype-specific mAbs, in this study we show that green turtles ( Chelonia mydas ) have a 5.7S 120-kDa IgY comprising two equally sized H/L chains with truncated Fc and a 7S 200-kDa IgY comprised of two differently sized H chains bound to L chains and apparently often noncovalently associated with an antigenically related 90-kDa moiety. Both the 200- and 90-kDa 7S molecules are made in response to specific Ag, although the 90-kDa molecule appears more prominent after chronic Ag stimulation. Despite no molecular evidence of a hinge, electron microscopy reveals marked flexibility of Fab arms of 7S and 5.7S IgY. Both IgY can be captured with protein G or melon gel, but less so with protein A. Thus, turtle IgY share some characteristics with mammalian IgG. However, the asymmetrical structure of some turtle Ig and the discovery of an Ig class indicative of chronic antigenic stimulation represent striking advances in our understanding of immunology.

Journal of Immunology

Topsy-turvy: Turning the counter-current heat exchange of leatherback turtles upside down

Counter-current heat exchangers associated with appendages of endotherms feature bundles of closely applied arteriovenous vessels. The accepted paradigm is that heat from warm arterial blood travelling into the appendage crosses into cool venous blood returning to the body. High core temperature is maintained, but the appendage functions at low temperature. Leatherback turtles have elevated core temperatures in cold seawater and arteriovenous plexuses at the roots of all four limbs. We demonstrate that plexuses of the hindlimbs are situated wholly within the hip musculature, and that, at the distal ends of the plexuses, most blood vessels supply or drain the hip muscles, with little distal vascular supply to, or drainage from the limb blades. Venous blood entering a plexus will therefore be drained from active locomotory muscles that are overlaid by thick blubber when the adults are foraging in cold temperate waters. Plexuses maintain high limb muscle temperature and avoid excessive loss of heat to the core, the reverse of the accepted paradigm. Plexuses protect the core from overheating generated by muscular thermogenesis during nesting.

Biology Letters

Causes of mortality in green turtles from Hawaii and the insular Pacific exclusive of fibropapillomatosis

Fibropapillomatosis (FP) comprises a majority of green turtle stranding in Hawaii; however, green turtles in the Pacific are also susceptible to non-FP related causes of death. We present here necropsy findings from 230 free-ranging green turtles originating from Hawaii, the Mariana archipelago, Palmyra Atoll, American Samoa, and Johnston Atoll that died from non-FP related causes. Most turtles died from fishing-induced or boat strike trauma followed by infectious/inflammatory diseases, nutritional problems (mainly cachexia), and an array of physiologic problems. Infectious/inflammatory problems included bacterial diseases of the lungs, eyes, liver or intestines, spirorchid fluke infection, or polyarthritis of unknown origin. Likelihood of a successful diagnosis of cause of death was a function of post-mortem decomposition. Fibropapillomatosis was not seen in turtles submitted from outside Hawaii. The preponderance of anthropogenic causes of mortality offers some management opportunities to mitigate causes of death in these animals by, for example, implementing measures to decrease boating and fishing interactions.

Diseases of Aquatic Organisms

Dynamics of virus shedding and in situ confirmation of chelonid herpesvirus 5 in Hawaiian green turtles with Fibropapillomatosis

Cancers in humans and animals can be caused by viruses, but virus-induced tumors are considered to be poor sites for replication of intact virions (lytic replication). Fibropapillomatosis (FP) is a neoplastic disease associated with a herpesvirus, chelonid herpesvirus 5 (ChHV5), that affects green turtles globally. ChHV5 probably replicates in epidermal cells of tumors, because epidermal intranuclear inclusions (EIIs) contain herpesvirus-like particles. However, although EIIs are a sign of herpesvirus replication, they have not yet been firmly linked to ChHV5. Moreover, the dynamics of viral shedding in turtles are unknown, and there are no serological reagents to confirm actual presence of the specific ChHV5 virus in tissues. The investigators analyzed 381 FP tumors for the presence of EIIs and found that overall, about 35% of green turtles had lytic replication in skin tumors with 7% of tumors showing lytic replication. A few (11%) turtles accounted for more than 30% cases having lytic viral replication, and lytic replication was more likely in smaller tumors. To confirm that turtles were actively replicating ChHV5, a prerequisite for shedding, the investigators used antiserum raised against F-VP26, a predicted capsid protein of ChHV5 that localizes to the host cell nucleus during viral replication. This antiserum revealed F-VP26 in EIIs of tumors, thus confirming the presence of replicating ChHV5. In this light, it is proposed that unlike other virus-induced neoplastic diseases, FP is a disease that may depend on superspreaders, a few highly infectious individuals growing numerous small tumors permissive to viral production, for transmission of ChHV5.

Veterinary Pathology

Investigating the potential role of persistent organic pollutants in Hawaiian green sea turtle fibropapillomatosis

It has been hypothesized for decades that environmental pollutants may contribute to green sea turtle fibropapillomatosis (FP), possibly through immunosuppression leading to greater susceptibility to the herpesvirus, the putative causative agent of this tumor-forming disease. To address this question, we measured concentrations of 164 persistent organic pollutants (POPs) and halogenated phenols in 53 Hawaiian green turtle ( Chelonia mydas ) plasma samples archived by the Biological and Environmental Monitoring and Archival of Sea Turtle Tissues (BEMAST) project at the National Institute of Standards and Technology Marine Environmental Specimen Bank. Four groups of turtles were examined: free-ranging turtles from Kiholo Bay (0% FP, Hawaii), Kailua Bay (low FP, 8%, Oahu), and Kapoho Bay (moderate FP, 38%, Hawaii) and severely tumored stranded turtles that required euthanasia (high FP, 100%, Main Hawaiian Islands). Four classes of POPs and seven halogenated phenols were detected in at least one of the turtles, and concentrations were low (often <200 pg/g wet mass). The presence of halogenated phenols in sea turtles is a novel discovery; their concentrations were higher than most man-made POPs, suggesting that the source of most of these compounds was likely natural (produced by the algal turtle diet) rather than metabolites of man-made POPs. None of the compounds measured increased in concentration with increasing prevalence of FP across the four groups of turtles, suggesting that these 164 compounds are not likely primary triggers for the onset of FP. However, the stranded, severely tumored, emaciated turtle group ( n = 14) had the highest concentrations of POPs, which might suggest that mobilization of contaminants with lipids into the blood during late-stage weight loss could contribute to the progression of the disease. Taken together, these data suggest that POPs are not a major cofactor in causing the onset of FP.

Hawai'i

Unique characteristics of the trachea of the juvenile leatherback turtle facilitate feeding, diving and endothermy

The adult leatherback turtle Dermochelys coriacea overlaps in body size (300&ndash;500 kg) with many marine mammals, yet develops from a 50 g hatchling. Adults can dive deeper than 1200 m and have core body temperatures of 25 &deg;C; hatchlings are near-surface dwellers. Juvenile leatherbacks have rarely been studied; here we present anatomical information for the upper respiratory tract of 3 turtles (66.7&ndash;83.0 cm straight carapace length; 33.2&ndash;53.4 kg body mass) incidentally captured by long-line fisheries. Combined with existing information from adults and hatchlings, our data show that there is an ontogenic shift in tracheal structure, with cartilaginous rings becoming broader and eventually fusing anteriorly. This ontogenic shift during independent existence is unique among extant deep-diving air breathing vertebrates. Tract wall thickness is graded, becoming progressively thinner from larynx to bronchi. In addition, cross-sectional shape becomes increasingly dorsoventrally flattened (more elliptical) from anterior to posterior. These characteristics ensure that the tract will collapse from posterior to anterior during dives. This study contains the first report of a double (= internally bifurcated) posterior section of the trachea; it is suggested that this allows continuous food movement along the esophagus without tracheal collapse. The whole upper respiratory tract (from larynx to lungs) has a vascular lining (thicker anteriorly than posteriorly) that appears to be a simple analog of the complex turbinates of birds and mammals. Our study confirmed that the leatherback tracheal structure represents a distinctive way of dealing with the challenges of diving in deep, cold sea water.

Journal of Experimental Marine Biology and Ecology