Broadening disease surveillance to include wild dolphins and killer whales: novel components of One Health

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Abstract We describe a minimally invasive pilot study to characterize the microbiota of exhaled breath from wild Pacific white-sided dolphins. Samples were collected in a site that is far from any agriculture facilities or large human settlements but home to a high concentration of open-net aquaculture facilities for Atlantic salmon. This case study in pathogen surveillance in wild dolphins reveals a wide diversity of pathogens, including several with the potential to cross species and infect critically endangered killer whales, or humans. Common species are often neglected in funding strategies that prioritize species at imminent risk of extinction, but they may be a top priority for disease surveillance. One important cobenefit of integrating biodiversity monitoring in a One Health framework may be to support monitoring of both abundance and zoonotic potential of common species whose biomass alone makes them key players in ecosystem function.

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Amidst growing animal rights movements, the release of captive cetaceans, particularly killer whales and dolphins, into their natural environments has gained increasing support from activists due to ethical concerns. However, there is a notable lack of quantitative studies on the interactions between wild and captive dolphins during rehabilitation before release. This study assesses the rehabilitation process of captive dolphin during its stay in the sea pen using advanced surveillance techniques. Methods including CCTV, hydrophone monitoring, and drone observations were utilized to document interactions between rehabilitating and wild dolphins. A convolutional neural network-based detector for dolphin whistle sound was used to automatically detect the whistle from underwater sound recorded at the rehabilitation site, which significantly expedited the identification of wild dolphin encounters compared to traditional manual methods. This technology also facilitated synchronized analysis of underwater sounds, CCTV footage, and drone videos, providing comprehensive visual and acoustic observations of captive and wild dolphins during encounters. This research offers insights that can guide future dolphin rehabilitation monitoring and release strategies.

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  • Research Article
  • Cite Count Icon 4
  • 10.1371/journal.pbio.1001573
An Inordinate Fondness of Rarity
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  • 10.3354/dao02917
Pathogen surveillance in wild bottlenose dolphins Tursiops truncatus.
  • Oct 16, 2015
  • Diseases of Aquatic Organisms
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The number and prevalence of diseases is rapidly increasing in the marine ecosystem. Although there is an increase in the number of marine diseases observed world-wide, current understanding of the pathogens associated with marine mammals is limited. An important need exists to develop and apply platforms for rapid detection and characterization of pathogenic agents to assess, prevent and respond to disease outbreaks. In this study, a broad-spectrum molecular detection technology capable of detecting all sequenced microbial organisms, the Lawrence Livermore Microbial Detection Array, was used to assess the microbial agents that could be associated with wild Atlantic dolphins. Blowhole, gastric, and fecal samples from 8 bottlenose dolphins were collected in Charleston, SC, as part of the dolphin assessment effort. The array detected various microbial agents from the dolphin samples. Clostridium perfringens was most prevalent in the samples surveyed using the microarray. This pathogen was also detected using microbiological culture techniques. Additionally, Campylobacter sp., Staphylococcus sp., Erwinia amylovora, Helicobacter pylori, and Frankia sp. were also detected in more than one dolphin using the microarray, but not in culture. This study provides the first survey of pathogens associated with 3 tissue types in dolphins using a broad-spectrum microbial detection microarray and expands insight on the microbial community profile in dolphins.

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  • 10.1007/978-3-319-55574-4_7
Let the Oceans Speak: The Synergistic Interaction Between Intensity and Interpretation During Wild Dolphin Experiences
  • Jan 1, 2017
  • Gayle Mayes

The desirable outcomes of interpretation in a wildlife setting include the stimulation of visitor intent to minimise impacts and maximise support for the marine environment and its wildlife. Existing frameworks and models of wildlife tourism focus on interpretation and the cognitive domain. However, wildlife tourism encounters, especially with whales and dolphins, can be intense, emotional, powerful and profound affective experiences. Theory and models from experiential education were more relevant and applicable for exploring synergistic relationships between the affective and cognitive domains that resulted in changes in attitudes, beliefs, behaviours and actions. This paper investigates the interactive effects between the intensity of wild dolphin tourism experiences in the presence of education/interpretation commentaries on: overall satisfaction levels; changes in knowledge; and changes in pro-environmental attitudes, beliefs, intended behaviours and intended actions of participants. A multiple case study approach was used to collect data on six matched and paired dolphin tourism activities which varied in intensity and educational and interpretive input. Chi-square, one and two-way ANOVAs and MANOVA analyses (with a reduced number of factors) were used on data from 600 structured self-administered questionnaires. Results suggested that high intensity wild dolphin experiences are highly satisfying, and that the overall satisfaction of participants is not enhanced by the inclusion of a high quality interpretation component. High intensity wildlife experiences in themselves appear to have significant educative impact or power which can impede positive effects of high quality interpretation commentaries on increases of knowledge of participants and intended pro-environmental behaviour change. Minimal information in these intense instances appears to gain maximum impacts—so interpretive staff should let the oceans speak! However, as the intensity of wildlife experiences decrease, the quality and presence of interpretation in wild dolphin encounters play a greater part in enhancing overall satisfaction, knowledge of participants, pro-environmental attitudes and beliefs, and intended behaviours and actions. Therefore, as the intensity level of wild dolphin encounters decrease, guides need to deliver increasingly high quality commentaries as essential inputs of the tourist experience.

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Bromeliad Malaria in Trinidad, British West Indies
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Summary Lutz (1903) first considered the possibility that anopheline mosquitoes of the subgenus Kerteszia might be involved in malaria transmission. He concluded, on epidemiological grounds, that Anopheles lutzi Theobald (= cruzi D. & K.) was a vector in Sao Paulo. However, Knab, stressing the connection between the feeding habits of insects and their importance as vectors of disease strongly opposed Lutz's view, maintaining that since Anopheles lutzi was a forest mosquito it would not have sufficient contact with man to transmit malaria. Independently, Urich and later de Verteuil believed that Anopheles (Kerteszia) bellator D. & K. was involved in the malaria complex in Trinidad, and this was confirmed eventually by Rozeboom and Laird, and also by Downs, Gillette, and Shannon. It is shown that in spite of the fact that Anopheles bellator is a forest mosquito it is intimately associated with man in the cacao areas of Trinidad. Two principal factors are adduced to account for this contact: in the first place Anopheles bellator inhabits the drier microclimates of the forest and is therefore able to leave forest as such for the drier conditions offered by cacao estates and the open spaces in the villages; secondly, the cacao industry has brought relatively large human settlements into immediate contact with the forests of cacao and immortelle trees, which support both larval and adult populations of A. bellator and heavy growths of water-holding bromeliads in which the anophelines breed. The breeding of A. bellator is restricted to certain bromeliad species. Its absence in some very common species such as Aechmea nudicaulis is a fact of practical importance. Again, bellator does not occur all over the island where forests and cacao estates exist. It is restricted to areas of high rainfall. In discussing control problems the writers do not consider that the simple removal of plants by hand could ever be adopted as a regular control procedure. It is too slow, expensive, and dangerous. It is shown that copper sulphate may be used as a selective herbicidal spray to destroy the bromeliad infestations without damaging the commercially important cacao trees or the immortelles. In field practice the heavy spraying equipment developed by the United States Department of Agriculture for the control of the gypsy moth is found to be highly satisfactory. This control method is much faster, cheaper, and safer than removal of bromeliads by hand. Finally it is pointed out that a change in agricultural practice, namely, the abandonment of interplanted immortelle shade trees and the adoption of windbreaks, would remove the ecological basis of the disease, which is the microclimatic condition produced by immortelle trees in existing cacao estates. Following such a change, which is now being encouraged by the Government of Trinidad and Tobago, endemic bromeliad malaria could be expected to disappear from the center of the island.

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Prey selection of offshore killer whales Orcinus orca in the Northeast Atlantic in late summer: spatial associations with mackerel
  • Mar 3, 2014
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The traditional perception of prey species preference of killer whales Orcinus orca L. in the Northeast Atlantic has, to a large extent, been linked to herring Clupea harengus L. Few studies have investigated the feeding ecology of killer whales from the offshore parts of this eco- system. We conducted 2 summer-season ecosystem-based surveys in the Norwegian Sea, when it is most crucial for these animals to build up their energy reserves, using observational, acoustic, oceanographic, plankton net, and pelagic trawl haul data to quantify any spatial overlap between killer whales and the 3 most common and abundant pelagic fish species: herring, mackerel Scomber scombrus L., and blue whiting Micromesistius poutassou R. No spatial relationships were found between killer whales and herring or blue whiting. However, there was a significant rela- tionship and spatial overlap between killer whales and mackerel. Feeding on this epipelagic schooling fish species during summer may incur lower migration costs and higher energetic gain than feeding on alternative prey. Killer whale group size was also correlated to the size of mack- erel trawl catches, indicating active group size adjustment to available prey concentrations.

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  • Jul 18, 2018
  • Proceedings of the Royal Society B: Biological Sciences
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The costs of predation may exert significant pressure on the mode of communication used by an animal, and many species balance the benefits of communication (e.g. mate attraction) against the potential risk of predation. Four groups of toothed whales have independently evolved narrowband high-frequency (NBHF) echolocation signals. These signals help NBHF species avoid predation through acoustic crypsis by echolocating and communicating at frequencies inaudible to predators such as mammal-eating killer whales. Heaviside's dolphins (Cephalorhynchus heavisidii) are thought to exclusively produce NBHF echolocation clicks with a centroid frequency around 125 kHz and little to no energy below 100 kHz. To test this, we recorded wild Heaviside's dolphins in a sheltered bay in Namibia. We demonstrate that Heaviside's dolphins produce a second type of click with lower frequency and broader bandwidth in a frequency range that is audible to killer whales. These clicks are used in burst-pulses and occasional click series but not foraging buzzes. We evaluate three different hypotheses and conclude that the most likely benefit of these clicks is to decrease transmission directivity and increase conspecific communication range. The expected increase in active space depends on background noise but ranges from 2.5 (Wenz Sea State 6) to 5 times (Wenz Sea State 1) the active space of NBHF signals. This dual click strategy therefore allows these social dolphins to maintain acoustic crypsis during navigation and foraging, and to selectively relax their crypsis to facilitate communication with conspecifics.

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1. Plasma thyroxine (T4), protein bound iodine (PBI), inorganic iodine, total iodine, thyroxine binding globulin (TGB), unsaturated TBG (resin T3 uptake test) and free thyroxine were measured in a series of tests on two species of porpoise (or dolphins) and two species of small whales. This was the first such work done on cetaceans. The values presented for the bottlenose dolphin, Tursiops truncatus, were derived from 86 plasma specimens from 31 different animals (Table 2) and should be clinically useful for the future diagnosis of thyroid disease in that species. 2. A total of twenty-four plasma specimens from the Pacific white-striped dolphin, Lagenorhynchus obliquidens (Fig. 3), the killer whale Orcinus area (Fig. 4) and the pilot whale Globicephala scammoni (Fig. 5) gave values that must be regarded as preliminary until a larger number of animals can be sampled. 3. All of these marine cetaceans have larger thyroids and smaller body surface areas than terresterial mammals of comparable weight. 4. In bottlenose dolphins and Pacific white-striped dolphins the total thyroid weight is about 2.25 times the total adrenal gland weight. The adrenals and the thyroid are both about one-third larger (on a gland weight to body weight basis) in Pacific white-striped dolphins. 5. Differences in water temperature of 6° C to 9° C did not appear to affect the plasma thyroid indices of bottlenose dolphins or killer whales (Fig. 4). A 72-hour fast caused an increase in plasma T4 levels of each of 3 bottlenose dolphins with an average rise of 1.2 μg/100 ml. 6. The high level of plasma T4 and PBI appear to correlate well with the relatively high metabolic rate observed in T. truncatus. However, the species that appears to have the highest metabolic rate, the Pacifie white-striped dolphin, Lagenorhynchus obliquidens (Fig. 3), had the lowest plasma level of T4, PBI, total iodine, TGB capacity and cholesterol (Table 2). This data points out the need for a comprehensive study of thyroid function in wild and captive white-striped dolphins and other species that are difficult to maintain in captivity.

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  • Cite Count Icon 5
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Effects of grazing intensity and topography on species abundance distribution in a typical steppe of Inner Mongolia
  • Jan 1, 2014
  • Chinese Journal of Plant Ecology
  • Li Wen-Huai + 1 more

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Wide ranging and abundant species, often termed common species, play critically important roles in ecosystem functioning. However, conservation practice usually focuses on rare and declining species, including monitoring their state, while population trends of common and widespread species are often logistically difficult to evaluate compared to rare habitat specialists. This is particularly the case for small nocturnal vertebrates such as common amphibians, where abundance data are typically absent across most of their range. Building on previous work, we used national scale volunteer-collected data across Switzerland and Britain to investigate population trends over four decades for Europe’s two most common amphibian species, common toads (Bufo bufo) and common frogs (Rana temporaria). We included an average of 86 populations per year with an average count of 87,900 toads and 74,000 frogs in Switzerland and 80 populations per year with an average count of 75,800 toads in Britain, resulting in a total count of nearly 5.5 million toads across the entire study period. Overall, toad abundance declined in all decades since 1973 in Switzerland (33% abundance reduction) and since 1985 in Great Britain (41% reduction), but there were significant regional recoveries in Britain since 2013. Common frog abundance trends in Switzerland varied and remained positive overall but population growth rate declined after the year 2000. The impacts of such large-scale and ongoing abundance loss of common species may affect the ecosystem services provided by these species and require effective conservation action that expands beyond protected areas.

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  • Cite Count Icon 45
  • 10.1111/acv.12030
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  • Feb 7, 2013
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Natura 2000 (N2000) is a network of European sites focused on the conservation of specific species and habitats. Despite the known importance of common biodiversity in ecosystem functioning, common species are currently not explicitly targeted by conservation initiatives in France. In this study, we investigated whether the N2000 network contributes to the protection of common breeding bird species. In particular, we focused on species abundance and species specialization, community specialization and community trophic levels. We also determined the effects of N2000 on temporal trends of specialist and generalist bird groups. We studied 100 species in 1461 plots monitored by the French Breeding Bird Survey (BBS) between 2001 and 2010. We found that species abundance increased for 54 species with the proportion of the plot covered by N2000 areas in the plot. The bird species with the abundances that were most influenced by proportion of the plot covered by N2000 areas were predominantly habitat specialists. Bird communities inside N2000 sites were more specialized and exhibited higher trophic indices than communities outside N2000 sites. We found no differences in the temporal trends of farmland and woodland birds inside and outside N2000 sites, but the temporal trend of generalist species was positive outside N2000 sites and stable inside. We concluded that N2000 sites showed greater abundance of a majority of common bird species but that the network was established too recently to assess its influence on population trends. The French BBS has proved to be an efficient tool in assessing protected area networks.

  • Research Article
  • Cite Count Icon 690
  • 10.1046/j.1461-0248.2003.00454.x
Dominant species maintain ecosystem function with non‐random species loss
  • May 8, 2003
  • Ecology Letters
  • Melinda D Smith + 1 more

Loss of species caused by widespread stressors, such as drought and fragmentation, is likely to be non‐random depending on species abundance in the community. We experimentally reduced the number of rare and uncommon plant species while independently reducing only the abundance of dominant grass species in intact, native grassland. This allowed us to simulate a non‐random pattern of species loss, based on species abundances, from communities shaped by natural ecological interactions and characterized by uneven species abundance distributions. Over two growing seasons, total above‐ground net primary productivity (ANPP) declined with reductions in abundance of the dominant species but was unaffected by a threefold decline in richness of less common species. In contrast, productivity of the remaining rare and uncommon species decreased with declining richness, in part due to loss of complementary interactions among these species. However, increased production of the dominant grasses offset the negative effects of species loss. We conclude that the dominant species, as controllers of ecosystem function, can provide short‐term resistance to reductions in ecosystem function when species loss is nonrandom. However, the concurrent loss of complementary interactions among rare and uncommon species, the most diverse component of communities, may contribute to additional species loss and portends erosion of ecosystem function in the long term.

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