Environmental DNA - An emerging tool in conservation for monitoring past and present biodiversity

The genomic revolution has fundamentally changed how we survey biodiversity on earth. High-throughput sequencing ("HTS") platforms now enable the rapid sequencing of DNA from diverse kinds of environmental samples (termed "environmental DNA" or "eDNA"). Coupling HTS with our ability to associate sequences from eDNA with a taxonomic name is called "eDNA metabarcoding" and offers a powerful molecular tool capable of noninvasively surveying species richness from many ecosystems. Here, we review the use of eDNA metabarcoding for surveying animal and plant richness, and the challenges in using eDNA approaches to estimate relative abundance. We highlight eDNA applications in freshwater, marine and terrestrial environments, and in this broad context, we distill what is known about the ability of different eDNA sample types to approximate richness in space and across time. We provide guiding questions for study design and discuss the eDNA metabarcoding workflow with a focus on primers and library preparation methods. We additionally discuss important criteria for consideration of bioinformatic filtering of data sets, with recommendations for increasing transparency. Finally, looking to the future, we discuss emerging applications of eDNA metabarcoding in ecology, conservation, invasion biology, biomonitoring, and how eDNA metabarcoding can empower citizen science and biodiversity education.

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Environmental DNA metabarcoding: transforming how we survey animal and plant communities

Extraction and identification of DNA from an environmental sample has proven noteworthy recently in detecting and monitoring not only common species, but also those that are endangered, invasive, or elusive. Particular attributes of so-called environmental DNA (eDNA) analysis render it a potent tool for elucidating mechanistic insights in ecological and evolutionary processes. Foremost among these is an improved ability to explore ecosystem-level processes, the generation of quantitative indices for analyses of species, community diversity, and dynamics, and novel opportunities through the use of time-serial samples and unprecedented sensitivity for detecting rare or difficult-to-sample taxa. Although technical challenges remain, here we examine the current frontiers of eDNA, outline key aspects requiring improvement, and suggest future developments and innovations for research.

https://www.cell.com/trends/ecology-evolution/pdf/S0169-5347(14)00086-X.pdf

Environmental DNA for wildlife biology and biodiversity monitoring

Ocean ambient noise results from both anthropogenic and natural sources. Different noise sources are dominant in each of 3 frequency bands: low (10 to 500 Hz), medium (500 Hz to 25 kHz) and high (>25 kHz). The low-frequency band is dominated by anthropogenic sources: pri- marily, commercial shipping and, secondarily, seismic exploration. Shipping and seismic sources con- tribute to ambient noise across ocean basins, since low-frequency sound experiences little attenua- tion, allowing for long-range propagation. Over the past few decades the shipping contribution to ambient noise has increased by as much as 12 dB, coincident with a significant increase in the num- ber and size of vessels comprising the world's commercial shipping fleet. During this time, oil explo- ration and construction activities along continental margins have moved into deeper water, and the long-range propagation of seismic signals has increased. Medium frequency sound cannot propagate over long ranges, owing to greater attenuation, and only local or regional (10s of km distant) sound sources contribute to the ambient noise field. Ambient noise in the mid-frequency band is primarily due to sea-surface agitation: breaking waves, spray, bubble formation and collapse, and rainfall. Var- ious sonars (e.g. military and mapping), as well as small vessels, contribute anthropogenic noise at mid-frequencies. At high frequencies, acoustic attenuation becomes extreme so that all noise sources are confined to an area close to the receiver. Thermal noise, the result of Brownian motion of water molecules near the hydrophone, is the dominant noise source above about 60 kHz.

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Anthropogenic and natural sources of ambient noise in the ocean

The underwater environment is filled with biotic and abiotic sounds, many of which can be important for the survival and reproduction of fish. Over the last century, human activities in and near the water have increasingly added artificial sounds to this environment. Very loud sounds of relatively short exposure, such as those produced during pile driving, can harm nearby fish. However, more moderate underwater noises of longer duration, such as those produced by vessels, could potentially impact much larger areas, and involve much larger numbers of fish. Here we call attention to the urgent need to study the role of sound in the lives of fish and to develop a better understanding of the ecological impact of anthropogenic noise.

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A noisy spring: the impact of globally rising underwater sound levels on fish

The demand for renewable energy has led to construction of offshore wind farms with high-power turbines, and many more wind farms are being planned for the shallow waters of the world's marine habitats. The growth of offshore wind farms has raised concerns about their impact on the marine environment. Marine mammals use sound for foraging, orientation and communication and are therefore possibly susceptible to negative effects of man-made noise generated from con- structing and operating large offshore wind turbines. This paper reviews the existing literature and assesses zones of impact from different noise-generating activities in conjunction with wind farms on 4 representative shallow-water species of marine mammals. Construction involves many types of activities that can generate high sound pressure levels, and pile-driving seems to be the noisiest of all. Both the literature and modeling show that pile-driving and other activities that generate intense impulses during construction are likely to disrupt the behavior of marine mammals at ranges of many kilometers, and that these activities have the potential to induce hearing impairment at close range. The reported noise levels from operating wind turbines are low, and are unlikely to impair hearing in marine mammals. The impact zones for marine mammals from operating wind turbines depend on the low-frequency hearing-abilities of the species in question, on sound-propagation conditions, and on the presence of other noise sources such as shipping. The noise impact on marine mammals is more severe during the construction of wind farms than during their operation.

/pdf/wind-turbine-underwater-noise-and-marine-mammals-54ysvpbdey.pdf

Wind turbine underwater noise and marine mammals: implications of current knowledge and data needs

Traditionally, sperm whale clicks have been described as multipulsed, long duration, nondirectional signals of moderate intensity and with a spectrum peaking below 10 kHz. Such properties are counterindicative of a sonar function, and quite different from the properties of dolphin sonar clicks. Here, data are presented suggesting that the traditional view of sperm whale clicks is incomplete and derived from off-axis recordings of a highly directional source. A limited number of assumed on-axis clicks were recorded and found to be essentially monopulsed clicks, with durations of 100 micros, with a composite directionality index of 27 dB, with source levels up to 236 dB re: 1 microPa (rms), and with centroid frequencies of 15 kHz. Such clicks meet the requirements for long-range biosonar purposes. Data were obtained with a large-aperture, GPS-synchronized array in July 2000 in the Bleik Canyon off Vesteralen, Norway (69 degrees 28' N, 15 degrees 40' E). A total of 14 h of sound recordings was collected from five to ten independent, simultaneously operating recording units. The sound levels measured make sperm whale clicks by far the loudest of sounds recorded from any biological source. On-axis click properties support previous work proposing the nose of sperm whales to operate as a generator of sound.

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The monopulsed nature of sperm whale clicks

The exploitation of non-invasive samples has been widely used in genetic monitoring of terrestrial species. In aquatic ecosystems, non-invasive samples such as feces, shed hair or skin, are less accessible. However, the use of environmental DNA (eDNA) has recently been shown to be an effective tool for genetic monitoring of species presence in freshwater ecosystems. Detecting species in the marine environment using eDNA potentially offers a greater challenge due to the greater dilution, amount of mixing and salinity compared with most freshwater ecosystems. To determine the potential use of eDNA for genetic monitoring we used specific primers that amplify short mitochondrial DNA sequences to detect the presence of a marine mammal, the harbor porpoise, Phocoena phocoena, in a controlled environment and in natural marine locations. The reliability of the genetic detections was investigated by comparing with detections of harbor porpoise echolocation clicks by static acoustic monitoring devices. While we were able to consistently genetically detect the target species under controlled conditions, the results from natural locations were less consistent and detection by eDNA was less successful than acoustic detections. However, at one site we detected long-finned pilot whale, Globicephala melas, a species rarely sighted in the Baltic. Therefore, with optimization aimed towards processing larger volumes of seawater this method has the potential to compliment current visual and acoustic methods of species detection of marine mammals.

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Investigating the Potential Use of Environmental DNA (eDNA) for Genetic Monitoring of Marine Mammals

In sperm whales (Physeter catodon L. 1758) the nose is vastly hypertrophied, accounting for about one-third of the length or weight of an adult male. Norris and Harvey [in Animal Orientation and Navigation, NASA SP-262 (1972), pp. 397–417] ascribed a sound-generating function to this organ complex. A sound generator weighing upward of 10 tons and with a cross-section of 1 m is expected to generate high-intensity, directional sounds. This prediction from the Norris and Harvey theory is not supported by published data for sperm whale clicks (source levels of 180 dB re 1 μPa and little, if any, directionality). Either the theory is not borne out or the data is not representative for the capabilities of the sound-generating mechanism. To increase the amount of relevant data, a five-hydrophone array, suspended from three platforms separated by 1 km and linked by radio, was deployed at the slope of the continental shelf off Andenes, Norway, in the summers of 1997 and 1998. With this system, source levels up to 223 dB re 1 μPa peRMS were recorded. Also, source level differences of 35 dB for the same click at different directions were seen, which are interpreted as evidence for high directionality. This implicates sonar as a possible function of the clicks. Thus, previously published properties of sperm whale clicks underestimate the capabilities of the sound generator and therefore cannot falsify the Norris and Harvey theory.

Sperm whale clicks: Directionality and source level revisited

Increasing numbers and speeds of vessels in areas with populations of cetaceans may have the cumulative effect of reducing habitat quality by increasing the underwater noise level. Here, we first use digital acoustic tags to demonstrate that free-ranging delphinids in a coastal deep- water habitat are subjected to varying and occasionally intense levels of vessel noise. Vessel noise and sound propagation measurements from a shallow-water habitat are then used to model the potential impact of high sound levels from small vessels on delphinid communication in both shallow and deep habitats, with bottlenose dolphins Tursiops sp. and short-finned pilot whales Globicephala macrorhynchus as model organisms. We find that small vessels travelling at 5 knots in shallow water can reduce the communication range of bottlenose dolphins within 50 m by 26%. Pilot whales in a quieter deep-water habitat could suffer a reduction in their communication range of 58% caused by a vessel at similar range and speed. Increased cavitation noise at higher speeds drastically increases the impact on the communication range. Gear shifts generate high-level transient sounds (peak- peak source levels of up to 200 dB re 1 µPa) that may be audible over many kilometres and may dis- turb close-range animals. We conclude that noise from small vessels can significantly mask acousti- cally mediated communication in delphinids and contribute to the documented negative impacts on animal fitness.

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Magnus Wahlberg

Papers

Wind turbine underwater noise and marine mammals: implications of current knowledge and data needs

The monopulsed nature of sperm whale clicks

Investigating the Potential Use of Environmental DNA (eDNA) for Genetic Monitoring of Marine Mammals

Sperm whale clicks: Directionality and source level revisited

Vessel noise effects on delphinid communication