The influence of locus number and information content on species delimitation: an empirical test case in an endangered Mexican salamander

Perhaps the most important recent advance in species delimitation has been the development of model‐based approaches to objectively diagnose species diversity from genetic data. Additionally, the growing accessibility of next‐generation sequence data sets provides powerful insights into genome‐wide patterns of divergence during speciation. However, applying complex models to large data sets is time‐consuming and computationally costly, requiring careful consideration of the influence of both individual and population sampling, as well as the number and informativeness of loci on species delimitation conclusions. Here, we investigated how locus number and information content affect species delimitation results for an endangered Mexican salamander species, Ambystoma ordinarium. We compared results for an eight‐locus, 137‐individual data set and an 89‐locus, seven‐individual data set. For both data sets, we used species discovery methods to define delimitation models and species validation methods to rigorously test these hypotheses. We also used integrated demographic model selection tools to choose among delimitation models, while accounting for gene flow. Our results indicate that while cryptic lineages may be delimited with relatively few loci, sampling larger numbers of loci may be required to ensure that enough informative loci are available to accurately identify and validate shallow‐scale divergences. These analyses highlight the importance of striking a balance between dense sampling of loci and individuals, particularly in shallowly diverged lineages. They also suggest the presence of a currently unrecognized, endangered species in the western part of A. ordinarium's range.     

Simulations inform design of regional occupancy‐based monitoring for a sparsely distributed,territorial species

Sparsely distributed species attract conservation concern, but insufficient information on population trends challenges conservation and funding prioritization. Occupancy‐based monitoring is attractive for these species, but appropriate sampling design and inference depend on particulars of the study system. We employed spatially explicit simulations to identify minimum levels of sampling effort for a regional occupancy monitoring study design, using white‐headed woodpeckers (Picoides albolvartus), a sparsely distributed, territorial species threatened by habitat decline and degradation, as a case study. We compared the original design with commonly proposed alternatives with varying targets of inference (i.e., species range, space use, or abundance) and spatial extent of sampling. Sampling effort needed to achieve adequate power to observe a long‐term population trend (≥80% chance to observe a 2% yearly decline over 20 years) with the previously used study design consisted of annually monitoring ≥120 transects using a single‐survey approach or ≥90 transects surveyed twice per year using a repeat‐survey approach. Designs that shifted inference toward finer‐resolution trends in abundance and extended the spatial extent of sampling by shortening transects, employing a single‐survey approach to monitoring, and incorporating a panel design (33% of units surveyed per year) improved power and reduced error in estimating abundance trends. In contrast, efforts to monitor coarse‐scale trends in species range or space use with repeat surveys provided extremely limited statistical power. Synthesis and applications. Sampling resolutions that approximate home range size, spatially extensive sampling, and designs that target inference of abundance trends rather than range dynamics are probably best suited and most feasible for broad‐scale occupancy‐based monitoring of sparsely distributed territorial animal species.     

Hierarchical distance sampling to estimate population sizes of common lizards across a desert ecoregion

Multispecies wildlife monitoring across large geographical regions is important for effective conservation planning in response to expected impacts from climate change and land use. Unlike many species of birds, mammals, and amphibians which can be efficiently sampled using automated sensors including cameras and sound recorders, reptiles are often much more challenging to detect, in part because of their typically cryptic behavior and generally small body sizes. Although many lizard species are more active during the day which makes them easier to detect using visual encounter surveys, they may be unavailable for sampling during certain periods of the day or year due to their sensitivity to temperature. In recognition of these sampling challenges, we demonstrate application of a recent innovation in distance sampling that adjusts for temporary emigration between repeat survey visits. We used transect surveys to survey lizards at 229 sites throughout the Mojave Desert in California, USA, 2016. We estimated a total population size of 82 million (90% CI: 65–99 million) for the three most common species of lizards across this 66,830 km² ecoregion. We mapped how density at the 1‐km² scale was predicted to vary with vegetation cover and human development. We validated these results against independent surveys from the southern portion of our study area. Our methods and results demonstrate how multispecies monitoring programs spanning arid ecoregions can better incorporate information about reptiles.     

Evaluating the interaction of faecal pellet deposition rates and DNA degradation rates to optimize sampling design for DNA‐based mark–recapture analysis of Sonoran pronghorn

Knowledge of population demographics is important for species management but can be challenging in low‐density, wide‐ranging species. Population monitoring of the endangered Sonoran pronghorn (Antilocapra americana sonoriensis) is critical for assessing the success of recovery efforts, and noninvasive DNA sampling (NDS) could be more cost‐effective and less intrusive than traditional methods. We evaluated faecal pellet deposition rates and faecal DNA degradation rates to maximize sampling efficiency for DNA‐based mark–recapture analyses. Deposition data were collected at five watering holes using sampling intervals of 1–7 days and averaged one pellet pile per pronghorn per day. To evaluate nuclear DNA (nDNA) degradation, 20 faecal samples were exposed to local environmental conditions and sampled at eight time points from one to 124 days. Average amplification success rates for six nDNA microsatellite loci were 81% for samples on day one, 63% by day seven, 2% by day 14 and 0% by day 60. We evaluated the efficiency of different sampling intervals (1–10 days) by estimating the number of successful samples, success rate of individual identification and laboratory costs per successful sample. Cost per successful sample increased and success and efficiency declined as the sampling interval increased. Results indicate NDS of faecal pellets is a feasible method for individual identification, population estimation and demographic monitoring of Sonoran pronghorn. We recommend collecting samples >7 days old and estimate that a sampling interval of 4–7 days in summer conditions (i.e. extreme heat and exposure to UV light) will achieve desired sample sizes for mark–recapture analysis while also maximizing efficiency.     

Does asymmetric gene flow among matrilines maintain the evolutionary potential of the European eel?

Using evolutionary theory to predict the dynamics of populations is one of the aims of evolutionary conservation. In endangered species, with geographic range extending over continuous areas, the predictive capacity of evolutionary‐based conservation measures greatly depends on the accurate identification of reproductive units. The endangered European eel (Anguilla anguilla) is a highly migratory fish species with declining population due to a steep recruitment collapse in the beginning of the 1980s. Despite punctual observations of genetic structure, the population is viewed as a single panmictic reproductive unit. To understand the possible origin of the detected structure in this species, we used a combination of mitochondrial and nuclear loci to indirectly evaluate the possible existence of cryptic demes. For that, 403 glass eels from three successive cohorts arriving at a single location were screened for phenotypic and genetic diversity, while controlling for possible geographic variation. Over the 3 years of sampling, we consistently identified three major matrilines which we hypothesized to represent demes. Interestingly, not only we found that population genetic models support the existence of those matriline‐driven demes over a completely panmictic mode of reproduction, but also we found evidence for asymmetric gene flow amongst those demes. We uphold the suggestion that the detection of demes related to those matrilines reflect a fragmented spawning ground, a conceptually plausible consequence of the low abundance that the European eel has been experiencing for three decades. Furthermore, we suggest that this cryptic organization may contribute to the maintenance of the adaptive potential of the species.     

A low‐cost,yet simple and highly repeatable system for acoustically surveying cryptic species

Accurate determination of the population density of key focal species is necessary for monitoring the success of management programs and ecosystem health across a wide range of contexts. Unfortunately, many key taxa are visually cryptic and thus difficult to count using traditional observation‐based techniques. Bell miners (Manorina melanophrys), are just such a species. They are widespread throughout south‐eastern Australia, yet they are critical to monitor given their association and potential causal link to spreading vegetative dieback in this region. A new passive acoustic monitoring technique was trialled by testing its ability to determine population densities of bell miner colonies via counting the distinctive ‘tink’ vocalization of this species. This call was given at a constant rate per individual, and at a common amplitude across 10 colonies throughout the entire geographic range of the species. Theoretical sound transmission and playback trials through typical habitat determined that any bird within a 50‐m radius of the recorders used would be louder than 70 dB, enabling this threshold amplitude to be used to determine the number of birds in a 50 m radius of the recorder. Field trials of the acoustic protocol versus human observers using traditional visual surveys found that passive acoustic monitoring was able to detect more individuals, using a less expensive protocol that drastically reduced the need for observer training or expertise. Sound therefore offers a reliable method for determining the density of this vocal, but visually cryptic species. We present methods for calibrating recording devices and detecting calls louder than species‐specific thresholds using readily available freeware, enabling our methods to be easily adapted to census a variety of acoustically distinctive species, offering a more effective, yet lower cost and in our case more efficient census technique for surveying difficult species.     

Monitoring marine macroalgae: the influence of spatial scale on the usefulness of biodiversity surrogates

Aim To examine the influence of spatial scale on the usefulness of commonly employed biodiversity surrogates in subtidal macroalgae assemblages. Location South‐west Australia. Methods The relationship between biodiversity surrogates and univariate and multivariate species‐level patterns was tested at multiple spatial scales, ranging from metres (between quadrats) to hundreds of kilometres (between regions), using samples collected from almost 2000 km of temperate coastline that represented almost 300 species. Biodiversity surrogates included commonly used cost‐effective alternatives to species‐level sampling, such as those derived from functional groups and from taxonomic aggregation. Results Overall, surrogates derived from taxonomic aggregation to genus or family level correlated strongly with species‐level patterns, although the family‐level surrogate was a less effective predictor of species richness at large spatial scales. Surrogates derived from aggregation to coarser taxonomic levels and functional groups performed poorly, while the effectiveness of a surrogate measure derived from canopy‐forming species improved with increasing spatial scale. Main conclusions A critical, but rarely examined, assumption of biodiversity surrogates is that the relationship between surrogate and species‐level patterns is consistent in both space and time, and across a range of spatial and temporal scales. As the performance of all surrogates was, to some degree, scale‐dependent, this work empirically demonstrated the need to consider the spatial extent and design of any biodiversity monitoring programme when choosing cost‐effective alternatives to species‐level data collection.     

Vessel noise cuts down communication space for vocalizing fish and marine mammals

Anthropogenic noise across the world's oceans threatens the ability of vocalizing marine species to communicate. Some species vocalize at key life stages or whilst foraging, and disruption to the acoustic habitat at these times could lead to adverse consequences at the population level. To investigate the risk of these impacts, we investigated the effect of vessel noise on the communication space of the Bryde's whale Balaenoptera edeni, an endangered species which vocalizes at low frequencies, and bigeye Pempheris adspersa, a nocturnal fish species which uses contact calls to maintain group cohesion while foraging. By combining long‐term acoustic monitoring data with AIS vessel‐tracking data and acoustic propagation modelling, the impact of vessel noise on their communication space was determined. Routine vessel passages cut down communication space by up to 61.5% for bigeyes and 87.4% for Bryde's whales. This influence of vessel noise on communication space exceeded natural variability for between 3.9 and 18.9% of the monitoring period. Additionally, during the closest point of approach of a large commercial vessel, <10 km from the listening station, the communication space of both species was reduced by a maximum of 99% compared to the ambient soundscape. These results suggest that vessel noise reduces communication space beyond the evolutionary context of these species and may have chronic effects on these populations. To combat this risk, we propose the application or extension of ship speed restrictions in ecologically significant areas, since our results indicate a reduction in sound source levels for vessels transiting at lower speeds.     

Interspecies interference and monitoring duration affect detection rates in chew cards

Pest monitoring methods should provide unbiased accurate estimates of pest densities and locations, while also minimizing time‐in‐field and costs. Recent pest mammal monitoring studies have found that chew cards are more effective than conventional mammal monitoring methods, but little experimental work has been done to determine optimal experimental duration or quantify the risks of saturation by one species biasing detections of other species. Here, we used chew cards in three sites within Awarua wetland (Southland, New Zealand) to investigate the optimal amount of time required to detect targeted pest species (rats, possums and mice), and to examine the potential of rats and possums to bias detection rates of other species. We found depressed detections of possums and rats where a contraspecific had been detected on a card, which is consistent with previous studies of a similar duration on interspecies interference. This experiment is the first to analyse the rates at which species detections accrue over the course of a survey, and we found rat detections lagged behind possums for the first four nights. We modelled the effect of survey duration and relative rat abundance on the likelihood of further possum detections. Duration and rat abundance interacted, meaning there are trade‐offs to be considered with regard to duration: shorter durations may avoid the risk of saturation in areas of high pest density, but risk not sampling sparse or neophobic populations. Our data suggest that chew cards remain one of the most sensitive pest monitoring tools for rats and possums, compared to conventional methods such as tracking tunnels and wax tags. In areas of moderate pest densities, we suggest that a duration of five nights is optimal for detecting pests. However, in areas of high pest density the sensitivity of chew cards may render them unsuitable because of saturation and interspecies interference effects.     

Some ‘ant’swers: Application of a layered barcode approach to problems in ant taxonomy

DNA barcoding has emerged as a routine tool in modern taxonomy. Although straightforward, this approach faces new challenges, when applied to difficult situation such as defining cryptic biodiversity. Ants are prime examples for high degrees of cryptic biodiversity due to complex population differentiation, hybridization and speciation processes. Here, we test the DNA barcoding region, cytochrome c oxidase 1 and two supplementary markers, 28S ribosomal DNA and long‐wavelength rhodopsin, commonly used in ant taxonomy, for their potential in a layered, character‐based barcoding approach across different taxonomic levels. Furthermore, we assess performance of the character‐based barcoding approach to determine cryptic species diversity in ants. We found (i) that the barcode potential of a specific genetic marker varied widely among taxonomic levels in ants; (ii) that application of a layered, character‐based barcode for identification of specimens can be a solution to taxonomical challenging groups; (iii) that the character‐based barcoding approach allows us to differentiate specimens even within locations based on pure characters. In summary, (layered) character‐based barcoding offers a reliable alternative for problematic species identification in ants and can be used as a fast and cost‐efficient approach to estimate presence, absence or frequency of cryptic species.     

Genetic signatures through space,time and multiple disturbances in a ubiquitous brooding coral

The predominance of self‐recruitment in many reef‐building corals has fundamental and complex consequences for their genetic diversity, population persistence and responses to climate change. Knowledge of genetic structure over local scales needs to be placed within a broad spatial context, and also integrated with genetic monitoring through time to disentangle these consequences. Here, we examined patterns of genetic diversity over multiple spatio‐temporal scales across tropical Australia in the ubiquitous brooding coral, Seriatopora hystrix. We also analysed complimentary environmental and demographic data to elucidate the seascape drivers of these patterns. Large genetic differences were detected between the east vs. west coasts of Australia. In northwest Australia, geographic differentiation dominated genetic structure over multiple scales. However, three sympatric lineages were detected at the largest offshore reef system (Scott Reef). Similar to the differences observed among putative species in eastern Australia, these lineages were associated with different levels of wave exposure. Local genetic structure within the Scott Reef system was relatively stable over 10 years, but temporal differences were observed that reflected small but important genetic changes over a few generations during recovery after severe bleaching. These results highlight the importance of self‐recruitment together with occasional longer distance connectivity for the persistence of a metapopulation across spatially and temporally variable environments. Our multidimensional research provides a foundation for further long‐term genetic monitoring to inform conservation strategies and highlights that sampling scales, ecological effects and cryptic diversity are important considerations to develop realistic understanding of the evolutionary resilience of corals.     

Survival estimation of a cryptic antelope via photographic capture–recapture

Adult survival is a primary determinant of abundance and dynamics of large herbivore populations. For species that are inconspicuous, however, accurate survival estimation depends on accommodating low detection probability. For species with individually recognizable markings, photographic capture–recapture (CR) provides an approach to estimate population parameters while accounting for imperfect detection. I investigated the use of photographic CR for a cryptic large herbivore, the nyala, in a region of Hluhluwe–iMfolozi Park, South Africa. I conducted photographic sampling based on the closed robust design, with 5–6 daily sampling occasions nested within three week‐long sampling periods, which delineated one dry and one wet season. Detection differed between sexes: encounter probability of female adults depended on whether individuals fell into high‐encounter (seasonal range: 0.61–0.71) or low‐encounter (seasonal range: 0.29–0.40) groups, whereas male adults had a constant encounter probability of 0.39 per day. For both sexes, monthly survival probability was ≥0.93 and did not differ appreciably between seasons or sexes. Given the role of survival in population dynamics, photographic CR has the potential to provide survival estimates for cryptic large herbivores that lack such information.     

Modelling variation in calling rates to develop a reliable monitoring method for the Australasian Bittern Botaurus poiciloptilus

Monitoring the abundance of cryptic species inevitably relies on the use of index methods. Unfortunately, detectability is often confounded by unidentified covariates. One such species is the critically endangered Australasian Bittern Botaurus poiciloptilus. Current monitoring relies upon the ability to count males based on the conspicuous breeding calls of males. However, as in many vocal species, calling rates vary spatially and temporally, making it necessary to account for this when using call counts to index abundance. We undertook 461 15‐min call counts of Australasian Bitterns, in a range of conditions, during two breeding seasons at Whangamarino wetland, New Zealand. We fitted a range of generalized linear mixed models to these data to determine which factors were the best predictors of calling rate per individual Bittern (CRPI), allowing us to make recommendations regarding the optimum time and conditions for monitoring. Bittern CRPI was predictable in terms of time of day, month, cloud cover, rainfall and certain moon parameters, but some spatial and temporal variation remained unexplained. Results showed that the best time to detect Australasian Bitterns was 1 h before sunrise, in September (austral spring), on a moonlit night with no cloud or rain. Such models are useful for identifying times and conditions when counts are the highest and least variable, and could be applied to any species or cue count monitoring method where detection depends on counting calling individuals. Results can be used to standardize index counts, or sensibly to adjust and compare counts from different times. Standardizing monitoring in this way can lead to the development of monitoring methods that have a greater power to show population changes across shorter time periods. Moreover, the use of modelling processes to estimate effect sizes creates potential for such methods to be applied in circumstances where monitoring conditions are rarely optimum and standardization creates logistical trade‐offs, something that is particularly common in studies of cryptic species.     

Algorithmic single‐locus species delimitation: effects of sampling effort,variation and nonmonophyly in four methods and 1870 species of beetles

The vast number of undescribed species and the fast rate of biodiversity loss call for new approaches to speed up alpha taxonomy. A plethora of methods for delimiting species or operational taxonomic units (OTUs) based on sequence data have been published in recent years. We test the ability of four delimitation methods (BIN, ABGD, GMYC, PTP) to reproduce established species boundaries on a carefully curated DNA barcode data set of 1870 North European beetle species. We also explore how sampling effort, intraspecific variation, nearest neighbour divergence and nonmonophyly affect the OTU delimitations. All methods produced approximately 90% identity between species and OTUs. The effects of variation and sampling differed between methods. ABGD was sensitive to singleton sequences, while GMYC showed tendencies for oversplitting. The best fit between species and OTUs was achieved using simple rules to find consensus between discordant OTU delimitations. Using several approaches simultaneously allows the methods to compensate for each other's weaknesses. Barcode‐based OTU‐picking is an efficient way to delimit putative species from large data sets where the use of more sophisticated methods based on multilocus or genomic data is not feasible.     

Temporally adaptive acoustic sampling to maximize detection across a suite of focal wildlife species

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Acoustic detection and acoustic habitat characterisation of the critically endangered white-bellied heron (Ardea insignis) in Bhutan

1. Growing developmental activities, such as hydropower construction, farm roads, and other human activities, are affecting the critically endangered white-bellied heron (WBH). Out of a known global population of 60, 28 individuals inhabit the river basin area and freshwater lakes and ponds of Bhutan. Several constraints impede continuous monitoring of endangered species, such as the isolated and cryptic nature of the species and the remoteness of its habitat; to date, there are no long-term reference data or techniques implemented for continuous monitoring of this species.
2. In this study, we designed acoustic detection and habitat characterisation methods using long-duration recordings from three habitat areas in Bhutan. Acoustic indices were extracted and used to implement a species-specific call detector and to generate habitat soundscape representations. Using WBH calls annotated in month-long recordings from a known site, a novel indices-based detector was implemented and tested. A total of 960 hr of continuous audio recordings from three habitats in Bhutan were analysed.
3. We found that a species call detector implemented using a combination of acoustic indices (that includes measures of spectral and temporal entropy and different angles of spectral ridges) has a correct detection rate of 81%. Additionally, visual inspection of the species’ acoustic habitat using long-duration false-colour spectrograms enabled qualitative assessment of acoustic habitat structure and other dominant acoustic events.
4. This study proposes a combined approach of species acoustic detection and habitat soundscape analysis for holistic acoustic monitoring of endangered species. As a direct outcome of this work, we documented acoustic reference data on the critically endangered WBH from multiple habitat areas and have analysed its temporal vocalisation patterns across sites.

     

Optimizing ultrasonic sampling effort for monitoring forest bats

Landscape‐scale monitoring is a key approach for assessing changes in indicators. However, great care needs to be taken to collect rigorous data and avoid wasting resources in long‐term programmes. Insect‐eating bats are diverse, functionally important and are often proposed as indicator species of environmental health. We used acoustic (ultrasonic) data from pilot bat surveys undertaken in forests and woodlands to optimize sampling effort to produce precise estimates of bat activity and occupancy. We also carried out simulations to evaluate the statistical power of different sampling designs to detect changes in activity and occupancy levels of individual bat species. There was little gain in precision for estimates of bat activity by sampling beyond five to six detector nights. To ensure spatial heterogeneity was sampled around a monitoring point, three detectors for two nights or two detectors for three nights would be required. This level of sampling was also sufficient to be 90% certain of recording occupancy for 11 of 12 taxa. Power simulations revealed that a sampling design using two detectors per monitoring point for two nights could detect a 30% decline within 10 years with 90% power for all species, except the white‐striped free tail bat (Tadarida australis), using either changes in activity levels or occupancy. However, fewer years were required when using occupancy. Setting detectors either on‐flyways or off‐flyways contributed only minor differences to the time taken to reach 90% power for both occupancy and activity levels, though sampling both locations has major implications for interpreting trends in bats. We suggest that bat activity levels are more sensitive for detecting change than occupancy because one pass or 1000 passes can be recorded per night by an acoustic detector, and this is not differentiated by occupancy. Bats can be monitored cost‐effectively and should be included in monitoring programmes.     

The Promise and Practicality of Population Genomics Research with Endangered Species

Recent technological advances have dramatically reduced the cost of DNA sequencing. In addition, these methods require lower DNA quantities and qualities than did the previous generation of molecular techniques. As a result, genomic-scale studies of natural populations of endangered species, including those using noninvasively collected samples, are increasingly feasible. Such studies have the potential to advance our understanding of behavior, demography, evolutionary ecology, biogeography, and population history, and to contribute to the prioritization of conservation efforts. I point to a number of salient examples. However, there are also some current limitations and challenges associated with this scale of population genomics research in nonhuman, nonmodel species. Here, I describe the practicalities of the present state of this research while providing what is intended to be a straightforward walkthrough of the technology and methods involved.     

Pedigree analysis for the genetic management of group‐living species

Captive breeding programs are an important tool for the conservation of endangered species. These programs are commonly managed using pedigrees containing information about the history of each individual's family, such as breeding pairs and parentage. However, there are some species that are kept in groups where it is hard to distinguish between particular individuals within the group, making it very difficult to record any information at an individual level. Currently, software and methods commonly used for registering and analyzing pedigrees to help manage populations at an individual level are not adequate for managing these group‐living species. Therefore, there is a need to further develop these tools and methodologies for pedigree analysis to better manage group‐living species. PMx is a program used for the management of ex situ populations in zoos and aquariums. We adapted the pedigree analysis method implemented in PMx to analyze pedigrees (records of descendant lineages) of group‐living species. In addition, we developed a group pedigree data entry sheet and group2PMx, a converter program that enables group datasets to be imported into PMx. We show how pedigree analysis of a group‐living species can be used for population management using the studbook of the endangered Texas blind cave salamander Eurycea rathbuni. Such analyses of the pedigree of groups can improve the management of group‐living species in ex situ breeding programs. Firstly, it enables better management decisions based on more accurate genetic measures between groups, allowing for greater control of inbreeding. Secondly, it can improve the conditions in which group‐living species are held by adapting husbandry practices to better reflect conditions of these species living in the wild. The use of the spreadsheet and group2PMx extends the application of PMx_, allowing conservation managers and other institutions outside the zoo and aquarium community to easily import and analyze their pedigree data.