Non-focal Species Research Articles

Effects of shark tourism on the daily residency and movements of a non-focal pelagic teleost

Marine wildlife tourism is increasing in popularity, with operations targeting a wide range of taxa globally. While previous studies have mostly focused on assessing the effects of provisioning from tourism on focal species, non-focal species that unintentionally feed on supplemental food sources have largely been overlooked. This study improves our understanding of the effects of shark-cage-diving tourism on the movements and behaviours of a non-focal pelagic fish. We used acoustic tracking to determine the effects of shark-cage-diving tourism on the residency and space use of 17 yellowtail kingfish Seriola lalandi at the Neptune Islands, South Australia. We revealed that while cage-diving did not affect the overall or weekly residency and space use of kingfish, daily time spent at the islands and location of kingfish was influenced by the presence of operators. Acoustic attractant did not affect kingfish behaviours, but operators using food-based attractants increased the average time spent at the Neptune Islands by ~27% (from 230.6 ± 6.8 to 293.8 ± 5.5 min). Kingfish were also observed closer to operators using food-based attractants (217 ± 4.82 m from vessel) compared to an acoustic attractant (412 ± 29.5 m from vessel). Our findings identify changes in the daily behaviour of kingfish at the Neptune Islands as a result of food-based attractants from shark-cage-diving, which demonstrates that non-focal large pelagic species can be affected by shark-diving tourism. These effects may lead to long-term effects on the physiological condition and energetic responses of these individuals.

Re-emphasizing mechanism in the community ecology of disease.

1. Hosts and their parasites exist within complex ecological communities. However, the role that non-focal community members, species which cannot be infected by a focal pathogen, may play in altering parasite transmission is often only studied in the lens of the "diversity-disease" relationship by focusing on species richness. This approach largely ignores mechanistic species interactions and risks collapsing our understanding of the community ecology of disease down to defining the prominence of "amplification" vs. "dilution" effects. 2. However, non-focal species vary in their traits, densities, and types of interactions with focal hosts and parasites. Therefore, a community ecology approach based on the mechanisms underlying parasite transmission, host harm, and dynamic species interactions may better advance our understanding of parasite transmission in complex communities. 3. Using the concept of the parasite's basic reproductive ratio, R0, as a generalizable framework, we examine several critical mechanisms by which interactions among hosts, parasites, and non-focal species modulate transmission and provide examples from relevant literature. 4. By focusing on the mechanism by which non-focal species impact transmission, we can emphasize the similarities among classic paradigms in the community ecology of disease, gain new insights into parasite invasion and persistence, community traits correlated with disease dilution or amplification, and the feasibility of biocontrol for parasites of conservation, agricultural, or human health concern.

Quantitative Airborne Inventories in Dense Tropical Forest Using Imaging Spectroscopy

Tropical forests have exceptional floristic diversity, but their characterization remains incomplete, in part due to the resource intensity of in-situ assessments. Remote sensing technologies can provide valuable, cost-effective, large-scale insights. This study investigates the combined use of airborne LiDAR and imaging spectroscopy to map tree species at landscape scale in French Guiana. Binary classifiers were developed for each of 20 species using linear discriminant analysis (LDA), regularized discriminant analysis (RDA) and logistic regression (LR). Complementing visible and near infrared (VNIR) spectral bands with short wave infrared (SWIR) bands improved the mean average classification accuracy of the target species from 56.1% to 79.6%. Increasing the number of non-focal species decreased the success rate of target species identification. Classification performance was not significantly affected by impurity rates (confusion between assigned classes) in the non-focal class (up to 5% of bias), provided that an adequate criterion was used for adjusting threshold probability assignment. A limited number of crowns (30 crowns) in each species class was sufficient to retrieve correct labels effectively. Overall canopy area of target species was strongly correlated to their basal area over 118 ha at 1.5 ha resolution, indicating that operational application of the method is a realistic prospect (R2 = 0.75 for six major commercial tree species).

Linking demographic and food-web models to understand management trade-offs.

Alternatives in ecosystem‐based management often differ with respect to trade‐offs between ecosystem values. Ecosystem or food‐web models and demographic models are typically employed to evaluate alternatives, but the approaches are rarely integrated to uncover conflicts between values. We applied multistate models to a capture–recapture dataset on common guillemots Uria aalge breeding in the Baltic Sea to identify factors influencing survival. The estimated relationships were employed together with Ecopath‐with‐Ecosim food‐web model simulations to project guillemot survival under six future scenarios incorporating climate change. The scenarios were based on management alternatives for eutrophication and cod fisheries, issues considered top priority for regional management, but without known direct effects on the guillemot population. Our demographic models identified prey quantity (abundance and biomass of sprat Sprattus sprattus) as the main factor influencing guillemot survival. Most scenarios resulted in projections of increased survival, in the near (2016–2040) and distant (2060–2085) future. However, in the scenario of reduced nutrient input and precautionary cod fishing, guillemot survival was projected to be lower in both future periods due to lower sprat stocks. Matrix population models suggested a substantial decline of the guillemot population in the near future, 24% per 10 years, and a smaller reduction, 1.1% per 10 years, in the distant future. To date, many stakeholders and Baltic Sea governments have supported reduced nutrient input and precautionary cod fishing and implementation is underway. Negative effects on nonfocal species have previously not been uncovered, but our results show that the scenario is likely to negatively impact the guillemot population. Linking model results allowed identifying trade‐offs associated with management alternatives. This information is critical to thorough evaluation by decision‐makers, but not easily obtained by food‐web models or demographic models in isolation. Appropriate datasets are often available, making it feasible to apply a linked approach for better‐informed decisions in ecosystem‐based management.

Persistence and extinction for stochastic ecological models with internal and external variables.

The dynamics of species' densities depend both on internal and external variables. Internal variables include frequencies of individuals exhibiting different phenotypes or living in different spatial locations. External variables include abiotic factors or non-focal species. These internal or external variables may fluctuate due to stochastic fluctuations in environmental conditions. The interplay between these variables and species densities can determine whether a particular population persists or goes extinct. To understand this interplay, we prove theorems for stochastic persistence and exclusion for stochastic ecological difference equations accounting for internal and external variables. Specifically, we use a stochastic analog of average Lyapunov functions to develop sufficient and necessary conditions for (i) all population densities spending little time at low densities i.e. stochastic persistence, and (ii) population trajectories asymptotically approaching the extinction set with positive probability. For (i) and (ii), respectively, we provide quantitative estimates on the fraction of time that the system is near the extinction set, and the probability of asymptotic extinction as a function of the initial state of the system. Furthermore, in the case of persistence, we provide lower bounds for the expected time to escape neighborhoods of the extinction set. To illustrate the applicability of our results, we analyze stochastic models of evolutionary games, Lotka-Volterra dynamics, trait evolution, and spatially structured disease dynamics. Our analysis of these models demonstrates environmental stochasticity facilitates coexistence of strategies in the hawk-dove game, but inhibits coexistence in the rock-paper-scissors game and a Lotka-Volterra predator-prey model. Furthermore, environmental fluctuations with positive auto-correlations can promote persistence of evolving populations and persistence of diseases in patchy landscapes. While our results help close the gap between the persistence theories for deterministic and stochastic systems, we highlight several challenges for future research.

Population projection models for 14 alien plant species in the presence and absence of aboveground competition.

Plant population ecologists strive to understand how environmental drivers influence demographic vital rates and thus population dynamics. Hundreds of studies have collected demographic data and used matrix and/or integral projection models to quantify lifetime fitness and population dynamics of plants. However, most of these studies have focused on native plant species, and there is a need for more studies on alien plants. Further, few studies on alien plants have experimentally manipulated environmental drivers in order to understand the mechanisms that allow alien plant species to have positive population growth. A synthetic understanding of the population dynamics of alien plant species will only be achieved if ecologists collect demographic data on many plant species and environments and provide the demographic data and model structure in a data archive for future comparisons and meta-analyses. Invasive alien species are a social, economic, and ecological issue that has become increasingly important in an increasingly globalized world. Researchers continue to forecast impacts and prevent new introductions by seeking a robust understanding of drivers of invasive species success and failure. Researchers have hypothesized that competitive differences may play a key role in determining alien species success in novel environments. Studies that experimentally manipulate competitors while quantifying demography provide mechanistic insight into species' responses to competition. To date, nearly all field manipulations of competition that measure plant demography and population dynamics have focused on native plant species. The data we provide here aim to address this gap in our knowledge for alien plant species. We present raw data and population-projection models for 14 alien plant species in eastern Missouri, USA. We sampled under ambient conditions and with all individuals of nonfocal species removed from the community, allowing us to project population dynamics in the presence and absence of competition. We have also included the data quantifying how much biomass we removed at the plot level during each removal procedure and data from our germination experiment. No copyright or proprietary restrictions are associated with the use of this data set other than citation of this Data Paper.

Predicting Optimal Sites for Ecosystem Restoration Using Stacked-Species Distribution Modeling

Habitat restoration is an important tool for managing degraded ecosystems, yet the success of restoration projects depends in part on adequately identifying preferred sites for restoration. Species distribution modeling using a machine learning approach provides novel tools for mapping areas of interest for restoration projects. Here we use stacked-species distribution models (s-SDMs) to identify candidate locations for installment of manmade reefs, a useful management tool for restoring structural habitat complexity and the associated biota in marine ecosystems. We created species distribution models for 21 species of commercial, recreational, ecological, or conservation importance within the Southern California Bight based on observations from long-term reef surveys combined with high resolution (200 x 200m) geospatial environmental data layers. We then combined the individual species models to create a stacked-species habitat suitability map, identifying over 800 km2 of potential area for reef restoration within the Bight. When considering only the 21 focal species, s-SDM scores were positively associated with observed bootstrap species richness not only on natural reefs (linear model: slope = 0.27, 95% CI = 0.17 - 0.36, w = 1), but also this result was supported by two independent test datasets. The predicted richness from this linear model was associated with observed species richness when considering only the focal species on manmade reefs (linear model: slope = 0.52, 95% CI = 0.13 - 0.92, w = 1) and also when considering 204 other non-focal species on both natural and manmade reefs in southern California (slope = 3.65, 95% CI = 2.93 - 4.37, w = 1). Finally, our results demonstrate that the existing manmade reefs included in our study on average are located in regions with habitat suitability that is not only less suitable than natural reefs (t-value = -5.4; p < 0.05) only, but also only slightly significantly better than random (p < 0.05), demonstrating a need for more biologically informed placement of manmade reefs. The stacked-species distribution model provides insight for marine restoration projects in southern California specifically, but more generally this method can also be widely applied to other types of habitat restoration including both marine and terrestrial.

Observations of marine wildlife tourism effects on a non‐focal species

A radio-acoustic positioning system was used to assess the effects of shark cage-diving operators (SCDO) on the fine-scale movements of a non-focal species, the smooth stingray Bathytoshia brevicaudata. The results revealed that the time spent in the array was individually variable, but generally increased when SCDO were present and that the presence of SCDO may have the capacity to elicit changes in the space use of B. brevicaudata. These results indicate that the effects of marine wildlife tourism may extend beyond the focal species of interest.

Volunteer survey effort for high-profile species can benefit conservation of non-focal species

SummaryThe last irrefutable record of the Critically Endangered Slender-billed CurlewNumenius tenuirostriscame from 1995. The range of the species is poorly known, but between 2009 and 2011, volunteer observers surveyed more than 680 sites in 19 countries, with additional search effort in a further 12 countries. Although there were no definite sightings (two birds that might have been Slender-billed Curlew were reported), there were other benefits. These included increased knowledge of species distributions and populations in seldom visited areas (over 500,000 birds of over 400 species were observed), the identification of threats to at least 10 Important Bird and Biodiversity Areas, the identification of sites that could qualify as Important Bird and Biodiversity Areas, and capacity building and education through involvement with local survey teams and observers and finally recommendations for future surveys. Thus, these surveys demonstrate the potential benefits of volunteer field surveys for non-focal species.

Courtship Songs of Green Lacewings Filmed in Slow Motion: How a Simple Vibrating Structure can Generate Complex Signals (Neuroptera: Chrysopidae: Chrysoperla)

All of the cryptic species in the Chrysoperla carnea-group of green lacewings produce substrate-borne duetting songs by vibrating the abdomen up and down. Here, we examine the motion of the abdomen during song production using a high-speed video camera. Through temporal (oscillogram) and frequency (sonogram) analysis, these motions are compared to the vibrational signals recorded from the substrate. In tests of three focal and seven non-focal species, we find that the movement of the abdomen follows a path that induces complex oscillations in lightweight substrates. Although the waveform of the signal in the substrate does not exactly mirror the waveform of abdominal motion, the frequencies of the two waveforms are nevertheless identical. In all species, the abdomen is driven by neuromuscular elements that simultaneously generate two or more signals (tones) of different frequency within the abdomen. Comparison in different species of how the abdomen moves when producing these distinct tones potentially allows us to detect homologous song elements across the carnea-group, thus clarifying some patterns of song evolution in this rapidly evolving clade.

Attracting songbirds with conspecific playback: a community approach

The presence of conspecifics is an indicator of good habitat for a number of songbird species; a cue positively associated with territory selection. Thus, conspecific playback may be a cost-effective tool for attracting songbirds to particular, preselected sites of high-quality habitat. Previous studies have used conspecific playback to encourage the establishment of a single species; however, few have researched the potential for the simultaneous attraction of multiple species. Furthermore, empirical studies on the effect of song playback for nonfocal species are sparse. We investigated whether 6 migratory songbird species are more likely to establish nesting territories in response to multispecies playback. To evaluate the effect on the greater songbird community, we assessed the responses of 22 nonfocal species. Three of 6 focal species increased their use of areas near playback speakers, and none became less common. However, several nonfocal species were less likely to use playback sites. Phylogenetic comparison revealed that species closely related to playback species were those most likely to be affected. Our results suggest that conspecific attraction can be used to attract multiple songbird species simultaneously, but that its impact on nonfocal species should be considered before implementation.

Design and Implementation of Degenerate Microsatellite Primers for the Mammalian Clade

Microsatellites are popular genetic markers in molecular ecology, genetic mapping and forensics. Unfortunately, despite recent advances, the isolation of de novo polymorphic microsatellite loci often requires expensive and intensive groundwork. Primers developed for a focal species are commonly tested in a related, non-focal species of interest for the amplification of orthologous polymorphic loci; when successful, this approach significantly reduces cost and time of microsatellite development. However, transferability of polymorphic microsatellite loci decreases rapidly with increasing evolutionary distance, and this approach has shown its limits. Whole genome sequences represent an under-exploited resource to develop cross-species primers for microsatellites. Here we describe a three-step method that combines a novel in silico pipeline that we use to (1) identify conserved microsatellite loci from a multiple genome alignments, (2) design degenerate primer pairs, with (3) a simple PCR protocol used to implement these primers across species. Using this approach we developed a set of primers for the mammalian clade. We found 126,306 human microsatellites conserved in mammalian aligned sequences, and isolated 5,596 loci using criteria based on wide conservation. From a random subset of ∼1000 dinucleotide repeats, we designed degenerate primer pairs for 19 loci, of which five produced polymorphic fragments in up to 18 mammalian species, including the distinctly related marsupials and monotremes, groups that diverged from other mammals 120–160 million years ago. Using our method, many more cross-clade microsatellite loci can be harvested from the currently available genomic data, and this ability is set to improve exponentially as further genomes are sequenced.

Cross-species Transferability of Rice Microsatellites in its Wild Relatives and the Potential for Conservation Genetic Studies

Here, we investigated the transferability of 60 microsatellite markers characterized for cultivated rice Oryza sativa L. in three wild Oryza species representing different genome types: O. rufipogon Griff. (AA), O. officinalis Wall. et Watt. (CC), and O. granulate Nees et Arn. ex Watt. (G). The results indicate the 60 rice SSR loci tested produced homologous amplification products to different extents in O. rufipogon (100%), O. officinalis (90%) and O. granulata (73.3%). Proportions of polymorphism for successfully amplified loci ranged from 0.983 via 0.667 to 0.364 in O. rufipogon, O. officinalis and O. granulata, respectively. The utility of these microsatellite markers was tested for the characterization of genetic diversity in 117 genotypes of these four Oryza species. The values of genetic diversity in cultivated rice are higher than the other two wild species O. officinalis and O. granulata, suggesting microsatellites tend to have more variability in the focal species than in non-focal species to which they are applied. However, much lower levels of genetic variation were observed in rice than in its wild progenitor O. rufipogon, which indicates severe loss of genetic variation may reflect the ‘domestication bottleneck’ through which rice passed. The observation that most of the rice microsatellites are able to detect allelic polymorphisms at different extent in Oryza species suggest that rice microsatellite loci should be useful for the analysis of genetic diversity and inter- and intra-specific relationships in the genus. Therefore, high rates of successful cross-amplification of rice microsatellites among Oryza species with different genome types will offer excellent opportunities to investigate the population genetic structure of wild rice species and explore their conservation genetics.

Phylogenetic species delimitation of the earthworms Eisenia fetida (Savigny, 1826) and Eisenia andrei Bouché, 1972 (Oligochaeta, Lumbricidae) based on mitochondrial and nuclear DNA sequences

Three samples (11 individuals) of Eisenia fetida (Savigny, 1826) and four samples (20 individuals) of Eisenia andrei Bouché, 1972 (focal species), and two samples (six individuals) of Eisenia eiseni (Levinsen, 1884) (nonfocal species; outgroup) were tested for species delimitation using the phylogeny-based method of Wiens and Penkrot (2002). Thirty-seven and 17 DNA sequences of the nuclear 28S (2031 bp) and mitochondrial COI (658 bp) genes, respectively, were generated. Phylogenetic hypotheses for each gene and both combined were built using maximum parsimony, maximum likelihood, and Bayesian approaches. Fully resolved and well-supported trees (>90% bootstrap proportions and 1.0 posterior probabilities) showed both E. fetida and E. andrei samples as monophyletic. Application of Wiens and Penkrot's protocol to those trees resulted in the recognition of these two taxa as different phylogenetic species. This result complements previous studies of crossability and allozyme genetics addressing their different biological status (biological species concept). Finally, our analyses also show that E. fetida is composed of reproductively isolated populations and suggest the presence of a hitherto unrecognized species or subspecies within this taxon.

Microsatellite variation in Drosophila melanogaster and Drosophila simulans: a reciprocal test of the ascertainment bias hypothesis.

Interspecific comparisons of microsatellite loci have repeatedly shown that the loci are longer and more variable in the species from which they are derived (the focal species) than are homologous loci in other (nonfocal) species. There is debate as to whether this is due to directional evolution or to an ascertainment bias during the cloning and locus selection processes. This study tests these hypotheses by performing a reciprocal study. Eighteen perfect dinucleotide microsatellite loci identified from a Drosophila simulans library screen and 18 previously identified in an identical Drosophila melanogaster library screen were used to survey natural populations of each species. No difference between focal and nonfocal species was observed for mean PCR fragment length. However, heterozygosity and number of alleles were significantly higher in the focal species than in the nonfocal species. The most common allele in the Zimbabwe population of both species was sequenced for 31 of the 36 loci. The length of the longest stretch of perfect repeat units is, on average, longer in the focal species than in the non-focal species. There is a positive correlation between the length of the longest stretch of perfect repeats and heterozygosity. The difference in heterozygosity can thus be explained by a reduction in the length of the longest stretch of perfect repeats in the nonfocal species. Furthermore, flanking-sequence length difference was noted between the two species at 58% of the loci sequenced. These data do not support the predictions of the directional-evolution hypothesis; however, consistent with the ascertainment bias hypothesis, the lower variability in nonfocal species is an artifact of the microsatellite cloning and isolation process. Our results also suggest that the magnitude of ascertainment bias for repeat unit length is a function of the microsatellite size distribution in the genomes of different species.