Dissecting the null model for biological invasions: A meta-analysis of the propagule pressure effect.

A consistent determinant of the establishment success of alien species appears to be the number of individuals that are introduced to found a population (propagule pressure), yet variation in the form of this relationship has been largely unexplored. Here, we present the first quantitative systematic review of this form, using Bayesian meta-analytical methods. The relationship between propagule pressure and establishment success has been evaluated for a broad range of taxa and life histories, including invertebrates, herbaceous plants and long-lived trees, and terrestrial and aquatic vertebrates. We found a positive mean effect of propagule pressure on establishment success to be a feature of every hypothesis we tested. However, establishment success most critically depended on propagule pressures in the range of 10-100 individuals. Heterogeneity in effect size was associated primarily with different analytical approaches, with some evidence of larger effect sizes in animal rather than plant introductions. Conversely, no variation was accounted for in any analysis by the scale of study (field to global) or methodology (observational, experimental, or proxy) used. Our analyses reveal remarkable consistency in the form of the relationship between propagule pressure and alien population establishment success.

Does phosphorus influence performance of a native hemiparasite and its impact on a native legume?

Phosphorus (P) is an essential plant nutrient and can become limiting in terrestrial ecosystems where parasitic plant:host associations occur. Yet little is known on how P availability influences parasite performance and its impact on hosts. We investigated the performance of the Australian native stem hemiparasite Cassytha pubescens and its impact on the native leguminous shrub Acacia paradoxa in high or low P conditions in a glasshouse experiment. Infected plants had significantly lower total, shoot, root and nodule biomass and shoot:root ratio than uninfected plants, regardless of P supply. The significant negative effect of infection on arbuscular mycorrhizal colonisation of host roots was more severe in the high P treatment. Infection significantly decreased predawn quantum yield of A. paradoxa in low P but not high P conditions. This finding may be due to the parasite-induced significant enrichment of aluminium in host foliage in low P but not high P treatments. A. paradoxa had significantly lower foliar phosphorus concentration [P] and nitrogen concentration in low P than high P conditions. Parasite biomass and photosynthetic performance were unaffected by P, whereas C. pubescens had significantly lower stem [P] in the low P than high P treatment. Parasite carbon isotope composition was significantly higher than that of the host, especially in low P conditions. Our results show that: (a) native parasite growth and its negative impact on growth of this native shrub was unaffected by P supply and (b) soil P conditions may have no influence on stem hemiparasite:host associations in nature.

Phototactic tails: Evolution and molecular basis of a novel sensory trait in sea snakes.

Dermal phototaxis has been reported in a few aquatic vertebrate lineages spanning fish, amphibians and reptiles. These taxa respond to light on the skin of their elongate hind-bodies and tails by withdrawing under cover to avoid detection by predators. Here, we investigated tail phototaxis in sea snakes (Hydrophiinae), the only reptiles reported to exhibit this sensory behaviour. We conducted behavioural tests in 17 wild-caught sea snakes of eight species by illuminating the dorsal surface of the tail and midbody skin using cold white, violet, blue, green and red light. Our results confirmed phototactic tail withdrawal in the previously studied Aipysurus laevis, revealed this trait for the first time in A. duboisii and A. tenuis, and suggested that tail photoreceptors have peak spectral sensitivities between blue and green light (457-514 nm). Based on these results, and an absence of photoresponses in five Aipysurus and Hydrophis species, we tentatively infer that tail phototaxis evolved in the ancestor of a clade of six Aipysurus species (comprising 10% of all sea snakes). Quantifying tail damage, we found that the probability of sustaining tail injuries was not influenced by tail phototactic ability in snakes. Gene profiling showed that transcriptomes of both tail skin and body skin lacked visual opsins but contained melanopsin (opn4x) in addition to key genes of the retinal regeneration and phototransduction cascades. This work suggests that a nonvisual photoreceptor (e.g., Gq rhabdomeric) signalling pathway underlies tail phototaxis, and provides candidate gene targets for future studies of this unusual sensory innovation in reptiles.

Predictors of contraction and expansion of area of occupancy for British birds.

Geographical range dynamics are driven by the joint effects of abiotic factors, human ecosystem modifications, biotic interactions and the intrinsic organismal responses to these. However, the relative contribution of each component remains largely unknown. Here, we compare the contribution of life-history attributes, broad-scale gradients in climate and geographical context of species' historical ranges, as predictors of recent changes in area of occupancy for 116 terrestrial British breeding birds (74 contractors, 42 expanders) between the early 1970s and late 1990 s. Regional threat classifications demonstrated that the species of highest conservation concern showed both the largest contractions and the smallest expansions. Species responded differently to climate depending on geographical distribution-northern species changed their area of occupancy (expansion or contraction) more in warmer and drier regions, whereas southern species changed more in colder and wetter environments. Species with slow life history (larger body size) tended to have a lower probability of changing their area of occupancy than species with faster life history, whereas species with greater natal dispersal capacity resisted contraction and, counterintuitively, expansion. Higher geographical fragmentation of species' range also increased expansion probability, possibly indicating a release from a previously limiting condition, for example through agricultural abandonment since the 1970s. After accounting statistically for the complexity and nonlinearity of the data, our results demonstrate two key aspects of changing area of occupancy for British birds: (i) climate is the dominant driver of change, but direction of effect depends on geographical context, and (ii) all of our predictors generally had a similar effect regardless of the direction of the change (contraction versus expansion). Although we caution applying results from Britain's highly modified and well-studied bird community to other biogeographic regions, our results do indicate that a species' propensity to change area of occupancy over decadal scales can be explained partially by a combination of simple allometric predictors of life-history pace, average climate conditions and geographical context.

Decoupling of component and ensemble density feedbacks in birds and mammals.

A component density feedback represents the effect of change in population size on single demographic rates, whereas an ensemble density feedback captures that effect on the overall growth rate of a population. Given that a population's growth rate is a synthesis of the interplay of all demographic rates operating in a population, we test the hypothesis that the strength of ensemble density feedback must augment with increasing strength of component density feedback, using long-term censuses of population size, fertility, and survival rates of 109 bird and mammal populations (97 species). We found that compensatory and depensatory component feedbacks were common (each detected in approximately 50% of the demographic rates). However, component feedback strength only explained <10% of the variation in ensemble feedback strength. To explain why, we illustrate the different sources of decoupling between component and ensemble feedbacks. We argue that the management of anthropogenic impacts on populations using component feedbacks alone is ill-advised, just as managing on the basis of ensemble feedbacks without a mechanistic understanding of the contributions made by its components and environmental variability can lead to suboptimal decisions.

Managed relocation as an adaptation strategy for mitigating climate change threats to the persistence of an endangered lizard.

The distributional ranges of many species are contracting with habitat conversion and climate change. For vertebrates, informed strategies for translocations are an essential option for decisions about their conservation management. The pygmy bluetongue lizard, Tiliqua adelaidensis, is an endangered reptile with a highly restricted distribution, known from only a small number of natural grassland fragments in South Australia. Land-use changes over the last century have converted perennial native grasslands into croplands, pastures and urban areas, causing substantial contraction of the species' range due to loss of essential habitat. Indeed, the species was thought to be extinct until its rediscovery in 1992. We develop coupled-models that link habitat suitability with stochastic demographic processes to estimate extinction risk and to explore the efficacy of potential climate adaptation options. These coupled-models offer improvements over simple bioclimatic envelope models for estimating the impacts of climate change on persistence probability. Applying this coupled-model approach to T. adelaidensis, we show that: (i) climate-driven changes will adversely impact the expected minimum abundance of populations and could cause extinction without management intervention, (ii) adding artificial burrows might enhance local population density, however, without targeted translocations this measure has a limited effect on extinction risk, (iii) managed relocations are critical for safeguarding lizard population persistence, as a sole or joint action and (iv) where to source and where to relocate animals in a program of translocations depends on the velocity, extent and nonlinearities in rates of climate-induced habitat change. These results underscore the need to consider managed relocations as part of any multifaceted plan to compensate the effects of habitat loss or shifting environmental conditions on species with low dispersal capacity. More broadly, we provide the first step towards a more comprehensive framework for integrating extinction risk, managed relocations and climate change information into range-wide conservation management.

Density dependence: an ecological Tower of Babel.

The concept of density dependence represents the effect of changing population size on demographic rates and captures the demographic role of social and trophic mechanisms (e.g. competition, cooperation, parasitism or predation). Ecologists have coined more than 60 terms to denote different statistical and semantic properties of this concept, resulting in a formidable lexicon of synonymies and polysemies. We have examined the vocabulary of density dependence used in the modern ecological literature from the foundational lexicon developed by Smith, Allee, Haldane, Neave and Varley. A few simple rules suffice to abate terminological inconsistency and to enhance the biological meaning of this important concept. Correct citation of original references by ecologists and research journals could ameliorate terminological standards in our discipline and avoid linguistic confusion of mathematically and theoretically complex patterns.

Confronting spatial capture-recapture models with realistic animal movement simulations.

Spatial capture-recapture (SCR) models have emerged as a robust method to estimate the population density of mobile animals. However, model evaluation has generally been based on data simulated from simplified representations of animal space use. Here, we generated data from animal movement simulated from a mechanistic individual-based model, in which movement emerges from the individual's response to a changing environment (i.e., from the bottom-up), driven by key ecological processes (e.g., resource memory and territoriality). We drew individual detection data from simulated movement trajectories and fitted detection data sets to a basic, resource selection and transience SCR model, as well as their variants accounting for resource-driven heterogeneity in density and detectability. Across all SCR models, abundance estimates were robust to multiple, but low-degree violations of the specified movement processes (e.g., resource selection). SCR models also successfully captured the positive effect of resource quality on density. However, covariate models failed to capture the finer scale effect of resource quality on detectability and space use, which may be a consequence of the low temporal resolution of SCR data sets and/or model misspecification. We show that home-range size is challenging to infer from the scale parameter alone, compounded by reliance on conventional measures of "true" home-range size that are highly sensitive to sampling regime. Additionally, we found the transience model challenging to fit, probably due to data sparsity and violation of the assumption of normally distributed inter-occasion movement of activity centers, suggesting that further development of the model is required for general applicability. Our results showed that further integration of complex movement into SCR models may not be necessary for population estimates of abundance when the level of individual heterogeneity induced by the underlying movement process is low, but appears warranted in terms of accurately revealing finer scale patterns of ecological and movement processes. Further investigation into whether this holds true in populations with other types of realistic movement characteristics is merited. Our study provides a framework to generate realistic SCR data sets to develop and evaluate more complex movement processes in SCR models.

Meta-analysis reveals that resting metabolic rate is not consistently related to fitness and performance in animals.

Explaining variation in the fitness of organisms is a fundamental goal in evolutionary ecology. Maintenance energy metabolism is the minimum energy required to sustain biological processes at rest (resting metabolic rate: RMR) and is proposed to drive or constrain fitness of animals; however, this remains debated. Hypotheses have been proposed as to why fitness might increase with RMR (the 'increased intake' or 'performance' hypothesis), decrease with RMR (the 'compensation' or 'allocation' hypothesis), or vary among species and environmental contexts (the 'context dependent' hypothesis). Here, we conduct a systematic review and meta-analysis of the literature, finding 114 studies with 355 relationships between RMR and traits that may be related to fitness. We show that individuals with relatively high RMR generally have high fitness overall, which might be supported by an increased energy intake. However, fitness proxies are not interchangeable: the nature of the RMR-fitness relationship varied substantially depending on the specific trait in question, and we found no consistent relationship between RMR and those traits most closely linked with actual fitness (i.e., lifetime reproductive success). We hypothesise that maintaining high RMR is not costly when resources are unlimited, and we propose ideas for future studies to identify mechanisms underlying RMR-fitness relationships.

Development and evaluation of a custom bait design based on 469 single-copy protein-coding genes for exon capture of isopods (Philosciidae: Haloniscus).

Transcriptome-based exon capture approaches, along with next-generation sequencing, are allowing for the rapid and cost-effective production of extensive and informative phylogenomic datasets from non-model organisms for phylogenetics and population genetics research. These approaches generally employ a reference genome to infer the intron-exon structure of targeted loci and preferentially select longer exons. However, in the absence of an existing and well-annotated genome, we applied this exon capture method directly, without initially identifying intron-exon boundaries for bait design, to a group of highly diverse Haloniscus (Philosciidae), paraplatyarthrid and armadillid isopods, and examined the performance of our methods and bait design for phylogenetic inference. Here, we identified an isopod-specific set of single-copy protein-coding loci, and a custom bait design to capture targeted regions from 469 genes, and analysed the resulting sequence data with a mapping approach and newly-created post-processing scripts. We effectively recovered a large and informative dataset comprising both short (<100 bp) and longer (>300 bp) exons, with high uniformity in sequencing depth. We were also able to successfully capture exon data from up to 16-year-old museum specimens along with more distantly related outgroup taxa, and efficiently pool multiple samples prior to capture. Our well-resolved phylogenies highlight the overall utility of this methodological approach and custom bait design, which offer enormous potential for application to future isopod, as well as broader crustacean, molecular studies.

Lasting the distance: The survival of alien birds shipped to New Zealand in the 19th century.

Invasive alien species are a major threat to biodiversity and human activities, providing a strong incentive to understand the processes by which alien invasion occurs. While it is important to understand the determinants of success at each of several invasion stages-transport, introduction, establishment, and spread-few studies have explored the first of these stages. Here, we quantify and analyze variation in the success of individual animals in surviving the transport stage, based on shipping records of European passerines destined for New Zealand. We mined the original documents of Acclimatisation Societies, established in New Zealand for the purpose of introducing supposedly beneficial alien species, in combination with recently digitized newspaper archives, to produce a unique dataset of 122 ships that carried passerines from Europe to New Zealand between 1850 and 1885. For 37 of these shipments, data on the survival of individual species were available. Using generalized linear mixed models, we explored how survival was related to characteristics of the shipments and the species. We show that species differed greatly in their survival, but none of the tested traits accounted for these differences. Yet, survival increased over time, which mirrors the switch from early haphazard shipments to larger organized shipments. Our results imply that it was the quality of care received by the birds that most affected success at this stage of the invasion process.

Persistence of Low Pathogenic Influenza A Virus in Water: A Systematic Review and Quantitative Meta-Analysis.

Avian influenza viruses are able to persist in the environment, in-between the transmission of the virus among its natural hosts. Quantifying the environmental factors that affect the persistence of avian influenza virus is important for influencing our ability to predict future outbreaks and target surveillance and control methods. We conducted a systematic review and quantitative meta-analysis of the environmental factors that affect the decay of low pathogenic avian influenza virus (LPAIV) in water. Abiotic factors affecting the persistence of LPAIV have been investigated for nearly 40 years, yet published data was produced by only 26 quantitative studies. These studies have been conducted by a small number of principal authors (n = 17) and have investigated a narrow range of environmental conditions, all of which were based in laboratories with limited reflection of natural conditions. The use of quantitative meta-analytic techniques provided the opportunity to assess persistence across a greater range of conditions than each individual study can achieve, through the estimation of mean effect-sizes and relationships among multiple variables. Temperature was the most influential variable, for both the strength and magnitude of the effect-size. Moderator variables explained a large proportion of the heterogeneity among effect-sizes. Salinity and pH were important factors, although future work is required to broaden the range of abiotic factors examined, as well as including further diurnal variation and greater environmental realism generally. We were unable to extract a quantitative effect-size estimate for approximately half (50.4%) of the reported experimental outcomes and we strongly recommend a minimum set of quantitative reporting to be included in all studies, which will allow robust assimilation and analysis of future findings. In addition we suggest possible means of increasing the applicability of future studies to the natural environment, and evaluating the biological content of natural waterbodies.

Bioluminescence in the ghost fungus Omphalotus nidiformis does not attract potential spore dispersing insects.

Bioluminescence has been known from fungi since ancient times, but little work has been done to establish its potential role. There is evidence that some bioluminescent fungi differentially attract potential spore-dispersing insects, and we aimed to establish if this was the case for the ghost fungus, Omphalotus nidiformis (Agaricales,Marasmiaceae), a widespread Australian temperate zone species. We examined three corroborative lines of evidence: circadian rhythmicity of bioluminescence; field-recorded insect abundance at the time of basidiome production; and attractiveness of glowing fungi to flying insects. Basidiomes glowed continuously day and night, and were present in winter (June-July) when insect abundance was low. To assess attractiveness, we deployed sticky-traps in open woodland in the absence of light pollution, in Treatment (baited with fresh bioluminescent O. nidiformis) and Control pairs, for 480 trap-hours on moonless nights. There was no statistical difference in mean insect abundance between Treatment and Control traps (mean 0.33 and 0.54 individuals per trap night, respectively). To interpret these results, we provide a brief review of competing hypotheses for fungal bioluminescence, and conclude that for some fungi, bioluminescence may be an incidental by-product of metabolism rather than conferring any selective advantage. It is possible that the role of bioluminescence differs among evolutionary lineages of fungi and/or with attributes of their growth environments that could affect spore dispersal, such as wind and insect abundance.

Correction: Persistence of Low Pathogenic Influenza A Virus in Water: A Systematic Review and Quantitative Meta-Analysis.

[This corrects the article DOI: 10.1371/journal.pone.0161929.].

Spatial and Temporal Variation in the Effects of Climatic Variables on Dugong Calf Production.

Knowledge of the relationships between environmental forcing and demographic parameters is important for predicting responses from climatic changes and to manage populations effectively. We explore the relationships between the proportion of sea cows (Dugong dugon) classified as calves and four climatic drivers (rainfall anomaly, Southern Oscillation El Niño Index [SOI], NINO 3.4 sea surface temperature index, and number of tropical cyclones) at a range of spatially distinct locations in Queensland, Australia, a region with relatively high dugong density. Dugong and calf data were obtained from standardized aerial surveys conducted along the study region. A range of lagged versions of each of the focal climatic drivers (1 to 4 years) were included in a global model containing the proportion of calves in each population crossed with each of the lagged versions of the climatic drivers to explore relationships. The relative influence of each predictor was estimated via Gibbs variable selection. The relationships between the proportion of dependent calves and the climatic drivers varied spatially and temporally, with climatic drivers influencing calf counts at sub-regional scales. Thus we recommend that the assessment of and management response to indirect climatic threats on dugongs should also occur at sub-regional scales.

Barramundi as an indicator species for environmental monitoring in North Queensland, Australia: laboratory versus field studies.

The dose-response relationship for hepatic 7-ethoxyresorufin-O-deethylase (EROD) induction in barramundi (Lates calcarifer) was examined under controlled laboratory conditions for 15 d using farm-reared barramundi. These results were compared with EROD activity measured in barramundi collected from two rivers catchments (impacted and nonimpacted) in northern Queensland, Australia. Barramundi were dosed by intraperitoneal injection with a known cytochrome P4501A (CYP1A) inducer, beta-naphthoflavone (beta-NF), at 5, 10, and 50 mg kg(-1) using two controls: A vehicle control (corn-oil injected) and an experimental control (no injection). The EROD induction occurred within 4 h in the 5, 10, and 50 mg beta-NF kg(-1) exposures, reaching mean maximum activities of 88.6 (+/-51.9), 85.5 (+/-91.7), and 149.1 (+/-106.4) pmol min(-1) mg protein(-1), respectively. Mean EROD activities remained low in the corn-oil controls (2.1+/-1.8 pmol min(-1) mg protein(-1)) and experimental controls (5.3+/-4.4 pmol min(-1) mg protein(-1)) throughout the study. Barramundi demonstrated a rapid response curve, which was dose dependent (50 > 10 > 5 mg beta-NF kg(-1)) and decreased progressively over time from induction. Measurement of total cytochrome P450 content (nmol mg protein(-1)) was not dose dependent. The EROD activities from field-collected barramundi from the Johnstone River (impacted) and Olive River (nonimpacted) suggest exposure to low-level contaminants in the Johnstone River fish only. With more controlled laboratory and field studies, barramundi have the potential to become a major indicator species in assessing exposure to environmental contaminants in coastal areas throughout northern Queensland, Australia.

Spatial climate patterns explain negligible variation in strength of compensatory density feedbacks in birds and mammals.

The use of long-term population data to separate the demographic role of climate from density-modified demographic processes has become a major topic of ecological investigation over the last two decades. Although the ecological and evolutionary mechanisms that determine the strength of density feedbacks are now well understood, the degree to which climate gradients shape those processes across taxa and broad spatial scales remains unclear. Intuitively, harsh or highly variable environmental conditions should weaken compensatory density feedbacks because populations are hypothetically unable to achieve or maintain densities at which social and trophic interactions (e.g., competition, parasitism, predation, disease) might systematically reduce population growth. Here we investigate variation in the strength of compensatory density feedback, from long-term time series of abundance over 146 species of birds and mammals, in response to spatial gradients of broad-scale temperature precipitation variables covering 97 localities in 28 countries. We use information-theoretic metrics to rank phylogenetic generalized least-squares regression models that control for sample size (time-series length) and phylogenetic non-independence. Climatic factors explained < 1% of the remaining variation in density-feedback strength across species, with the highest non-control, model-averaged effect sizes related to extreme precipitation variables. We could not link our results directly to other published studies, because ecologists use contrasting responses, predictors and statistical approaches to correlate density feedback and climate--at the expense of comparability in a macroecological context. Censuses of multiple populations within a given species, and a priori knowledge of the spatial scales at which density feedbacks interact with climate, seem to be necessary to determine cross-taxa variation in this phenomenon. Despite the availability of robust modelling tools, the appropriate data have not yet been gathered for most species, meaning that we cannot yet make any robust generalisations about how demographic feedbacks interact with climate.

Strength of density feedback in census data increases from slow to fast life histories.

Life-history theory predicts an increasing rate of population growth among species arranged along a continuum from slow to fast life histories. We examine the effects of this continuum on density-feedback strength estimated using long-term census data from >700 vertebrates, invertebrates, and plants. Four life-history traits (Age at first reproduction, Body size, Fertility, Longevity) were related statistically to Gompertz strength of density feedback using generalized linear mixed-effects models and multi-model inference. Life-history traits alone explained 10 to 30% of the variation in strength across species (after controlling for time-series length and phylogenetic nonindependence). Effect sizes were largest for body size in mammals and longevity in birds, and density feedback was consistently stronger for smaller-bodied and shorter-lived species. Overcompensatory density feedback (strength <-1) occurred in 20% of species, predominantly at the fast end of the life-history continuum, implying relatively high population variability. These results support the idea that life history leaves an evolutionary signal in long-term population trends as inferred from census data. Where there is a lack of detailed demographic data, broad life-history information can inform management and conservation decisions about rebound capacity from low numbers, and propensity to fluctuate, of arrays of species in areas planned for development, harvesting, protection, and population recovery.