A simple approach to optimal control of invasive species

The problem of invasive species and their control is one of the most pressing applied issues in ecology today. We developed simple approaches based on linear programming for determining the optimal removal strategies of different stage or age classes for control of invasive species that are still in a density-independent phase of growth. We illustrate the application of this method to the specific example of invasive Spartina alterniflora in Willapa Bay, WA. For all such systems, linear programming shows in general that the optimal strategy in any time step is to prioritize removal of a single age or stage class. The optimal strategy adjusts which class is the focus of control through time and can be much more cost effective than prioritizing removal of the same stage class each year.     

Large-Scale Removal of Invasive Honeysuckle Decreases Mosquito and Avian Host Abundance

Invasive species rank second only to habitat destruction as a threat to native biodiversity. One consequence of biological invasions is altered risk of exposure to infectious diseases in human and animal populations. The distribution and prevalence of mosquito-borne diseases depend on the complex interactions between the vector, the pathogen, and the human or wildlife reservoir host. These interactions are highly susceptible to disturbance by invasive species, including terrestrial plants. We conducted a 2-year field experiment using a Before–After/Control–Impact design to examine how removal of invasive Amur honeysuckle (Lonicera maackii) in a forest fragment embedded within a residential neighborhood affects the abundance of mosquitoes, including two of the most important vectors of West Nile virus, Culex pipiens and Cx. restuans. We also assessed any potential changes in avian communities and local microclimate associated with Amur honeysuckle removal. We found that (1) removal of Amur honeysuckle reduces the abundance of both vector and non-vector mosquito species that commonly feed on human hosts, (2) the abundance and composition of avian hosts is altered by honeysuckle removal, and (3) areas invaded with honeysuckle support local microclimates that are favorable to mosquito survival. Collectively, our investigations demonstrate the role of a highly invasive understory shrub in determining the abundance and distribution of mosquitoes and suggest potential mechanisms underlying this pattern. Our results also give rise to additional questions regarding the general impact of invasive plants on vector-borne diseases and the spatial scale at which removal of invasive plants may be utilized to effect disease control.     

Plant-disperser mutualisms in a semi-arid habitat invaded by <Emphasis Type="Italic">Lantana camara</Emphasis> L.

Dispersal is an important ecological process that affects plant population structure and community composition. Invasive plants with fleshy fruits rapidly form associations with native and invasive dispersers, and may affect existing native plant-disperser associations. We asked whether frugivore visitation rate and fruit removal was associated with plant characteristics in a community of fleshy-fruited plants and whether an invasive plant receives more visitation and greater fruit removal than native plants in a semi-arid habitat of Andhra Pradesh, India. Tree-watches were undertaken at individuals of nine native and one invasive shrub species to assess the identity, number and fruit removal by avian frugivores. Network analyses and generalised linear mixed-effects models were used to understand species and community-level patterns. All plants received most number of visits from abundant, generalist avian frugivores. Number of frugivore visits and time spent by frugivores at individual plants was positively associated with fruit crop size, while fruit removal was positively associated with number of frugivore visits and their mean foraging time at individual plants. The invasive shrub, Lantana camara L. (Lantana), had lower average frugivore visit rate than the community of fleshy-fruited plants and received similar average frugivore visits but greater average per-hour fruit removal than two other concurrently fruiting native species. Based on the results of our study, we infer that there is little evidence of competition between native plants and Lantana for the dispersal services of native frugivores and that more data are required to assess the nature of these interactions over the long term. We speculate that plant associations with generalist frugivores may increase the functional redundancy of this frugivory network, buffering it against loss of participating species.     

Biodiversity influences invasion success of a facultative epiphytic seaweed in a marine forest

The biotic resistance hypothesis predicts that more diverse communities should have greater resistance to invasions than species-poor communities. However for facultative and obligate epiphytic invaders a high native species richness, abundance and community complexity might provide more resources for the invader to thrive to. We conducted surveys across space and time to test for the influence of native algal species abundance and richness on the abundance of the invasive facultative epiphytic filamentous alga Lophocladia lallemandii in a Mediterranean Cystoseira balearica seaweed forest. By removing different functional groups of algae, we also tested whether these relationships were dependent on the complexity and abundance of the native algal community. When invasion was first detected, Lophocladia abundance was positively related to species richness, but the correlation became negative after two years of invasion. Similarly, a negative relationship was also observed across sites. The removal experiment revealed that more complex native communities were more heavily invaded, where also a positive relationship was found between native algal richness and Lophocladia, independently of the native algal abundance. Our observational and experimental data show that, at early stages of invasion, species-rich seaweed forests are not more resistant to invasion than species-poor communities. Higher richness of native algal species may increase resource availability (i.e. substrate) for invader establishment, thus facilitating invasion. After the initial invasion stage, native species richness decreases with time since invasion, suggesting negative impacts of invasive species on native biodiversity.     

Age-structured non-pharmaceutical interventions for optimal control of COVID-19 epidemic

In an epidemic, individuals can widely differ in the way they spread the infection depending on their age or on the number of days they have been infected for. In the absence of pharmaceutical interventions such as a vaccine or treatment, non-pharmaceutical interventions (e.g. physical or social distancing) are essential to mitigate the pandemic. We develop an original approach to identify the optimal age-stratified control strategy to implement as a function of the time since the onset of the epidemic. This is based on a model with a double continuous structure in terms of host age and time since infection. By applying optimal control theory to this model, we identify a solution that minimizes deaths and costs associated with the implementation of the control strategy itself. We also implement this strategy for three countries with contrasted age distributions (Burkina-Faso, France, and Vietnam). Overall, the optimal strategy varies throughout the epidemic, with a more intense control early on, and depending on host age, with a stronger control for the older population, except in the scenario where the cost associated with the control is low. In the latter scenario, we find strong differences across countries because the control extends to the younger population for France and Vietnam 2 to 3 months after the onset of the epidemic, but not for Burkina Faso. Finally, we show that the optimal control strategy strongly outperforms a constant uniform control exerted over the whole population or over its younger fraction. This improved understanding of the effect of age-based control interventions opens new perspectives for the field, especially for age-based contact tracing.     

Optimal schedule for monitoring a plant incursion when detection and treatment success vary over time

Management of an invasive plant species can be viewed as two separate and successive processes. The first, survey, aims to find infested areas and remove individuals. The second, monitoring, consists of repeated visits to these areas in order to prevent possible re-emergence. As detection probability may vary over time, the timing and number of monitoring visits can dramatically impact monitoring efficacy. We explore the optimal timing and number of monitoring visits, by focusing on one infested site. Our decision-analysis framework defines an optimal monitoring schedule which accounts for a time-dependent probability of detection, based on the presence/absence of a flower. We use this framework to investigate the optimal monitoring schedule for Hieracium aurantiacum, an invasive species in the Australian Alps and many other countries. We also perform a sensitivity analysis to draw more general conclusions. For H. aurantiacum eight monitoring visits (compared to 12 visits in the current program) are sufficient to obtain a 99% monitoring efficacy. When four or fewer visits to a site are allowed, it is optimal to visit during the high season, when the weed is likely to initiate flowering. Any extra visits should be scheduled in the early season, before the plants flower. The sensitivity analysis shows that increasing the detection probability early in the season has a greater impact than increasing it late in the season. An effective treatment method increases the value of site visits late in the season, when the detection probability is higher. Our decision-analysis framework can assist invasive species managers to reduce or reallocate management resources by determining the minimum number of monitoring visits required to satisfy an acceptable risk of re-emergence.     

Minimizing invader impacts: striking the right balance between removal and restoration

Invasive species can cause severe damage in their introduced range; this damage often persists even after removal of the invader. In order to efficiently allocate a limited budget between invader removal and restoration of habitat from which the invader has been removed, it is vital to quantify the impacts of the invasion within an economic context. Here we develop optimal management strategies for biological invasions, which minimize both the direct economic costs of removal and restoration, and the ecological costs of present and future damage caused by the invasion. We demonstrate how this can be formulated as a linear programming problem, enabling the fast and efficient computation of optimal solutions. Using a simple example, we outline some general principles for the optimal control of an invader that damages its environment. Notably, we show that the most effective strategies often switch the priority of removal and restoration over time, and outline the conditions under which restoration is prioritized over removal. The proportion of total funds allocated to restoration will depend on the annual budget, the persistence of damage, and the relative costs of damage, removal and restoration.     

Direct impact of invasive bivalve (<Emphasis Type="Italic">Sinanodonta woodiana</Emphasis>) parasitism on freshwater fish physiology: evidence and implications

Direct and potentially damaging effects of invasive alien species can remain unnoticed or insufficiently quantified, resulting in a lack of stakeholder awareness. We report for the first time that parasitic larvae (glochidia) of the invasive freshwater mussel Sinanodonta (Anodonta) woodiana (Unionidae, Bivalvia) cause an unexpected reduction in the condition factor of parasitized native fish species. The reduction in the body mass and condition factor of experimentally infested European chub (Squalius cephalus) was associated with changes in several physiological parameters measured in host fish plasma. Ion concentrations (potassium, chloride) and enzymes activities (aspartate aminotransferase, alanine aminotransferase, lactate dehydrogenase, alkaline phosphatase) were significantly affected; hence, the results reveal the complex effects of non-native glochidia on the homeostasis of the individually tested fish. Changes in host physiology and condition status were recorded also in environmentally relevant infestation intensities (mean of 3.02 ± 0.51 glochidia g^?1). Despite intensive concern regarding the negative biodiversity and ecosystem impacts of the adult stage of S. woodiana among conservationists and natural resource managers, potential effects of its larval stage have been neglected until now. Because fish hosts are an obligatory part of the reproductive cycle of the mussel and the main vector for spreading, documentation of this direct and easily quantifiable impact on fish has great potential to influence the key community of stakeholders in fisheries and aquaculture sectors and to serve as a strong motivating factor for invasive species control. We argue for more careful consideration of potential multiple life-stage effects of S. woodiana and of other invasive alien species as well, as different life stages can have highly specific impacts and corresponding relevance for key stakeholder groups.     

米槠-木荷林优势种群的年龄结构及其更新策略

通过年轮分析,构建了浙江天童米槠-木荷林优势种木荷、米槠、石栎的年龄结构,分析了高生长和径向生长及萌枝策略随年龄的变化规律,探讨了干扰对群落动态的影响。研究结果表明:(1)3个物种的胸径、高度与年龄的关系均可用logistic曲线和线性模型拟合,但随年龄增加胸径、高度与年龄的关系显著下降。(2)随年龄增加3树种的DBH/H逐渐增加,米槠、石栎幼龄个体(1-20a)的有萌个体率和有萌个体萌枝数逐渐下降;米槠和石栎幼苗的主干较木荷细长、多萌枝,木荷和石栎成树主干较米槠细长;体现了米槠的更新策略具开拓性,木荷的具保守性,石栎在幼龄期具开拓性,成年期转为保守性。(3)米槠和石栎的年龄结构呈逆J型,幼龄个体充足,但中龄段(21-40a)存在更新断层,这与其高消耗的开拓性策略有关;木荷的年龄结构呈间歇型,各龄级均存有个体,这与其保守性策略有关;(4)3物种在大龄级上(52-60a)均存在更新高峰,与该地区的择伐干扰时间一致,高强度的干扰促生了次生演替,形成了以木荷为第一优势种的群落。(5)米槠、木荷、石栎的年龄结构是更新策略和干扰的综合表现,它不仅与径级结构一样可展现种群更新特征、预测种群发展动态,更能精确地反映群落动态事件的发生频次和发生时间。     

Does localized control of invasive eastern gambusia (Poeciliidae: Gambusia holbrooki) increase population growth of generalist wetland fishes?

While invasive fish management is heavily focussed on containment measures when introductions occur, examples from invasive species management in terrestrial systems suggest that there may also be considerable conservation benefits in implementing localized control programmes. We conducted a field‐based experiment to assess the effectiveness of removing a globally significant invasive fish, eastern gambusia Gambusia holbrooki, from natural wetland habitats of south‐eastern Australia. With recent work suggesting the impacts of eastern gambusia may be minimal for species with generalist life‐history strategies, we hypothesized that the removal of eastern gambusia will reduce localized population growth of the invasive species, but will have little influence on the population growth of more generalist sympatric wetland fish species. We used a predictive modelling approach to investigate changes in eastern gambusia populations following removal activities, and how sympatric fish species responded to such changes. Although eastern gambusia rapidly populated habitats, we demonstrated that control actions substantially reduced the rate of population increase over the four‐month study period. This suggests that control may be an effective localized strategy to suppress eastern gambusia densities. There was however, no evidence of any response to the removal actions by any of the three sympatric fish species investigated – carp gudgeon (Hypseleotris spp.), Australian smelt (Retropinna semoni) and the invasive common carp (Cyprinus carpio). These results support previous work which suggests that the flexible life‐history strategies and behavioural traits of all three species allow co‐existence with eastern gambusia. The study highlights the importance of understanding the potential outcomes of control options which is particularly pertinent for established aquatic invasive species where information on control effectiveness, population dynamics and/or ecosystem response is currently lacking.     

Conflicting values: ecosystem services and invasive tree management

Tree species have been planted widely beyond their native ranges to provide or enhance ecosystem services such as timber and fibre production, erosion control, and aesthetic or amenity benefits. At the same time, non-native tree species can have strongly negative impacts on ecosystem services when they naturalize and subsequently become invasive and disrupt or transform communities and ecosystems. The dichotomy between positive and negative effects on ecosystem services has led to significant conflicts over the removal of non-native invasive tree species worldwide. These conflicts are often viewed in only a local context but we suggest that a global synthesis sheds important light on the dimensions of the phenomenon. We collated examples of conflict surrounding the control or management of tree invasions where conflict has caused delay, increased cost, or cessation of projects aimed at invasive tree removal. We found that conflicts span a diverse range of taxa, systems and countries, and that most conflicts emerge around three areas: urban and near-urban trees; trees that provide direct economic benefits; and invasive trees that are used by native species for habitat or food. We suggest that such conflict should be seen as a normal occurrence in invasive tree removal. Assessing both positive and negative effects of invasive species on multiple ecosystem services may provide a useful framework for the resolution of conflicts.     

Phylogenetic conservation prioritization with uncertainty

We consider a set of species S and are interested in the assessment of the subsets of S from a phylogenetic diversity viewpoint. Several measures can be used for this assessment. Here we have retained phylogenetic diversity (PD) in the sense of Faith, a measure widely used to reflect the evolutionary history accumulated by a group of species. The PD of a group of species X included in S is easy to calculate when the phylogenetic tree associated with S is perfectly known but this situation is rarely verified. We are interested here in cases where uncertainty regarding the length of branches and the topology of the tree is reflected in the fact that several phylogenetic trees are considered to be plausible for the set S. We propose several measures of the phylogenetic diversity to take account of the uncertainty arising from this situation. A natural problem in the field of biological conservation is to select the best subset of species to protect from a group of threatened species. Here, the best subset is the one that optimizes the proposed measures. We show how to solve these optimal selection problems by integer linear programming. The approach is illustrated by several examples.     

Comparison of trophic function between the globally invasive crayfishes <Emphasis Type="Italic">Pacifastacus leniusculus</Emphasis> and <Emphasis Type="Italic">Procambarus clarkii</Emphasis>

Impacts of invasive species may manifest most strongly if these organisms are highly distinct functionally from the native species they often replace. Yet, should we expect functional differences between native and invasive species of generalist organisms like freshwater crayfish? Some existing evidence has pointed to native and invasive crayfish species as ecologically equivalent. We contribute to this literature by comparing the trophic niches of the globally invasive crayfishes Pacifastacus leniusculus and Procambarus clarkii, by applying carbon and nitrogen stable isotope analyses to replicated allopatric (alone) and sympatric (together) lake populations in western Washington State, USA, where P. clarkii has been recently introduced and P. leniusculus is presumed native. Our study corrected for potential inherent differences in lake food webs as a consequence of lake abiotic or biotic characteristics using random effects in linear mixed effects models. We found that although overall trophic niche size or area of these species was not significantly different, P. leniusculus was significantly higher in trophic position than P. clarkii when also accounting for the effects of body size, sex, and lakes as random effects. This pattern of increased trophic position of P. leniusculus over P. clarkii was conserved over time in one sympatric lake for which we had data over multiple years. Cumulatively, our findings point to trophic differences between the globally cosmopolitan crayfishes P. leniusculus and P. clarkii, particularly when accounting for the ways that ecosystem context can affect food web structure of communities and the trophic resources available to these consumers.     

Reliance on Exotic Plants by Two Groups of Threatened Samango Monkeys, <Emphasis Type="Italic">Cercopithecus albogularis labiatus</Emphasis>, at Their Southern Range Limit

Understanding how threatened species adapt their behavior to landscapes shaped by humans is increasingly important to ensuring they persist in a changing world. Matrix habitats can be shared spaces where human and nonhuman primates coexist. We set out to determine how an endemic, threatened forest specialist, the frugivorous, arboreal samango monkey (Cercopithecus albogularis labiatus), has responded to a matrix habitat made up of residential gardens and commercial plantations in Eastern Cape province, South Africa. We followed two groups from dawn to dusk for a mean of 3 days/mo for 12 mo (February 1, 2011 to January 31, 2012) using scan sampling to collect data on their diet, activity, and ranging patterns. We used resource abundance transects to describe the groups’ home ranges and monitored tree phenology to calculate fruit and seed availability indices. Monkeys from both groups consumed large quantities of exotic plant species, accounting for >50% of their overall annual diet, with seeds of the invasive black wattle (Acacia mearnsii) the most commonly consumed exotic species followed by acorns of two oak species (Quercus robur and Q. palustris.). However, monkeys responded to the availability of indigenous rather than exotic fruits and seeds and increased their consumption of exotics when indigenous fruits were less available. Although monkeys spent less time moving when feeding on exotic species compared to indigenous species, eating exotics did not free up monkeys’ time to rest or socialize, as additional time was required to process exotic foods. To offset the possible negative consequences of the monkeys’ reliance on exotic seeds, including escalating conflict between monkeys and people in gardens, we suggest gradual removal of exotic plant species in the habitat and replacement with indigenous species as one mitigation strategy.     

Throwing the baby out with the bathwater: does laurel forest restoration remove a critical winter food supply for the critically endangered Azores bullfinch?

The invasive Clethra arborea has a dual-role in the diet of the Azores bullfinch, a critically endangered bird species endemic to the island of São Miguel (Azores, Portugal). This is a crucial winter food resource but it lowers the availability of native laurel forest species that compose most of the bird’s diet throughout the year. The removal of this and other invasive alien species is part of current laurel forest habitat restoration programmes, disregarding the impact on the Azores bullfinch population. In order to evaluate the first responses of the Azores bullfinch to habitat restoration, we studied bird diet, foraging behaviour, food availability and habitat occupancy in managed (without C. arborea) and control areas. Significant increases in the availability of native food resources in managed areas were noticeable in the diet, particularly the intake of Ilex perado ssp. azorica and Prunus lusitanica ssp. azorica flower buds. In most of the studied months birds heavily used and foraged in managed over control areas. The one exception was in December, when a resource-gap occurred in managed areas, which may be overcome in the short-term due to re-establishment of native plants following removal of invasive aliens.     

Booms,busts and population collapses in invasive ants

The abundance of many invasive species can vary substantially over time, with dramatic population declines and local extinctions frequently observed in a wide range of taxa. We highlight population crashes of invasive ants, which are some of the most widespread and damaging invasive animals. Population collapse or substantial declines have been observed in nearly all of the major invasive ant species including the yellow crazy ant (Anoplolepis gracilipes), Argentine ants (Linepithema humile), big-headed or coastal brown ant (Pheidole megacephala), the tropical fire ant (Solenopsis geminata), red imported fire ants (Solenopsis invicta), and the little fire ant or electric ant (Wasmannia auropunctata). These declines frequently attract little attention, especially compared with their initial invasion phase. Suggested mechanisms for population collapse include pathogens or parasites, changes in the food availability, or even long-term effects of the reproductive biology of invasive ants. A critical component of the collapses may be a reduction in the densities of the invasive ant species, which are often competitively weak in low abundance. We propose that mechanisms causing a reduction in invasive ant abundance may initiate a local extinction vortex. Declines in abundance likely reduce the invasive ant’s competitive ability, resource acquisition and defense capability. These reductions could further reduce the abundance of an invasive ant species, and so on. Management of invasive ants through the use of pesticides is expensive, potentially ecologically harmful, and can be ineffective. We argue that pesticide use may even have the potential to forestall natural population declines and collapses. We propose that in order to better manage these invasive ants, we need to understand and capitalize on features of their population dynamics that promote population collapse.     

Invasion of the alien shrub Prunus laurocerasus in suburban deciduous forests: Effects on native vegetation and soil properties

Most invading alien plants affect native biodiversity and ecosystem functioning. In a field survey, we assessed the impact of the invasive shrub Prunus laurocerasus on the native vegetation and soil properties in suburban deciduous forests in the region of Basel, Switzerland. We installed four pairs of plots in patches of P. laurocerasus and in adjacent not invaded areas in each of twelve forest areas. Native species richness, Shannon-diversity and species composition of the ground vegetation and shrub layer were assessed in each plot. Furthermore, in each plot we measured physical and soil chemical characteristics, enzyme activities and the carbon source utilization pattern of the soil microbial community using Ecoplates™. The maximum age of P. laurocerasus in each plot was determined using tree ring analysis, indicating the time elapsed since the invasive plant has established. A lower native plant species richness in both the ground vegetation and shrub layer was observed in plots with presence of P. laurocerasus. A different species composition of the ground vegetation was also found among plots with and without the invasive shrub. Plots invaded by P. laurocerasus had a lower soil moisture content than control plots. The intensity, diversity and substrate richness of the carbon sources were increased in soil from invaded plots compared to soil in control plots. However, the chemical soil characteristics examined and the activities of enzymes were not influenced by the invasive plant. The effects of P. laurocerasus became more pronounced with the time elapsed since the invasive plant has established. Thus, the removal of young P. laurocerasus individuals would be an appropriate management practice for this invasive shrub species.     

Optimization of control strategies for epidemics in heterogeneous populations with symmetric and asymmetric transmission

There is growing interest in incorporating economic factors into epidemiological models in order to identify optimal strategies for disease control when resources are limited. In this paper we consider how to optimize the control of a pathogen that is capable of infecting multiple hosts with different rates of transmission within and between species. Our objective is to find control strategies that maximize the discounted number of healthy individuals. We consider two classes of host-pathogen system, comprising two host species and a common pathogen, one with asymmetrical and the other with symmetrical transmission rates, applicable to a wide range of SI (susceptible-infected) epidemics of plant and animal pathogens. We motivate the analyses with an example of sudden oak death in California coastal forests, caused by Phytophthora ramorum, in communities dominated by bay laurel (Umbellularia californica) and tanoak (Lithocarpus densiflorus). We show for the asymmetric case that it is optimal to give priority in treating disease to the more infectious species, and to treat the other species only when there are resources left over. For the symmetric case, we show that although a switching strategy is an optimum, in which preference is first given to the species with the lower level of susceptibles and then to the species with the higher level of susceptibles, a simpler strategy that favors treatment of infected hosts for the more susceptible species is a robust alternative for practical application when the optimal switching time is unknown. Finally, since transmission rates are notoriously difficult to estimate, we analyze the robustness of the strategies when the true state with respect to symmetry or otherwise is unknown but one or other is assumed.     

Open removal models with temporary emigration and population dynamics to inform invasive animal management

Removal sampling data are the primary source of monitoring information for many populations (e.g., invasive species, fisheries). Population dynamics, temporary emigration, and imperfect detection are common sources of variation in monitoring data and are key parameters for informing management. We developed two open robust‐design removal models for simultaneously modeling population dynamics, temporary emigration, and imperfect detection: a random walk linear trend model (estimable without ancillary information), and a 2‐age class informed population model (InfoPM, closely related to integrated population models) that incorporated prior information for age‐structured vital rates and relative juvenile availability. We applied both models to multiyear, removal trapping time‐series of a large invasive lizard (Argentine black and white tegu, Salvator merianae) in three management areas of South Florida to evaluate the effectiveness of management programs. Although estimates of the two models were similar, the InfoPMs generally returned more precise estimates, partitioned dynamics into births, deaths, net migration, and provided a decision support tool to predict population dynamics under different effort scenarios while accounting for uncertainty. Trends in tegu superpopulation abundance estimates were increasing in two management areas despite generally high removal rates. However, tegu abundance appeared to decline in the Core management area, where trapping density was the highest and immigration the lowest. Finally, comparing abundance predictions of no‐removal scenarios to those estimated in each management area suggested significant population reductions due to management. These results suggest that local tegu population control via systematic trapping may be feasible with high enough trap density and limited immigration; and highlights the value of these trapping programs. We provided the first estimates of tegu abundance, capture probabilities, and population dynamics, which is critical for effective management. Furthermore, our models are applicable to a wide range of monitoring programs (e.g., carcass recovery or removal point‐counts).     

Embryonic learning and developmental carry-over effects in an invasive anuran

Carry-over effects influence trait responses in later life stages as a result of early experience with environmental cues. Predation risk is an influential stressor and selection exists for early recognition of threats. In particular, invasive species may benefit from carry-over effects by preemptively recognizing and responding to novel predators via latent developmental changes and embryonic learning. In a factorial experiment, we conditioned invasive American bullfrog embryos (Lithobates catesbeianus) to the odor of a novel fish predator, largemouth bass (Micropterus salmoides) alone or in combination with injured conspecific cues. We quantified developmental carryover in the larval life stage and found that individuals conditioned to the highest risk (fish and injured conspecific cues) grew into longer bodied larvae relative to larvae from lower risk treatments. We also assessed embryonic learning, a behavioral carry-over effect, and found an interaction between embryonic conditioning and larval exposure. Behavioral responses were only found in scenarios when predation risk varied in intensity across life history stages, thus requiring a more flexible antipredator strategy. This indicates a potential trade-off between the two strategies in larval growth and development rates, and time until metamorphosis. Our results suggest that early predator exposure and carry-over effects have significant impacts on life history trajectories for American bullfrogs. This research contributes to our understanding of a potentially important invasion mechanism in an anuran species of conservation concern.