Animal Pollination Under Human-Induced Rapid Environmental Change

Billions of wild and semiwild animals live in captive conditions very different from their ancestral environments. Some of the potential challenges they face here, such as greater human proximity, constrained natural behaviours and altered climates, resemble those occurring during urbanization, translocation and other forms of human-induced rapid environmental change (HIREC) in the wild. These parallels between HIREC and captivity suggest that certain species could be in double jeopardy: struggling in both wild and captive environments. This raises new hypotheses for future research, including one tested in this paper: that a species' presence in captivity predicts its chances of establishment when translocated to novel natural habitats. Furthermore, understanding the mechanisms that predispose captive populations to thrive or fail can yield new insights into how animals respond to HIREC. For example, populations adjusting to captivity demonstrate rapid developmental effects. Within one generation, captive-reared animals may show beneficial phenotypic changes (e.g. smaller stress responses than F0s wild caught as adults), illustrating how adaptive developmental plasticity can help populations succeed. However, captive-reared animals also illustrate the risks of developing in evolutionarily new environments (being prone to reduced behavioural flexibility, and sometimes impaired reproduction), suggesting that disrupted ontogeny is one reason why HIREC can be harmful. Overall, analogies between captivity and HIREC are thus interesting and useful. However, captivity and HIREC do differ in some regards, captivity tending to be safer yet more monotonous; we therefore end by discussing how species-typical risk/protective factors, and the phenotypic changes induced in affected animals, may vary between the two. ► Billions of animals live in captive conditions very different from their ancestral environments. ► Some challenges resemble those for translocation and other forms of human-induced rapid environmental change (HIREC). ► Parallels between HIREC and captivity suggest that some species may struggle in both wild and captive environments. ► Common presence in captivity predicted chance of establishment in natural habitats for 99 vertebrate species examined. ► Populations adjusting to captivity show rapid developmental effects, often modelling effects during HIREC.

Understanding variation in behavioural responses to human-induced rapid environmental change: a conceptual overview

Host-parasite interactions increasingly are influenced by human-induced rapid environmental change (HIREC), and the fitness effects of parasitism may be compounded or exacerbated by host traits and/or exposure to additional extrinsic stressors associated with HIREC. Potential interactions between parasitism and different stressors associated with environmental change, however, remain poorly understood for most systems. We examined how parasitism by bird blow flies (Trypocalliphora braueri), ambient weather conditions and habitat disturbance jointly affected offspring traits and juvenile mortality for two declining species of sagebrush songbirds (Brewer's Sparrow, Spizella breweri; and Sage Thrasher, Oreoscoptes montanus) in Wyoming, USA. We evaluated two alternative hypotheses: that parasitism could act (i) in an independent and additive manner with temperature and habitat alteration (Multiple Stressors Hypothesis) or (ii) synergistically to exacerbate the effects of temperature and habitat alteration (Parasitism-HIREC Interaction Hypothesis) on offspring traits and juvenile mortality. We assessed morphometric traits of nestlings and survival of fledglings in relation to parasite loads, temperature and habitat disturbance associated with natural gas development to test these hypotheses. Higher parasite loads and colder temperatures were associated with different effects for nestlings of each host species, reducing tarsus and wing chord length for Brewer's Sparrow and increasing mass for Sage Thrasher. Despite differences in the effect of parasitism on nestling traits, post-fledging mortality risk for both species increased with higher parasite loads. The effects of parasitism and temperature mainly were additive, with limited evidence that weather exacerbated the effects of parasitism. Habitat disturbance had a weak positive effect on nestling tarsus length and post-fledging survival probability for Brewer's Sparrow. Although parasitism rarely results in direct mortality of hosts, parasites can nonetheless exert considerable fitness consequences, especially when combined with extrinsic stressors associated with human-induced environmental changes.

Human-induced rapid environmental change (HIREC) poses threats to a variety of species, and if or how it changes phenotypes is a question of central importance bridging evolutionary ecology and conservation management. Social learning is one type of phenotypic plasticity that can shape organismal responses to HIREC; it allows organisms to acquire phenotypes on a timescale that closely tracks environmental change while minimizing the costs of individual learning. A common assumption in behavioral ecology, is that social learning is generally an adaptive way to cope with HIREC by facilitating the rapid spread of innovative responses to change. While this can be true, social learning can also be maladaptive. It may hinder the spread of adaptive behavior by causing a carryover of old, no longer adaptive behaviors that slow the response to HIREC or even promote the spread of maladaptive behaviors. Here, we present a conceptual framework outlining how an organism’s evolutionary history can shape cognitive mechanisms, social behavior, and population composition, which in turn affect how an organism responds to HIREC. We review quantitative theory and empirical evidence spanning the cultural evolution and behavioral ecology literature discussing how social learning helps or hinders organismal or species’ responses to HIREC. We highlight how mismatch of social learning mechanisms and time-lags in a post-HIREC environment can slow or limit the acquisition of adaptive behavior. We then discuss how different pathways of cultural transmission and social learning strategies can help or hinder responses to HIREC. We also review how HIREC may interfere with the transmission process by altering the public information sent from sender to receiver through the environment before receivers acquire any public information. Lastly, we discuss gaps and future directions including how animals integrate personal and social information, the interaction between personality and social learning, and social learning between heterospecifics.

Human-induced rapid environmental change (HIREC) has recently led to alterations in the fitness and behavior of many organisms. Game theory is an important tool of behavioral ecology for analyzing evolutionary situations involving multiple individuals. However, game theory bypasses the details by which behavioral phenotypes are determined, taking the functional perspective straight from expected payoffs to predicted frequencies of behaviors. In contrast with optimization approaches, we identify that to use existing game theoretic models to predict HIREC effects, additional mechanistic details (or assumptions) will often be required. We illustrate this in relation to the hawk-dove game by showing that three different mechanisms, each of which support the same ESS prior to HIREC (fixed polymorphism, probabilistic choice, or cue dependency), can have a substantial effect on behavior (and success) following HIREC. Surprisingly, an increase in the value of resources can lead to a reduction in payoffs (and vice versa), both in the immediate- and long-term following HIREC. An increase in expected costs also increases expected payoffs. Along with these counter-intuitive findings, this work shows that simply understanding the behavioral payoffs of existing games is insufficient to make predictions about the effects of HIREC.

While migrating, animals make directionally persistent movements and may only respond to human-induced rapid environmental change (HIREC), such as climate and land-use change, once a threshold of HIREC is surpassed. In contrast, animals on other seasonal ranges (e.g., winter range) make more localized and tortuous movements while foraging and may have the flexibility to adjust the location of their range and the intensity of use within it to minimize interactions with HIREC. Because of these seasonal differences in movement, animals on seasonal ranges should avoid areas that contain any level of HIREC, however, during migration, animals should use areas that contain low levels of HIREC, avoiding it only once a threshold of HIREC has been surpassed. We tested this hypothesis using a decade of GPS collar data collected from migratory mule deer (Odocoileus hemionus; n=56 migration, 143 winter) and pronghorn (Antilocapra americana; n=70 migration, 89 winter) that winter on and migrate through a natural gas field in western Wyoming. Using surface disturbance caused by well pads and roads as an index of HIREC, we evaluated behavioral responses across three spatial scales during winter and migration seasons. During migration, both species tolerated low levels of disturbance. Once a disturbance threshold was surpassed, however, they avoided HIREC. For mule deer, thresholds were consistently ~3%, whereas thresholds for pronghorn ranged from 1% to 9.25% surface disturbance. In contrast to migration, both species generally avoided all levels of HIREC while on winter range. Our study suggests that animal responses to HIREC are mediated by season-specific movement patterns. Our results provide further evidence of ungulates avoiding human disturbance on winter range and reveal disturbance thresholds that trigger mule deer and pronghorn responses during migration: information that managers can use to maintain the ecological function of migration routes and winter ranges.

Human-induced rapid environmental change (HIREC) has altered landscape processes and negatively impacted many species globally. Some of the most dramatic changes have been in wetlands where flows have been disrupted, and new wetlands have been created to retain runoff. In response to disrupted natural wetland conditions, Wood Stork (Mycteria americana) populations in South Florida have significantly declined over the past several decades. Despite the well-documented sensitivity of Wood Storks to natural wetland conditions, Wood Storks are often observed foraging in roadside created wetlands; however, the availability of prey in created wetlands is currently unknown. We sampled natural and created wetlands to determine aquatic fauna available for foraging Wood Storks. To determine prey use, we collected food boluses from Wood Storks in both natural wetland and urban landscapes. Historical studies found nonnative fish were absent in Wood Stork diet prior to the dominance of created wetlands in the landscape; however, we found nonnative fish frequently in both created wetlands and boluses. Furthermore, urban nesting Wood Storks consumed large-bodied prey species that were more characteristic of created wetlands whereas Wood Storks nesting in natural wetlands consumed large-bodied prey more characteristic of natural wetlands. Overall, Wood Storks consumed prey that were more similar to the fish community in created wetlands than those in natural wetlands. These dietary patterns suggest that Wood Storks have behavioral plasticity in both foraging habitat and prey use to cope with HIREC. Conservation efforts for species existing in both natural and urban habitats should consider the importance of novel prey and foraging habitats, as they may assist in sustaining populations in a rapidly changing world.

Human-induced rapid environmental changes often cause behavioural alterations in animals. The consequences that these alterations in turn have for the viability of populations are, however, poorly known. We used a population of threespine sticklebacks Gasterosteus aculeatus in the Baltic Sea to investigate the consequences of behavioural responses to human-induced eutrophication for offspring production. The investigated population has been growing during the last decades, and one cause could be increased offspring production. We combined field-based surveys with laboratory-based experiments, and found that an enhanced growth of macroalgae relaxed agonistic interactions among males. This allowed more males to nest, improved hatching success, and increased the number of reproductive cycles that males completed. Thus, the behavioural responses were adaptive at the individual level and increased offspring production. However, a larger proportion of small males of low competitive ability reproduced in dense vegetation. As male size and dominance are heritable, this could influence the genetic composition of the offspring. Together with a higher number of offspring produced, this could influence natural selection and the rate of adaptation to the changing environment. Thus, behavioural responses to a rapid human-induced environmental change can influence offspring production, with potential consequences for population dynamics and evolutionary processes.

Integrating environmental complexity and the plasticity-first hypothesis to study responses to human-altered habitats

A fundamental focus of current ecological and evolutionary research is to illuminate the drivers of animals' success in coping with human-induced rapid environmental change (HIREC). Behavioural adaptations are likely to play a major role in coping with HIREC because behaviour largely determines how individuals interact with their surroundings. A substantial body of research reports behavioural modifications in urban dwellers compared to rural conspecifics. However, it is often unknown whether the observed phenotypic divergence is due to phenotypic plasticity or the product of genetic adaptations. Here, we aimed at investigating (a) whether behavioural differences arise also between rural and urban populations of non-commensal rodents; and (b) whether these differences result from behavioural flexibility or from intrinsic behavioural characteristics, such as genetic or maternal effects. We captured and kept under common environment conditions 42 rural and 52 urban adult common voles (Microtus arvalis) from seven subpopulations along a rural-urban gradient. We investigated individual variation in behavioural responses associated with risk-taking and exploration, in situ at the time of capture in the field and ex situ after 3months in captivity. Urban dwellers were bolder and more explorative than rural conspecifics at the time of capture in their respective sites (in situ). However, when tested under common environmental conditions ex situ, rural individuals showed little change in their behavioural responses whereas urban individuals altered their behaviour considerably and were consistently shyer and less explorative than when tested in situ. The combination of elevated risk-taking and exploration with high behavioural flexibility might allow urban populations to successfully cope with the challenges of HIREC. Investigating whether the observed differences in behavioural flexibility are adaptive and how they are shaped by additive and interactive effects of genetic make-up and past environmental conditions will help illuminate eco-evolutionary dynamics under HIREC and predict persistence of populations under urban conditions.

The current and cascading effects of global change challenges the interactions both between animal individuals (i.e. social and sexual behaviour) and the environment they inhabit. Amphibians are an ecologically diverse class with a wide range of social and sexual behaviours, making them a compelling model to understand the potential adaptations of animals faced with the effects of human-induced rapid environmental changes (HIREC). Poison frogs (Dendrobatoidea) are a particularly interesting system, as they display diverse social behaviours that are shaped by conspecific and environmental interactions, thus offering a tractable system to investigate how closely related species may respond to the impacts of HIREC. Here, we discuss the potential impacts of global change on poison frog behaviour, and the future challenges this group may face in response to such change. We pay special attention to parental care and territoriality, which are emblematic of this clade, and consider how different species may flexibly respond and adapt to increasingly frequent and diverse anthropogenic stress. More specifically, we hypothesise that some parents may increase care (i.e. clutch attendance and distance travelled for tadpole transport) in HIREC scenarios and that species with more generalist oviposition and tadpole deposition behaviours may fare more positively than their less flexible counterparts; we predict that the latter may either face increased competition for resources limited by HIREC or will be forced to adapt and expand their natural preferences. Likewise, we hypothesise that human-driven habitat alteration will disrupt the acoustic and visual communication systems due to increased noise pollution and/or changes in the surrounding light environment. We highlight the need for more empirical research combining behavioural ecology and conservation to better predict species’ vulnerability to global change and efficiently focus conservation efforts.

Many animals respond well behaviorally to stimuli associated with human-induced rapid environmental change (HIREC), such as novel predators or food sources. Yet others make errors and succumb to evolutionary traps: approaching or even preferring low quality, dangerous or toxic options, avoiding beneficial stimuli, or wasting resources responding to stimuli with neutral payoffs. A common expectation is that learning should help animals adjust to HIREC; however, learning is not always expected or even favored in many scenarios that expose animals to ecological and evolutionary traps. We propose a conceptual framework that aims to explain variation in when learning can help animals avoid and escape traps caused by HIREC. We first clarify why learning to correct two main types of errors (avoiding beneficial options, and not avoiding detrimental options) might be difficult (limited by constraints). We then identify and discuss several key behavioral mechanisms (adaptive sampling, generalization, habituation, reversal learning) that can be targeted to help animals learn to avoid traps. Finally, we discuss how individual differences in neophobia/neophilia and personality relate to learning in the context of HIREC traps, and offer some general guidance for disarming traps. Given how devastating traps can be for animal populations, any breakthrough in mitigating trap outcomes via learning could make the difference in developing effective solutions.

Endangered species have small, unsustainable population sizes that are geographically or genetically restricted. Ex-situ conservation programmes are therefore faced with the challenge of breeding sufficiently sized, genetically diverse populations earmarked for reintroduction that have the behavioural skills to survive and breed in the wild. Yet, maintaining historically beneficial behaviours may be insufficient, as research continues to suggest that certain cognitive-behavioural skills and flexibility are necessary to cope with human-induced rapid environmental change (HIREC). This paper begins by reviewing interdisciplinary studies on the ‘captivity effect’ in laboratory, farmed, domesticated and feral vertebrates and finds that captivity imposes rapid yet often reversible changes to the brain, cognition and behaviour. However, research on this effect in ex-situ conservation sites is lacking. This paper reveals an apparent mismatch between ex-situ enrichment aims and the cognitive-behavioural skills possessed by animals currently coping with HIREC. After synthesizing literature across neuroscience, behavioural biology, comparative cognition and field conservation, it seems that ex-situ endangered species deemed for reintroduction may have better chances of coping with HIREC if their natural cognition and behavioural repertoires are actively preserved. Evaluating the effects of environmental challenges rather than captivity per se is recommended, in addition to using targeted cognitive enrichment.

Fresh waters are particularly vulnerable to climate change because (i) many species within these fragmented habitats have limited abilities to disperse as the environment changes; (ii) water temperature and availability are climate-dependent; and (iii) many systems are already exposed to numerous anthropogenic stressors. Most climate change studies to date have focused on individuals or species populations, rather than the higher levels of organization (i.e. communities, food webs, ecosystems). We propose that an understanding of the connections between these different levels, which are all ultimately based on individuals, can help to develop a more coherent theoretical framework based on metabolic scaling, foraging theory and ecological stoichiometry, to predict the ecological consequences of climate change. For instance, individual basal metabolic rate scales with body size (which also constrains food web structure and dynamics) and temperature (which determines many ecosystem processes and key aspects of foraging behaviour). In addition, increasing atmospheric CO(2) is predicted to alter molar CNP ratios of detrital inputs, which could lead to profound shifts in the stoichiometry of elemental fluxes between consumers and resources at the base of the food web. The different components of climate change (e.g. temperature, hydrology and atmospheric composition) not only affect multiple levels of biological organization, but they may also interact with the many other stressors to which fresh waters are exposed, and future research needs to address these potentially important synergies.

Human-Induced Rapid Environmental Change (HIREC), particularly climate change and habitat conversion, affects species distributions worldwide. Here, we aimed to (i) assess the factors that determine range patterns of European badger (Meles meles) at the southwestern edge of their distribution and (ii) forecast the possible impacts of future climate and landcover changes on those patterns. We surveyed 272 cells of 5 × 5 km, to assess badger presence and confirmed its occurrence in 95 cells (35%). Our models estimate that badger’s presence is promoted by the occurrence of herbaceous fields and shrublands (5%–10%), and low proportions of Eucalyptus plantations (<~15%). Regions with >50% of podzols and eruptive rocks, higher sheep/goat density (>4 ind/km2), an absence of cattle, intermediate precipitation regimes (800–1000 mm/year) and mild mean temperatures (15–16 °C) are also more likely to host badgers. We predict a decrease in favourability of southern areas for hosting badgers under forecasted climate and landcover change scenarios, which may lead to a northwards retraction of the species southern distribution limit, but the overall landscape favourability is predicted to slightly increase. The forecasted retraction may affect community functional integrity, as its role in southern ecological networks will be vacant.