Assessing the Vulnerabilities of Vertebrate Species to Light and Noise Pollution: Expert Surveys Illuminate the Impacts on Specialist Species.

Global expansion of lighting and noise pollution alters how animals receive and interpret environmental cues. However, we lack a cross-taxon understanding of how animal traits influence species vulnerability to this growing phenomenon. This knowledge is needed to improve the design and implementation of policies that mitigate or reduce sensory pollutants. We present results from an expert knowledge survey that quantified the relative influence of 21 ecological, anatomical, and physiological traits on the vulnerability of terrestrial vertebrates to elevated levels of anthropogenic lighting and noise. We aimed not only to quantify the importance of threats and the relative influence of traits as viewed by sensory and wildlife experts, but to examine knowledge gaps based on the variation in responses. Identifying traits that had less consensus can guide future research for strengthening ecologists' and conservation biologists' understanding of sensory abilities. Our findings, based on 280 responses of expert opinion, highlight the increasing recognition among experts that sensory pollutants are important to consider in management and conservation decisions. Participant responses show mounting threats to species with narrow niches; especially habitat specialists, nocturnal species, and those with the greatest ability to differentiate environmental visual and auditory cues. Our results call attention to the threat specialist species face and provide a generalizable understanding of which species require additional considerations when developing conservation policies and mitigation strategies in a world altered by expanding sensory pollutant footprints. We provide a step-by-step example for translating these results to on-the-ground conservation planning using two species as case studies.

Direct and Ambient Light Pollution Alters Recruitment for a Diurnal Plant-Pollinator System.

Artificial light at night (ALAN) functions as a novel environmental stimulus that has the potential to disrupt interactions among species. Despite recent efforts to explain nocturnal pollinators' responses to this stimulus, the likelihood and associated mechanisms of attraction toward artificial light and potential consequences on fitness for diurnal pollinators are still largely unclear. Here, we took advantage of the obligate mutualism between yucca moths (Tegeticula maculata maculata) and yucca plants (Hesperoyucca whipplei) to understand how direct light exposure and skyglow can influence a pairwise plant-pollinator interaction. To surmise whether adult moths exhibit positive phototaxis, we deployed a set of field-placed light towers during the peak of yucca flowering and compared the number of moths caught in traps between dark-controlled and light-treated trials. Adult moth abundance was much higher when light was present, which suggests that ALAN may alter this diurnal moth's activity patterns to expand their temporal niche into the night. To evaluate ALAN effects on yucca fruit set and moth larva recruitment, we measured skyglow exposure above yucca plants and direct light intensity from a second set of light towers. Both larva and fruit recruitment increased with skyglow, and fruit set also increased with direct lighting, but the relationship was weaker. Contrarily, larva recruitment did not change when exposed to a gradient of direct light, which may instead reflect effects of ALAN on moth physiology, such as disrupted female oviposition, or misdirecting behaviors essential to oviposition activity. Our results suggest that ALAN can positively influence the fitness of both plants and moths in this tightly co-evolved mutualism, but the benefits to each species may depend on whether night lighting is direct or indirect. Whether such effects and mechanisms could relate to susceptibility to the presence of ALAN on this or other plant-pollinator relationships will remain an important focus of future research.

Evolutionary novelty in communication between the sexes.

The diversity of signalling traits within and across taxa is vast and striking, prompting us to consider how novelty evolves in the context of animal communication. Sexual selection contributes to diversification, and here we endeavour to understand the initial conditions that facilitate the maintenance or elimination of new sexual signals and receiver features. New sender and receiver variants can occur through mutation, plasticity, hybridization and cultural innovation, and the initial conditions of the sender, the receiver and the environment then dictate whether a novel cue becomes a signal. New features may arise in the sender, the receiver or both simultaneously. We contend that it may be easier than assumed to evolve new sexual signals because sexual signals may be arbitrary, sexual conflict is common and receivers are capable of perceiving much more of the world than just existing sexual signals. Additionally, changes in the signalling environment can approximate both signal and receiver changes through a change in transmission characteristics of a given environment or the use of new environments. The Anthropocene has led to wide-scale disruption of the environment and may thus generate opportunity to directly observe the evolution of new signals to address questions that are beyond the reach of phylogenetic approaches.

Why conservation biology can benefit from sensory ecology.

Global expansion of human activities is associated with the introduction of novel stimuli, such as anthropogenic noise, artificial lights and chemical agents. Progress in documenting the ecological effects of sensory pollutants is weakened by sparse knowledge of the mechanisms underlying these effects. This severely limits our capacity to devise mitigation measures. Here, we integrate knowledge of animal sensory ecology, physiology and life history to articulate three perceptual mechanisms-masking, distracting and misleading-that clearly explain how and why anthropogenic sensory pollutants impact organisms. We then link these three mechanisms to ecological consequences and discuss their implications for conservation. We argue that this framework can reveal the presence of 'sensory danger zones', hotspots of conservation concern where sensory pollutants overlap in space and time with an organism's activity, and foster development of strategic interventions to mitigate the impact of sensory pollutants. Future research that applies this framework will provide critical insight to preserve the natural sensory world.

Diversity in warning coloration: selective paradox or the norm?

Aposematic theory has historically predicted that predators should select for warning signals to converge on a single form, as a result of frequency-dependent learning. However, widespread variation in warning signals is observed across closely related species, populations and, most problematically for evolutionary biologists, among individuals in the same population. Recent research has yielded an increased awareness of this diversity, challenging the paradigm of signal monomorphy in aposematic animals. Here we provide a comprehensive synthesis of these disparate lines of investigation, identifying within them three broad classes of explanation for variation in aposematic warning signals: genetic mechanisms, differences among predators and predator behaviour, and alternative selection pressures upon the signal. The mechanisms producing warning coloration are also important. Detailed studies of the genetic basis of warning signals in some species, most notably Heliconius butterflies, are beginning to shed light on the genetic architecture facilitating or limiting key processes such as the evolution and maintenance of polymorphisms, hybridisation, and speciation. Work on predator behaviour is changing our perception of the predator community as a single homogenous selective agent, emphasising the dynamic nature of predator-prey interactions. Predator variability in a range of factors (e.g. perceptual abilities, tolerance to chemical defences, and individual motivation), suggests that the role of predators is more complicated than previously appreciated. With complex selection regimes at work, polytypisms and polymorphisms may even occur in Müllerian mimicry systems. Meanwhile, phenotypes are often multifunctional, and thus subject to additional biotic and abiotic selection pressures. Some of these selective pressures, primarily sexual selection and thermoregulation, have received considerable attention, while others, such as disease risk and parental effects, offer promising avenues to explore. As well as reviewing the existing evidence from both empirical studies and theoretical modelling, we highlight hypotheses that could benefit from further investigation in aposematic species. Finally by collating known instances of variation in warning signals, we provide a valuable resource for understanding the taxonomic spread of diversity in aposematic signalling and with which to direct future research. A greater appreciation of the extent of variation in aposematic species, and of the selective pressures and constraints which contribute to this once-paradoxical phenomenon, yields a new perspective for the field of aposematic signalling.

Environment-dependent attack rates of cryptic and aposematic butterflies.

Many organisms have evolved adaptive coloration that reduces their risk of predation. Cryptic coloration reduces the likelihood of detection/recognition by potential predators, while warning or aposematic coloration advertises unprofitability and thereby reduces the likelihood of attack. Although some studies show that aposematic coloration functions better at decreasing attack rate than crypsis, recent work has suggested and demonstrated that crypsis and aposematism are both successful strategies for avoiding predation. Furthermore, the visual environment (e.g., ambient lighting, background) affects the ability for predators to detect prey. We investigated these 2 related hypotheses using 2 well-known visually aposematic species of Heliconius butterflies, which occupy different habitats (open-canopy vs. closed-canopy), and one palatable, cryptic, generalist species Junonia coenia. We tested if the differently colored butterflies differ in attack rates by placing plasticine models of each of the 3 species in 2 different tropical habitats where the butterflies naturally occur: disturbed, open-canopy habitat and forested, closed-canopy habitat. The cryptic model had fewer attacks than one of the aposematic models. Predation rates differed between the 2 habitats, with the open habitat having much higher predation. However, we did not find an interaction between species and habitat type, which is perplexing due to the different aposematic phenotypes naturally occurring in different habitats. Our findings suggest that during the Panamanian dry season avian predation on perched butterflies is not a leading cause in habitat segregation between the 2 aposematic species and demonstrate that cryptically colored animals at rest may be better than aposematic prey at avoiding avian attacks in certain environments.

Enlightening Butterfly Conservation Efforts: The Importance of Natural Lighting for Butterfly Behavioral Ecology and Conservation.

Light is arguably the most important abiotic factor for living organisms. Organisms evolved under specific lighting conditions and their behavior, physiology, and ecology are inexorably linked to light. Understanding light effects on biology could not be more important as present anthropogenic effects are greatly changing the light environments in which animals exist. The two biggest anthropogenic contributors changing light environments are: (1) anthropogenic lighting at night (i.e., light pollution); and (2) deforestation and the built environment. I highlight light importance for butterfly behavior, physiology, and ecology and stress the importance of including light as a conservation factor for conserving butterfly biodiversity. This review focuses on four parts: (1) Introducing the nature and extent of light. (2) Visual and non-visual light reception in butterflies. (3) Implications of unnatural lighting for butterflies across several different behavioral and ecological contexts. (4). Future directions for quantifying the threat of unnatural lighting on butterflies and simple approaches to mitigate unnatural light impacts on butterflies. I urge future research to include light as a factor and end with the hopeful thought that controlling many unnatural light conditions is simply done by flipping a switch.

Cool Bands: Wing bands decrease rate of heating, but not equilibrium temperature in Anartia fatima.

Butterflies regulate their internal thoracic temperature in order to optimize performance activities (e.g. flight, foraging). Previous research has shown that butterfly wings, particularly the innermost portions, play a role in thermoregulation. We investigated to see whether a lightly colored wing band would alter the thermal properties of the banded peacock butterfly (Anartia fatima) with two within subject experiments in a laboratory setting: (1) band color manipulation in which euthanized individuals were heated to thermal equilibrium with the band unaltered and then again with the wing darkened; (2) wing ablation in which individuals already run through experiment 1 were heated to equilibrium two more times; once with the outer portion of the wing including the band removed and then with the entire wing removed. Individuals were spread so that the dorsal surface of the wing was exposed to illumination from a lamp suspended above. Twelve Anartia fatima males were collected in Panama and were run through experiment one. Four individuals were run through experiment two. We found no effect of darkening the band on the internal thoracic equilibrium temperature, but the darkened band did increase the rate of heating. The wing ablation experiment revealed that wing removal lowered the internal thoracic equilibrium temperature but did not affect the heating rate. Therefore we show that butterfly bands may be important in butterfly thermoregulation and we discuss the importance of the wing band on thermoregulatory abilities in Anartia fatima with respect to the butterfly's natural history. We conclude that the wing band may allow butterflies to reduce heat stress induced by their warm environments.

Mimicry's palette: widespread use of conserved pigments in the aposematic signals of snakes.

Mimicry, where one species resembles another species because of the selective benefits of sharing a common signal, is especially common in snakes. Snakes might be particularly prone to evolving mimicry if all species share some of the same proximate mechanisms that can be used to produce aposematic/mimetic signals. We evaluated this possibility by examining color pigments in 11 species of snakes from four different families, three species of which participate in a coral snake mimicry complex involving convergence in coloration. We found that all 11 species used combinations of two pteridine pigments and melanin in their coloration, regardless of whether or not they were mimics. Furthermore, the presence or absence of red pteridines was strongly correlated with the relative excitation of medium- and long-wavelength photoreceptors in birds, thereby linking shared pigmentation to perception of those pigments by likely agents of selection. Thus, precise color mimicry might be relatively easy to evolve among snakes owing to symplesiomorphies in pigmentation.