Conservation implications of anthropogenic impacts on visual communication and camouflage

Anthropogenic environmental impacts can disrupt the sensory environment of animals and affect important processes from mate choice to predator avoidance. Currently, these effects are best understood for auditory and chemosensory modalities, and recent reviews highlight their importance for conservation. We examined how anthropogenic changes to the visual environment (ambient light, transmission, and backgrounds) affect visual communication and camouflage and considered the implications of these effects for conservation. Human changes to the visual environment can increase predation risk by affecting camouflage effectiveness, lead to maladaptive patterns of mate choice, and disrupt mutualistic interactions between pollinators and plants. Implications for conservation are particularly evident for disrupted camouflage due to its tight links with survival. The conservation importance of impaired visual communication is less documented. The effects of anthropogenic changes on visual communication and camouflage may be severe when they affect critical processes such as pollination or species recognition. However, when impaired mate choice does not lead to hybridization, the conservation consequences are less clear. We suggest that the demographic effects of human impacts on visual communication and camouflage will be particularly strong when human‐induced modifications to the visual environment are evolutionarily novel (i.e., very different from natural variation); affected species and populations have low levels of intraspecific (genotypic and phenotypic) variation and behavioral, sensory, or physiological plasticity; and the processes affected are directly related to survival (camouflage), species recognition, or number of offspring produced, rather than offspring quality or attractiveness. Our findings suggest that anthropogenic effects on the visual environment may be of similar importance relative to conservation as anthropogenic effects on other sensory modalities.     

Signaling in multiple modalities in male rhesus macaques: sex skin coloration and barks in relation to androgen levels, social status, and mating behavior

The past decade has seen an increasing shift in animal communication towards more studies that incorporate aspects of signaling in multiple modalities. Although nonhuman primates are an excellent group for studying the extent to which different aspects of condition may be signaled in different modalities, and how such information may be integrated during mate choice, very few studies of primate species have incorporated such analyses. Here, we present data from free-ranging male rhesus macaques on sex skin coloration (modeled to receiver perception), bark vocal signals, androgen levels, morphometric variables, dominance status, and female mate choice. We show that, consistent with data on females, most intra- and interindividual variation in sex skin appearance occurs in luminance rather than color. Sex skin luminance was significantly correlated across different skin regions. Sex skin luminance did not correlate with the majority of bark parameters, suggesting the potential for the two signals to convey different information. Sex skin appearance was not related to androgen levels although we found some evidence for links between androgen levels and bark parameters, several of which were also related to morphometric variables. We found no evidence that either signal was related to male dominance rank or used in female mate choice, though more direct measures of female proceptive behavior are needed. Overall, the function of male sex skin coloration in this species remains unclear. Our study is among the first nonhuman primate studies to incorporate measurements of multiple signals in multiple modalities, and we encourage other authors to incorporate such analyses into their work.     

A game theoretic approach to multimodal communication

Over the last few decades the animal communication community has become increasingly aware that much communication occurs using multiple signals in multiple modalities. The majority of this work has been empirical, with less theoretical work on the advantages conferred by such communication. In the present paper, we ask: Why should animals communicate with multiple signals in multiple modalities? To tackle this question we use game theoretic techniques, and highlight developments in the economic signaling literature that might offer insight into biological problems. We start by establishing a signaling game, and investigate signal honesty under two prevailing paradigms of honest communication – costly signaling and cheap talk. In both paradigms, without further constraint, it is simple to show that anything that can be achieved with multiple signals can be achieved with one. We go on to investigate different sets of possible constraints that may make multiple signals and multimodal signals in particular more likely to evolve. We suggest that constraints on cost functions and bandwidths, orthogonal noise across modalities, strategically distinct modes, multiple qualities, multiple signalers, and multiple audiences, all provide biologically plausible scenarios that theoretically favor multiple and multimodal signaling.     

Ten unanswered questions in multimodal communication

The study of multimodal communication has become an active and vibrant field. This special issue of Behavioral Ecology and Sociobiology brings together new developments in this rapidly expanding area. In this final contribution to the special issue, I look to the future and discuss ten questions in need of further work, touching on issues ranging from theoretical modeling and the evolution of behavior to molecular mechanisms and the development of behavior. In particular, I emphasize that the use of multimodal communication allows animals to switch between sensory channels when one channel becomes too noisy, and suggest that a better understanding of this process may help us both to understand the evolution of multisensory signaling and to predict the success of species facing environmental changes that affect signaling channels, such as urbanization and climate change. An expanded section is included on the effects of climate change on animal communication across sensory channels, urging researchers to pursue this topic due to the rapidity with which the environment is currently transforming.     

A comparison of visual and olfactory learning performance in the bumblebee Bombus terrestris

Animals use cues from a range of sensory modalities to discriminate stimuli and as predictors of reward. Whilst there is appreciable variation in the cognitive performance of animals, we know surprisingly little about the extent to which learning varies among individuals across different sensory modalities. Do individuals that are good at learning in one sensory modality also perform well in another (performance is correlated between modalities), or do individuals demonstrate specialisation in learning performance in one modality (trading-off performance between modalities)? We tested these hypotheses by examining the performance of 76 Bombus terrestris workers, from four colonies, in both an odour-and visual learning task. Olfactory learning was assessed using proboscis extension reflex (PER) conditioning and visual (colour) learning was examined using a well-established free-flying paradigm. Our results showed neither a correlation, nor a trade-off, in individual performance for learning tasks using different sensory modalities. However, there was considerable variation among workers within each colony in their performance in both learning tasks. This extent of interindividual variation in learning ability across sensory modalities could be adaptive for colonies dealing with changeable foraging conditions. There was also significant intercolony variation in final task performance level in the olfactory learning task, and both the strength and persistence of blue preference in the colour learning task. This is the first study to demonstrate variation in olfactory learning performance across multiple bumblebee colonies using PER conditioning, suggesting this is an effective paradigm for assessing associative olfactory learning performance both within and among colonies.     

Facial asymmetry is negatively related to condition in female macaque monkeys

The face is an important visual trait in social communication across many species. In evolutionary terms, there are large and obvious selective advantages in detecting healthy partners, both in terms of avoiding individuals with poor health to minimise contagion and in mating with individuals with high health to help ensure healthy offspring. Many models of sexual selection suggest that an individual's phenotype provides cues to their quality. Fluctuating asymmetry is a trait that is proposed to be an honest indicator of quality, and previous studies have demonstrated that rhesus monkeys gaze longer at symmetric faces, suggesting preferences for such faces. The current study examined the relationship between measured facial symmetry and measures of health in a captive population of female rhesus macaque monkeys. We measured asymmetry from landmarks marked on front-on facial photographs and computed measures of health based on veterinary health and condition ratings, number of minor and major wounds sustained and gain in weight over the first 4?years of life. Analysis revealed that facial asymmetry was negatively related to condition-related health measures, with symmetric individuals being healthier than more asymmetric individuals. Facial asymmetry appears to be an honest indicator of health in rhesus macaques, and asymmetry may then be used by conspecifics in mate-choice situations. More broadly, our data support the notion that faces are valuable sources of information in non-human primates and that sexual selection based on facial information is potentially important across the primate lineage.     

Circatidal swimming activity rhythm in a subtidal cumacean Dimorphostylis asiatica (Crustacea)

Dimorphostylis asiatica, a cumacean crustacea inhabiting the sublittoral line of the Seto Inland Sea, shows a rhythmic pattern of swimming activity coinciding with daily and tidal components in the field. This activity pattern was bimodal at first, i.e., circatidal activity coinciding with high tides at their habitat. The mean free-running period (i.e., bitidal interval) of this endogenous rhythm was 23.1 h at 10°C, which was significantly shorter than the environmental tidal cycle. In most cases (90% of the records) this bimodal activity became unimodal within 10 d. The unimodal period was 24 to 27.5 h, which is markedly longer than the preceding bimodal period. The bimodal pattern observed in the present study was not observed in the field. The difference between field and laboratory activity patterns can be explained in terms of direct response of the bimodal circatidal rhythm to the day-night cycle in the field. Field observations were made and laboratory experiments conducted between 1988 and 1992.     

Variation in the temporal and spatial use of signals and its implications for multimodal communication

The use of signals across multiple sensory modalities in communication is common in animals and plants. Determining the information that each signal component conveys has provided unique insights into why multimodal signals evolve. However, how these complex signals are assessed by receivers will also influence their evolution, a hypothesis that has received less attention. Here, we explore multimodal signal assessment in a closely related complex of island flycatchers that have diverged in visual and acoustic signals. Using field experiments that manipulated song and plumage colour, we tested if song, a possible long-range signal, is assessed before plumage colour in conspecific recognition. We find that divergent song and colour are assessed in sequence, and this pattern of sequential assessment is likely mediated by habitat structure and the extent of differences in signal characteristics. A broad survey of the literature suggests that many organisms from a wide range of taxa sequentially assess multimodal signals, with long-range signals attracting conspecifics for further assessment of close-range signals. Our results highlight the need to consider how signals are assessed when understanding multimodal signal evolution. Finally, given the results of our field experiments indicating sequential assessment of divergent song and colour in the recognition of conspecifics, we discuss the consequences of multimodal signal divergence for the origin of species, as changes in signals across different sensory modalities may influence the evolution of premating reproductive isolation.     

The dominance of seismic signaling and selection for signal complexity in Schizocosa multimodal courtship displays

Schizocosa wolf spiders show tremendous diversity in courtship complexity, with different species employing varying numbers of components within and across sensory modalities. Using a comparative approach, we investigate the importance of each signaling modality in the courtship display of five Schizocosa species (three stridulating and two drumming) by assessing mating success under manipulated signaling environments. Irrespective of the degree of male ornamentation, the three stridulating species exhibit a dependence on the seismic, but not visual, signaling environment for mating success. Mating was independent of signaling environment for the two drumming species. We next ask whether the degree to which each species depends upon a signaling modality for mating (i.e., modality importance) is correlated with the estimated modality-specific signal complexity. We first calculate effect sizes for the influence of seismic versus visual signaling environments on the likelihood to mate for ten Schizocosa species and then use an element-counting approach to calculate seismic and visual signal complexity scores. We use a phylogenetic regression analysis to test two predictions: (1) the importance of seismic signaling is correlated with seismic signal complexity and (2) the importance of visual signaling is correlated with visual signal complexity. We find a significant relationship between visual signal importance and visual signal complexity, but no relationship between seismic signal importance and seismic signal complexity. Finally, we test the hypothesis that selection acts on complexity per se by determining whether seismic and visual signal complexity is correlated across species. We find support for this hypothesis in a significant relationship between seismic and visual signal complexity.     

浅论语境在言语交际中的作用

语境是言语交际中生成、实现并制约言语行为的相关因素的总和．本文通过分析语境诸因素中两大重要因素即交际对象、时空因素对于言语交际活动的影响，阐明言语交际过程中注重语境的重要性．     

Carotenoid-rich mouth colors influence the conspicuousness of nestling birds

When allocating investment among offspring, parents might maximize their fitness by biasing investment toward offspring with the best direct fitness prospects. The observed preferences of avian parents for carotenoid-rich mouth colors that advertise good condition has been interpreted as support for this hypothesis. However, because these condition-dependent visual signals might also make offspring more visually conspicuous, active parental preferences for carotenoid-rich traits are difficult to distinguish from passive responses to differences in detectability among offspring. Here, we used a visual model to examine how mouth colors influence the visual conspicuousness of nestling house sparrows (Passer domesticus) to parents under a suite of realistic ambient light conditions. We found little evidence that mouths rich in carotenoids provided more conspicuous targets to parents than mouths poor in carotenoids. While other features of mouth color may have evolved to increase conspicuousness, our results suggest that carotenoid-based coloration is not a product of detectability pressures and rather may serve as a signal of nestling quality.     

Multimodal signals increase active space of communication by wolf spiders in a complex litter environment

Multimodal signals may compensate for environmental constraints on communication, as signals in different modalities vary in efficacy. We examined the influence of complex microhabitats on transmission of vibratory and visual signals of courting male Schizocosa ocreata wolf spiders (Araneae: Lycosidae) with laser Doppler vibrometry (LDV) and behavioral observations in lab and field. We measured maximum potential detection distance of visual and vibratory signals by females in laboratory mesocosms, recorded vibration signal attenuation on different substrates, and estimated transmission distances for male vibration signals in the field. We also determined effective line-of-sight visual detection distances in the field with laser distance measures. Together, these data were used to estimate the potential and effective active space of multimodal signals. LDV measures show leaves are highly conductive substrates for wolf spider vibratory signals compared to others (soil, wood, rock). For both visual and vibratory modes, lab estimates of maximum potential distance for signal transmission and detection (behavior studies) exceeded estimates of effective active space (signal attenuation, “vanishing point,” and “line-of-sight” measures). Field estimates of transmission distance for signal modes overlap, such that in close range (<20 cm), vibratory signals are more likely to be detected, while farther away, visual signals are more likely to be seen. These findings thus support current hypotheses regarding how multimodal communication might extend the range of overall signal active space or compensate for environmental constraints.     

Bold minnows consistently approach danger in the field and lab in response to either chemical or visual indicators of predation risk

A behavioral syndrome is a suite of behaviors correlated across multiple social contexts. In this study, boldness in the face of predation risk was assessed twice in fish across two different sensory modalities in both the field and lab to ascertain the biological relevance and complexity of this attribute. Individual fathead minnows were captured from a natural field population using traps that either contained chemical alarm cues (conspecific skin extract) or control (well water) and their responses to the presence of predator behind a glass partition assessed in the laboratory. Although fewer fish were captured in alarm cue-labeled traps, these bold fish performed longer predator inspections than shy fish captured in control traps. Thus, a shy/bold behavioral syndrome was expressed consistently across field and lab settings in response to both chemical and visual indicators of danger. Shy and bold individuals did not differ in sex, body length, secondary sexual characteristics, or parasite load but were of more robust physical condition.     

Signal recognition by frogs in the presence of temporally fluctuating chorus-shaped noise

The background noise generated in large social aggregations of calling individuals is a potent source of auditory masking for animals that communicate acoustically. Despite similarities with the so-called "cocktail-party problem" in humans, few studies have explicitly investigated how non-human animals solve the perceptual task of separating biologically relevant acoustic signals from ambient background noise. Under certain conditions, humans experience a release from auditory masking when speech is presented in speech-like masking noise that fluctuates in amplitude. We tested the hypothesis that females of Cope's gray treefrog (Hyla chrysoscelis) experience masking release in artificial chorus noise that fluctuates in level at modulations rates characteristic of those present in ambient chorus noise. We estimated thresholds for recognizing conspecific advertisement calls (pulse rate=40-50 pulses/s) in the presence of unmodulated and sinusoidally amplitude modulated (SAM) chorus-shaped masking noise. We tested two rates of modulation (5 Hz and 45 Hz) because the sounds of frog choruses are modulated at low rates (e.g., less than 5-10 Hz), and because those of species with pulsatile signals are additionally modulated at higher rates typical of the pulse rate of calls (e.g., between 15-50 Hz). Recognition thresholds were similar in the unmodulated and 5-Hz SAM conditions, and 12 dB higher in the 45-Hz SAM condition. These results did not support the hypothesis that female gray treefrogs experience masking release in temporally fluctuating chorus-shaped noise. We discuss our results in terms of modulation masking, and hypothesize that natural amplitude fluctuations in ambient chorus noise may impair mating call perception.     

Displaying in the dark: light-dependent alternative mating tactics in the Alpine newt

Environment plays a major role for determining the kind of courtship behaviours or alternative mating tactics employed, but the effect of physical variables on fitness has received little attention. The Alpine newt courts during both day and night times and exhibits a complex suite of behaviours involving olfactory, visual and tactile cues. Displaying in both dark and light conditions may increase the number of mating opportunities and alleviate predation risk, but the frequency and efficacy of the various tactics deployed may vary across light conditions, leading males to vary their use of these tactics across different light regimes. To test this hypothesis, we video-recorded sexual encounters at two light intensities in a controlled experimental design. When courting in the dark, males used comparatively more olfactory rather than visual displays. They also relied more on positive feedback from the female before releasing a spermatophore for her to pick up. The particular mix of tactics used under each light condition is likely to be adaptive because in the dark (1) visual communication is hampered, making olfactory displays possibly more effective and (2) males depositing spermatophores are more likely to lose fertilizations to competitors. Mating in light and dark conditions has similar reproductive payoffs, which shows that displaying in the dark is not detrimental and may even be advantageous if predation risk is reduced at night. These results confirm the importance of taking into account physical variables to understand the evolution of sexual communication in animals.     

Implications of genetics and current protected areas for conservation of 5 endangered primates in China

Most of China's 24–28 primate species are threatened with extinction. Habitat reduction and fragmentation are perhaps the greatest threats. We used published data from a conservation genetics study of 5 endangered primates in China (Rhinopithecus roxellana, R. bieti, R. brelichi, Trachypithecus francoisi, and T. leucocephalus); distribution data on these species; and the distribution, area, and location of protected areas to inform conservation strategies for these primates. All 5 species were separated into subpopulations with unique genetic components. Gene flow appeared to be strongly impeded by agricultural land, meadows used for grazing, highways, and humans dwellings. Most species declined severely or diverged concurrently as human population and crop land cover increased. Nature reserves were not evenly distributed across subpopulations with unique genetic backgrounds. Certain small subpopulations were severely fragmented and had higher extinction risk than others. Primate mobility is limited and their genetic structure is strong and susceptible to substantial loss of diversity due to local extinction. Thus, to maximize preservation of genetic diversity in all these primate species, our results suggest protection is required for all sub‐populations. Key priorities for their conservation include maintaining R. roxellana in Shennongjia national reserve, subpopulations S4 and S5 of R. bieti and of R. brelichi in Fanjingshan national reserve, subpopulation CGX of T. francoisi in central Guangxi Province, and all 3 T. leucocephalus sub‐populations in central Guangxi Province.     

Speaking across boundaries to explore the potential for interdisciplinarity in ecosystem services knowledge production

Conservation is likely to be most successful if it draws on knowledge from across the natural and social sciences. The ecosystem services concept has been called a boundary object in that it facilitates development of such interdisciplinary knowledge because it offers a common platform for researchers, policy makers, and practitioners. However, a question that remains is to what extent the interdisciplinary knowledge needed is provided by disciplinary diversity within the field. We asked where is knowledge on ecosystem services produced, how interdisciplinary is this knowledge, and which disciplines facilitate the greatest disciplinary integration? We defined interdisciplinarity as the extent to which published research draws on knowledge that crosses disciplinary borders and used citations as a quantitative indicator of communication among disciplines, based on journal classification. We used disciplinary diversity, richness, and heterocitation as measures of interdisciplinarity and betweenness centrality as a measure of disciplinary integration. Our data set contained 22,153 publications on ecosystem services, published from 1983 to 2018. We found that ecosystem services research matured; average yearly output growth was 33.8%, more than the 8–9% growth in scientific output across all fields. Over time, the network clustering coefficient, measuring connectedness of individual disciplines, rose from 0.388 to 0.727, suggesting increased density in the network of citations. Researchers in the field published more articles (3566 in 2018 alone) across more disciplines (77 unique disciplines in 2018). However, this growth was not mirrored by an increase in the diversity (stable at 0.7–0.9) or richness (averaging 0.35 unique disciplines per citation) of citation patterns. Heterocitation scores, or out-of-group citations, for arts, humanities, social sciences, and law ranged from 56% to 64%, which was lower than we expected, although this may serve to protect the integrity of social science disciplines and attract broader engagement from within. Ultimately, a small number of productive disciplines are central to supporting disciplinary integration. However, opportunities exist for conservation practice to draw on a broader field of research, to realize the potential that the diverse body of knowledge of interdisciplinary work offers.     

Male response to an aggressive visual signal, the wing wave display, in swamp sparrows

Signaling often involves complex suites of behaviors that incorporate different sensory modalities. Whatever modality is used to establish that a signal functions in communication researchers must demonstrate that receivers respond to it. The territory defense response of male swamp sparrows involves a variety of behaviors that includes both vocal and visual displays. One of these, the “wing wave” display, is a distinctive movement that predicts physical attack. Here, we use robotic taxidermic mounts paired with song to test the hypothesis that wing waving is a signal and, specifically, that male receivers respond to wing waving as a signal of aggressive intent. As predicted, subjects responded more aggressively to the mount during wing waving trials than during stationary trials. A second experiment demonstrated that this effect cannot be attributed simply to increased attention to movement. Less expectedly, subjects did not alter their own display behavior in response to wing waving as compared to a static mount. We conclude that the wing wave display in the context of singing is a signal that functions in male–male aggressive communication. Questions remain, including whether wing waving functions as a signal in the absence of singing and whether wing waving and song are redundant signals or communicate different information.