Anthropogenic Impacts as a Driver of Sensory Organ Morphology

Simple Summary

The process of receiving and responding to information, such as smells revealing the location of food or vocal calls revealing the location of a potential mate, is essential to survival for all animals. There are three key steps: a signal is produced (e.g., a male cricket chirps); the signal is detected by the sensory organs of the animal who receives the information; and the behaviour of the receiver may change as a result (e.g., the female cricket moves towards the song). The second step requires the shape and sensitivity of the receiver’s sensory organs—e.g., eyes, ears, antennae—to enable the signal to be perceived amongst all other information, or background noise, in the environment. As humans alter the environment by introducing pollutants such as noises that drown out the cricket’s chirp or bright lights at night that make it difficult for a sea turtle to see the moon to navigate towards it, the shape and sensitivity of animals’ sensory organs may need to change over generations so they can still distinguish the relevant information from the background noise. This article reviews the evidence for these changes and explores the potential impacts on animal communication and the survival implications for impacted populations.

Abstract

All animals require the ability to use visual, auditory, tactile, and olfactory information to survive through activities including locating and identifying conspecifics including potential mates, locating food or shelter, or noticing an approaching predator. Detecting such information invariably requires sensory organs. The morphology of sensory organs evolves under natural selection to optimise the ability to detect salient cues and signals against the background noise in the natural environment. The rapidly proliferating anthropogenic impacts on almost all natural environments include light, noise, and chemical pollution, which can interfere with an animal’s ability to detect visual, acoustic or seismic, and olfactory information, respectively. Many studies examine the resulting changes in the characteristics of signals or the behavioural responses to them in affected natural populations, but very few examine the resulting changes in the sensory organs required to detect the signals; those that do all find evidence of morphological changes. Here, I review the current knowledge on the impact of anthropogenic pollution on sensory organ morphology in wild and captive populations, highlighting knowledge gaps and future directions for addressing them. This is especially important in the context of the growing recognition of the cruciality of sensory ecology in the design of effective threatened species conservation programs and invasive species management strategies.

1. Introduction

All organisms require the ability to decode their extrinsic environment. This can range from a bacterium responding to chemical or mechanical signals upon contact with a surface through to an animal simultaneously processing visual, auditory, tactile, and olfactory information to locate and identify conspecifics including potential reproductive mates, locate food or shelter, or notice an approaching predator and quickly identify an appropriate refuge or escape route. Detecting such information invariably requires sensory systems, whether rudimentary or complex, the morphology of which has considerable diversity in animals.

Akin to any other genetically encoded trait with biological fitness implications, the morphology and function of sensory organs evolve under natural selection, a concept that was recognised as early as Charles Darwin [1]: “As the male has to search for the female, he requires for this purpose organs of sense and locomotion, but if these organs are necessary for the other purposes of life, as is generally the case, they will have been developed through natural selection”. Specifically, the morphology of sensory organs should be optimised to efficiently detect salient information against the irrelevant information, or “background noise”, in the organism’s environment [2]. Therefore, these selection pressures result from a combination of the nature of the information to be detected and the complexity of the sensory landscape against which they must be detected. Salient information comes in the form of cues and signals: cues passively provide a receiver with information to guide action despite having not evolved for this purpose, whereas signals are acts or structures that have evolved to influence the behaviour of the receiver and to which the receiver has evolved a behavioural response [3].

While most species have had a relatively stable habitat to which to adapt over centuries, humans have changed almost every natural environment on Earth in an unprecedentedly short timeframe [4]. This increasing natural habitat fragmentation, destruction, urbanisation, and pollution has brought considerable changes to the sensory landscape with the introduction and proliferation of artificial light at night, anthropogenic noise, and chemical pollution vastly increasing the background complexity against which animals must detect visual, auditory/seismic, and olfactory information, respectively. Put simply, the signal-to-noise ratio has decreased [5,6]. This detection can be further complicated for a given species when the pollution overlaps with the spectral characteristics, such as the sound frequency range, or the timing of the signal or cue on which they rely, as this salient information becomes masked [7]. If sustained, anthropogenic pollutants can act as strong selection pressures on populations in affected environments, favouring shifts in signals to minimise spectral and/or temporal overlap with pollutants in that sensory modality or favouring sensory system adaptations that increase an individual’s sensitivity to cues and signals in this more complex sensory environment [5].

Similarly, many animal populations are maintained over generations in captive environments. Here, the complexity of the sensory landscape tends to be simplified compared to that in natural environments, typically being characterised by abundant resources and a scarcity or complete absence of natural predators. This may result in selection for adaptations that optimise sensory organs to the signal detection requirements of this relatively simplified environment, with variation in environmental conditions known to impose selection pressures on sensory systems [8]. This is especially poignant for sensory systems given their energetically expensive nature due to the neural architecture required [9]: resource investment in unnecessarily sensitive sensory organs detracts from, rather than improves, biological fitness.

Studies on species responses to urbanisation and pollution often examine compositional and temporal changes to signals, such as plumage colour or acoustics, between urban and natural habitat populations. Others examine behavioural responses with a range of mechanisms ranging from plasticity through to adaptation by selection hypothesised as underlying them. This knowledge can inform strategies to mitigate anthropogenic impacts on animal communication, potentially making such environments refuges for some species. Despite the close evolutionary relationship between signals, the behaviours they inform, and the sensory systems that must be possessed to detect those signals [2,3] (Figure 1), the sensory organs that must receive these signals are typically overlooked in these same contexts [10]. Furthermore, of the three major forms of pollution—light, noise, and chemical—affecting most natural environments, studies that explicitly examine phenotypic change regarding sensory organ morphology are restricted to the context of light pollution (

Table 1. Summary of documented changes to sensory organ morphology resulting from adaptation to anthropogenically created or anthropogenically polluted environments.

Environment	Context	Species	Sense Affected	Morphological Changes Observed	References
Artificial/captive	Conservation breeding	Lord Howe Island stick insect (Dryococelus australis)	Vision	Smaller compound eye	Freelance, Magrath, Elgar and Wong [11]
			Olfaction	Lower density of olfactory antennal sensilla
	Aquaculture	Steelhead salmon (Oncorhynchus mykiss)	Mechanoreception, hearing	Fewer lateral line organs	Brown, et al. [16]
		Masu salmon (O. mykiss)	Mechanoreception, hearing	Fewer lateral line organs	Nakae, et al. [17]
Natural	Artificial light at night	Heart and dart moth (Agrotis exclamationis)	Vision	Smaller compound eye (females)	Keinath, et al. [18]
		Carolina wren (Thryothorus ludovicianus)	Vision	Smaller eye size	Jones, et al. [19]
		Northern cardinal (Cardinalis cardinalis)	Vision	Smaller eye size	Jones, Llamas and Phillips [19]

). This is problematic not only in terms of an incomplete understanding of how anthropogenic change is altering the sensory ecology of a species but also as sensory ecology is increasingly recognised as being crucial in the design of effective threatened species conservation programs [11,12,13,14,15] and invasive species management strategies [12,14].

Here, I identify four key anthropogenic impacts that may be associated with changes to sensory organ morphology in impacted populations: anthropogenically created/captive environments, light pollution of the natural environment, noise pollution of the natural environment, and chemical pollution of the natural environment. For each of these contexts, I summarise the findings of the few studies that do explore changes to sensory organ morphology, or I explain whether one would expect to see such changes. Following this exploration, I identify five priority areas on which future studies could focus to efficiently and effectively fill the key knowledge gaps with maximum relevance to conservation.

2. Anthropogenically Generated Sensory Environments: Captivity

Many animal populations are maintained over generations in artificial or captive environments. Such environments are typically benign with abundant resources and no predators, thus selecting for survival in an environment that may have little resemblance to the natural habitat of the species [20,21]. Indeed, adaptations to captivity are frequently maladaptive to natural environments [22,23], with potential survival implications for captive-bred individuals released into the wild.

The complexity of the sensory landscape in captive environments tends to differ from that in the natural environment in many ways: the ready availability of food and shelter reduces or eliminates the need to use visual, olfactory, or tactile cues to identify and locate resources; the limited maximum distance between individuals reduces the need to rely on pheromones to locate a potential mate (however, such information may still be used to assess the suitability of any potential mate once located); and the absence of predators negates the need to have sufficient sensitivity to detect their approach in time to shelter and/or escape [11,24]. If sustained over generations, this relative simplification of the sensory landscape—both in terms of background complexity and in the volume of salient cues and signals to detect—has potential to drive sensory system adaptation via selection. In this context, selection may favour individuals with reduced sensitivity and/or complexity of sensory systems such that they are optimised to the signal-detection requirements of the simplified environment.

Aquaculture is a technique commonly used to maintain populations of fish for commercial harvesting, with the aim of preserving natural fish populations by reducing the need for commercially fishing them. Hatcheries can also provide fish for release into the wild to bolster diminishing natural populations. Investigations of the morphology of lateral line organs, which are found in fish and detect movement, vibration, and pressure, and therefore have a role in predator detection and movement control, revealed that hatchery-bred steelhead salmon (Oncorhynchus mykiss) (Salmoniformes: Salmonidae) have fewer lateral line organ neuromasts (and smaller brains) than wild-origin steelhead [16] (Table 1). Interestingly, the otoliths (a structure of the inner ear) were also more heavily crystalised in the hatchery-bred steelheads, likely indicating a relative reduction in auditory function. More recently, captive-bred masu salmon (O. masou) populations have also been found to exhibit a decrease in the number of lateral line organ neuromasts over generations [17] (Table 1), with the authors proposing that this likely reduction in mechanoreceptive sensitivity is a potential explanation for the low survival rates of captive-bred masu released into the wild to supplement natural populations [25].

Captive breeding programs are an increasingly common approach to threatened species conservation. Established with individuals from wild populations of a threatened species, conservation breeding populations act as insurance against extinction and provide a source of individuals that can be used for species reintroduction or to reinforce natural populations following mitigation of extinction drivers [26]. Changes to sensory organ morphology have been documented recently in this context. The critically endangered Lord Howe Island stick insect Dryococelus australis (Phasmatodea: Phasmatidae) was rediscovered on Balls Pyramid (Australia) after almost a century of supposed extinction following the introduction of black rats (Rattus rattus) (Rodentia: Muridae) onto Lord Howe Island following a shipwreck in the early 20th century [27]. Individuals from Balls Pyramid were used to establish a captive breeding population that has now been bred for over 14 generations. Comparison of sensory organ morphology between captive-bred individuals and preserved museum specimens from the historic wild population on Lord Howe Island and the founding population on Balls Pyramid has been undertaken, revealing relatively smaller compound eyes and a lower abundance of olfactory sensilla (sensory hairs) on the antennae of individuals in the captive population [11] (Table 1). These changes are consistent with predictions based on less background noise in the sensory environment and reduced reliance on the use of visual and olfactory cues to locate food and potential mates. In insects, compound eye size is related to visual acuity and sensitivity to light [28], and antennal olfactory sensilla density/abundance is positively correlated with the physiological and behavioural response to odours [29,30], suggesting the changes observed confer reduced visual and olfactory sensitivity. Therefore, if used for threatened species reintroduction, captive-bred insects may be less efficient at locating food plants and potential mates, which would likely have negative implications for their biological fitness in the natural environment [11].

3. Anthropogenic Disruption to the Sensory Environment

3.1. Light Pollution

The penetration of artificial light into once dark nighttime natural environments is widespread across the planet and continues to increase globally [31], with the nighttime sky being considered astronomically polluted (unable to see stars in the sky with the naked eye) for approximately 80% of the world’s human population [32]. Alarmingly, the greatest increases in exposure to artificial light at night (ALAN) are seen in terrestrial ecosystems that are often fragmented biodiversity hotspots of considerable conservation importance [33].

Impacts on aspects of communication and sensory-related behaviours have been documented in a variety of species including impaired visual navigation of sea turtle hatchlings [34], altered onset of singing behaviour in several species of songbirds [35,36,37], altered calling behaviour and call characteristics in frogs [38,39], and reduced attraction of male glow-worms to females [40,41]. Given how fundamental light, and particularly a stable light cycle, is to life in almost every habitat on the planet, ALAN should be considered a potent driver of evolutionary change [42].

Persistent changes to the levels of light in the environment a population inhabits are known to drive evolutionary changes in the sensory organs that receive this information: eyes. For example, cave-dwelling populations of the Mexican cave fish (Astyanax mexicanus) (Characiformes: Characidae) have evolved non-functional eyes while surface-dwelling populations retain their eyes [43], and the troglomorphic traits of reduced or absent eyes, and often elaborated antennae, are observed in cave-dwelling arthropods including crickets [44], springtails [45], and dytiscid beetles [46]. These adaptations reflect greatly increased reliance on non-visual stimuli in the complete absence of light with which to see. Eye morphology adaptations are also seen in non-extreme environments: dim-light-active insects across many taxonomic orders have relatively larger compound eyes compared to diurnal/day-active species [47], and dim-light-active birds have relatively longer eyes with greater corneal diameters compared to birds active mostly during the day [48]. Both adaptations reflect the need for more sensitive eyes to receive visual cues and signals in the presence of lower levels of light.

In the presence of persistent ALAN, affected environments become more like daytime environments with higher levels of light compared to the natural nighttime, meaning less visual sensitivity is required for night-active animals to use visual information in that habitat. Consequently, a reduction in eye size could be predicted. While very few studies have explored this, all the contexts in which it has been investigated have confirmed the predicted pattern. Examination of the compound eye size of the moth Agrotis exclamationis (Lepidoptera: Noctuidae) using specimens representing 137 years of collection revealed a negative relationship between compound eye size in females and the intensity of ALAN to which populations were exposed [18]. More recently, eye size was measured in two non-migratory species of songbird, and populations living in urban habitats characterised by a higher intensity of ALAN demonstrated a relatively smaller eye size [19]. While limited to only three species, these results demonstrate the potential for ALAN to act as a potent evolutionary driver of eye morphology and emphasise the need for this phenomenon to be explored with greater taxonomic breadth to better understand the potential impact on animal communities and the ecosystems of which they are a part.

3.2. Noise Pollution

A multitude of human activities generate noise, which can penetrate the surrounding environment, with rapidly increasing taxonomically diverse evidence of negative impacts on wildlife [49]. In addition to sound waves travelling through the air as auditory information, as sounds are mechanical waves they can transmit vibrations through substrates such as vegetation and water, thus also impacting terrestrial and aquatic organisms that use seismic communication. The communication impacts of noise pollution are largely driven by a decrease in the signal-to-noise ratio, with pollution masking salient signals and cues in those same modalities [7,50]. This is most pronounced when noise pollution occurs in the same spectral range as the signal. In addition to the masking of signals, noise pollution can also provide misleading input which the receiver mistakes for salient information, thus distracting the receiver and causing them to miss a signal or cue when it is broadcast [7,50,51].

The negative impacts of road and air traffic noise on acoustic communication are well documented in a range of taxa. These include temporal and/or volume shifts in singing for songbirds to reduce masking of calls [15,52,53,54], impaired mate searching [55] and reduced male call duration [56] in Orthopteran insects, and impaired female orientation to male calls as well as changes to the temporal and spectral characteristics of male mating calls in anuran amphibians [57,58,59]. Impairment to acoustic communication has been linked to negative fitness consequences driven by factors including reduced predator detection, increased stress, increased energy expenditure on generating effective calls, and decreased reproductive success [15,51,58,60,61]. If prolonged, such impacts may compromise the persistence of impacted populations.

The impacts of noise pollution on seismic communication are also characterised in both terrestrial and aquatic environments. In wolf spiders, white noise that overlaps with the frequency (Hz) of the male vibratory courtship displays reduces the female response, initiation of male courtship displays, and overall mating success [62]. Web-building spiders demonstrate changes in prey detection sensitivity mediated by both the intensity of anthropogenic noise and the presence of artificial substrates to which webs are attached (with such substrates hypothesised to be more robust to vibrational disturbance than natural substrates such as twigs) [63]. Traffic noise masks the foot-drumming signals of the endangered Stephen’s kangaroo rat Dipodomys stephensi (Rodentia: Heteromyidae), and its onset can even deceptively induce exposed individuals to perform foot-drumming behaviour [64]. Seismic disruption of stridulation during reproduction of the margined burying beetle Nicrophorus marginatus (Coleoptera: Silphidae) results in smaller brood sizes, likely due to disrupted seismic communication and/or inaccurate assessment of brood resources [65]. Male common midwife toads Alytes obstetricans (Anura: Alytidae) exposed to seismic noise exhibit a reduced call rate, with females anurans tending to prefer males with higher call rates [66]. With regard to aquatic environments, vibrations in the frequency range of substrate disturbances caused by anthropogenic activity (e.g., drilling, dredging, tunnel boring) trigger startle responses and the raising of the shell off the substrate (to reduce vibration) in the hermit crab Pagurus bernhardus (Decapoda: Paguridae) [67].

While no evolutionary/adaptive comparisons of sensory organ morphology between pristine and impacted populations have been performed to date, any changes observed would likely be to the effect of increasing sensitivity in hearing and/or mechanoreception as a way of improving the ability to detect more heavily masked signals in polluted environments. However, the range of contexts in which temporal or spectral/compositional shifts in acoustic and/or seismic communication occur in response to noise pollution is wide [15,61,68], which suggests that these strategies that serve to increase the signal-to-noise ratio are generally effective and efficient. Therefore, it is only in contexts in which these temporal or spectral shifts in signalling, or spatial relocation away from the source of anthropogenic disruption, are not possible/feasible that adaptive morphological changes to the sensory organs of the receiver are likely to occur.

3.3. Chemical Pollution

Many animals rely on olfactory information to drive behaviours essential to their survival. This can include information about the location of resources or entities such as potential mates (via pheromones), the presence of a potential predator or prey item, and the location and suitability of a food plant. Olfactory information is typically in the form of airborne volatile chemicals in the cases of terrestrial/avian animals and dissolved waterborne compounds in the case of aquatic animals.

There are many ways in which chemical pollution can impact upon animal communication and behaviour depending on their habitat type and whether the pollution is direct or indirect. For example, aquatic pharmaceutical contamination is associated with altered mating [69,70], anxiety-related [71], predator-avoidance [72], and exploratory [72] behaviours in fish. Flies living in environments with higher levels of air pollution demonstrate a higher amount of particulate matter on the sensilla of their antennae, which is associated with an impaired ability to detect food- and mate-related odours [73].

Indirect pollution can also impair olfactory communication. For example, ocean acidification conditions mediated by elevated levels of carbon dioxide (CO₂) are associated with the disruption of olfactory-guided behaviours, including prey detection [74], homing and determination of habitat suitability [75], and with impaired predator avoidance [76]; it is unknown whether these changes are related to the reduced function of the olfactory epithelium or due to changes in the neural processing of olfactory information. More recently, an altered behavioural response to an olfactory cue in salmon living in elevated-CO₂ seawater was linked to altered neural signalling in the olfactory bulb of the brain, which was associated with disrupted gene expression in the same brain region [77].

Despite these wide-ranging documented impacts, no studies to date have explored the impacts of transgenerational exposure on the morphology of the sensory organs required to detect olfactory information. If a population is not able to adapt either in terms of the characteristics of the olfactory signal to increase the signal-to-noise ratio or in terms of the behavioural response to the signal/cue in the presence of the pollution, then morphological changes to the olfactory organs may be expected. These would either increase sensitivity to enable sufficient detection of the signal against the background noise, or decrease complexity to reflect a persistent reduction in the ability of olfaction to provide information that contributes to biological fitness. For example, in the instance of elevated CO₂ in seawater, transgenerational studies reveal that offspring often possess enhanced resistance to the impacts of those CO₂ levels [78,79], thus mitigating its negative impact on the behavioural response to olfactory information; in this context, morphological changes to sensory organs would not be predicted. In the case of air pollution that deposits particulate matter on insect antennal sensilla and thus impairs olfaction [73], having a higher density of olfactory sensilla may increase the likelihood that odour molecules would still encounter sufficient olfactory pores on enough sensilla to provide salient information to the focal individual.

4. Future Directions

There are few studies that explore morphological changes to sensory organs in contexts of persistent environmental change in which communication behaviours are known to be disrupted. Furthermore, the contexts of studies that do address this are very limited (Table 1). As outlined above, those that do explore this show clear evidence that aligns with the theorised changes in these traits based on the nature of the anthropogenic change. The need for greater research in this area is evident, with the following knowledge gaps being of high priority:

4.1. Timeframe

Given the dearth of studies, the timeframe in which morphological changes to sensory organs will start to occur in these contexts is unclear [10]. While more generations must pass for evolutionary change via adaptation to occur, this still creates a particular risk for invertebrates who have relatively short lifespans. Additionally, this is further confounded by situations in which the production of a signal or cue also shifts due to the cause of environmental change, as that shift may mitigate any initial decrease in the signal-to-noise ratio, and, therefore, selection would not favour any change in sensory organ morphology.

From a practical perspective, understanding the timeframes underpinning the change can provide valuable insight into how long after environmental change begins adaptation will start to occur. This may inform planning for wildlife managers and conservationists to implement measures to attempt to mitigate disruption to the affected animal populations before phenotypic change starts to occur. For conservation breeding, it is considered desirable to breed the species in captivity for as few generations as possible to minimise potential adaptations [20], and efforts to reduce the opportunity for maladaptive phenotypic changes to sensory systems (or any morphological trait) in such an environment would further contribute to building more biologically fit captive populations for rewilding [11].

4.2. Functional Impact

In each of the examples of morphological adaptation of sensory systems to anthropogenically driven environmental change in Table 1, the functional impact of the altered morphology is unclear. For example, insect antennal sensilla density positively correlates with physiological and behavioural responses to odours [29,30,80]. However, no behavioural or physiological assay has been performed on individuals from the captive-bred Lord Howe Island stick insect population to assess the behavioural relevance of reduced sensilla density; interestingly, the sensitivity of hermit crabs to vibration (detected by their antennae in addition to other organs) has been found to be greater for crabs with shorter times in captivity [67]. Based off this established correlation between antennal sensilla density and behavioural/physiological responses to odours in insects, there is a possibility that captive-bred Lord Howe Island stick insects would be less efficient at locating food plants and potential mates in the wild. This would likely have negative implications for the body condition and reproductive output for individuals and, therefore, for the biological fitness of the rewilded population; further studies are required to confirm any functional impact in this context. Similarly, while the number of functional mechanosensory hair cells in a fish’s lateral line organs is positively associated with its ability to orient itself against constant water flow [81], behavioural changes to captive/hatchery bred salmon with fewer lateral line organs have not been assessed [16], but, if present, predicted behaviour changes would be reduced ability to orient themselves relative to water flow and potentially to detect waterborne vibrations. Akin to studies of the nature and quality of a signal informing a deeper understanding of how that system of signalling and receiving has evolved/is evolving, we must identify any behavioural impacts of morphological changes to the sensory organs required to receive those signals to gain a full understanding of the consequences for communication in animal populations adapting to environmental change.

4.3. Mechanism

Trait shifts in response to environmental disturbance can be driven by one or both of phenotypic plasticity and genetic change [82], with both being confirmed mechanisms for adaptive changes to sensory systems [10]. Furthermore, while rapid changes are frequently due to plasticity, some rapid phenotypic changes in natural populations can be a result of genetic change [83]. In each of the examples provided in Table 1, the mechanism of adaptation—phenotypic plasticity or genetic change—is unknown. Additionally, plastic changes can also precede and alter the rate and strength of genetic change for a given trait, with implications for the biological fitness costs of the environmental change a population is experiencing [82] and, therefore, for the persistence of that population. This is especially important in the context of conservation captive breeding programs for threatened species reintroduction, as adaptations to captivity are typically maladaptive to natural environments [22,23] and changes that result from phenotypic plasticity are typically easier to reverse than those that result from genetic adaptation. Complicating the issue further is that many threatened populations have low genetic diversity, meaning there may be insufficient variation for adaptation to occur [84]; the impact of this could be favourable or unfavourable: a lack of adaptive potential could indicate that phenotypic plasticity is the likely driver of sensory morphology change observed in such populations and, therefore, that sensory organ morphology changes may be easier to reverse. Conversely, a lack of adaptive potential could reflect an inability for genetically driven changes to sensory organ morphology over generations following the reduction of anthropogenic selection pressures for a given threatened population. Whether plasticity, genetic change, or both underpin the sensory organ morphology changes observed in captive populations to be used for species reintroduction is of relevance to developing strategies, such as enclosed predator-free nature reserves, to better mimic the sensory complexity of the natural environment in captivity and, thus, impart a similar selective pressure on sensory organ morphology.

4.4. Taxonomic Breadth

The confirmed presence (albeit in few species) in both vertebrates and invertebrates of changes to sensory organ morphology is indicative of the strength of anthropogenic impacts as potential evolutionary drivers. However, in each of the examples provided in Table 1, the studies are taxonomically restricted to insects, one species of fish, and two species of bird. This is especially problematic in the context of ALAN, as the ability to predict biological responses to ALAN is hampered by the diversity in photosensitivity across taxa [85]. Given the diversity in the morphology of olfactory and auditory organs across taxa– such as a mammal’s nose and ear compared to an insect’s antennae—the ability to extrapolate the impacts of a given environmental change on these organs is similarly limited. Addressing this deficiency requires sensory ecology studies across a wider range of taxa to expand their assessment beyond signal production or behavioural responses to also include the morphology and/or physiology of the sensory organs required to receive the signals.

4.5. Multimodality

While there are many examples of unimodal communication in the animal kingdom, multimodal communication is abundant wherein a given signal engages multiple sensory modalities simultaneously [86]. In the discussion provided in this review, the impacts of light, noise, and chemical pollution are considered unimodally, which may simplify that scenario beyond what realistically occurs [7]. For example, interference in one sensory modality can impact information processing in another modality; pollution in the different modalities often occurs simultaneously, such as in urban environments in which light and noise pollution often both occur, meaning there may be additive or multiplicative effects (e.g., the ability to use both visual and auditory cues to locate a resource may be reduced); a given pollutant may impact upon multiple sensory modalities (e.g., noise pollution can simultaneously impact upon acoustic and seismic communication), thus expanding the breadth of potential impairment in a given context. The ability of a focal species to use a combination of visual, acoustic, and/or chemical cues for orientation/navigation may mitigate the impact of light pollution on navigation if there is a behavioural shift to rely more heavily upon the acoustic or chemical cues than on the visual ones [5,10] (assuming noise and/or chemical pollution are not occurring). Indeed, sensory compensation is a common response to the presence of pollution in a sensory modality. For example, bats experiencing noise pollution masking the mating calls of potential prey frogs increase their use of echolocation to actively pinpoint the location of the frog rather than homing in on the frog’s own call [87], and the three-spined stickleback Gasterosteus aculeatus (Perciformes: Gasterosteidae) relies more heavily on olfactory than on visual cues for mate choice only when the water is turbid (using predominantly visual cues in clear water) [88]. In the context of CO₂-mediated impairment of the ability of reef predators to respond to prey-related odours, it was observed that greater movement by the impacted predators enabled the visual detection of prey [74], thus partially compensating for the impaired olfactory response. In all of these instances of behavioural adaptation when the availability of information in one was compromised, anthropogenic changes did not impact the “backup” modality; the presence of a form of pollution also impacting that secondary modality may limit the ability for additional behavioural adaptation and it is in these situations in which a behavioural adaptation is not efficient or effective that morphological changes to sensory organs may be favoured. Therefore, future studies should assess all forms of pollution/environmental disruption present in the context of focus, testing these pollutants both combined and in isolation to determine their specific contributions to any impairment for each sensory modality and, therefore, on the overall behavioural, morphological, and/or evolutionary impact(s) observed.

5. Conclusions

Communication is fundamental for all animal populations regardless of species but is increasingly being disrupted by anthropogenic changes to the environment. While many studies in these contexts focus on adaptive changes to the signals themselves or to the behaviours they have evolved to elicit, very few consider the morphology of the sensory organs the receiver of these signals must possess; those that do consider this are taxonomically and contextually narrow. With a close evolutionary relationship between signals, sensory organs, and the responses elicited by a cue or signal and with many forms of anthropogenic pollution shown to be potential drivers of selection, this oversight renders a large gap in our knowledge of the interplay between environmental change and sensory ecology. In particular, there are substantial knowledge deficits regarding the timeframe over which changes to sensory organ morphology may occur, the functional impact of any such changes including potential implications for population fitness, the mechanism by which this happens (phenotypic plasticity, genetic adaptation, or both), the taxonomic breadth in which such impacts are seen in the context of a given anthropogenic impact, and the interplay between multimodality and the likelihood of behavioural adaptation vs. morphological change in response to a given anthropogenic impact in a given environment. Prioritising these future directions is crucial to effectively reducing the key knowledge gaps regarding the underlying mechanisms and functional impacts of morphological changes to sensory organs in wild and captive populations, including those of economic (e.g., aquaculture) and conservation (e.g., threatened or keystone species) importance. This is important not only for developing a full understanding of how anthropogenic change alters the sensory ecology of species but also for realising the full potential of sensory ecology in improving the design and efficacy of threatened species conservation programs and invasive species management strategies.