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Do any terrestrial herbivores use auditory crypsis for predator avoidance?

Do any terrestrial herbivores use auditory crypsis for predator avoidance?



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Some terrestrial predators "stalk" their prey: they sneak up on it slowly, maintaining a low profile, while keeping as close to silent as possible. This makes sense from an evolutionary perspective: silent predators catch more prey.

However, the prey near where I live are hopelessly noisy. Deer will freeze if they suspect the presence of a predator, then bolt when they see one for sure. Squirrels and other small mammals run around at top speed all the time - you can hear them dozens of feet away, rustling the dead leaves around. Hedgehogs just wander, making a similar noise. It seems like the only "stealth" option they have, as far as sound is concerned, is to remain still.

Are there any examples of terrestrial herbivores evolving to move more quietly in order to avoid predation? I'm not looking for a comprehensive list, but rather simply individual examples.


Does soundproofing count?

Most predators locate prey using visual or olfactory cues; the only predators I can think of that use auditory cues are nocturnal ones - owls and bats. Bats, of course, use echolocation, so even completely silent prey are still detectable. It has been suggested that the soft, fur-like body coverings of some owlet moths (Noctuidae) and tiger moths (within the Arctiinae) help hide them from echolocating predators by passively absorbing sound, although subsequent studies have suggested that they may instead be mimicking the acoustic signature of unpalatable prey.

(public domain image: source)

I have a suspicion this isn't what you meant by 'land-dwelling herbivore', but insects are people too…

Edit: just discovered this paper from May that provides evidence supporting the hypothesis that the twisted tails of luna moths (Actias luna) disrupt tracking by echolocating bats.

Image owned by Shawn Hanrahan, licensed under CC BY-SA 2.5


I think that there are too many examples of animals being deliberately quiet when grazing to count. I'll discuss specifically the exceptions you raise and how they are exceptional. Hopefully you'll see my point: A lot of grazers are quiet and cautious or failing that have other adaptive strategies for not being eaten.

Deer are incredibly quiet and cautious when grazing, and fast and agile once they decide it's not safe. Squirrels use trees as an defense - not many predators of theirs can even climb trees let alone keep up with a squirrel darting through them, (related question about bushy tails of squirrels being counter intuitive). And hedgehogs… well… how do you eat one without getting a mouthful of pain? On a bigger scale, here is a related video of a juvenile lion trying to attack a porcupine. Being unsubtle helps them.


Herbivore diet breadth mediates the cascading effects of carnivores in food webs

This study shows the far-reaching effects of herbivore dietary specialization on the ecological and evolutionary dynamics of carnivore–herbivore–plant interactions. First, we test the long-standing hypothesis that dietary specialization of insect herbivores mediates the strength of bird predation on herbivores. Accounting for phylogenetic nonindependence of herbivores and plants, we show for the first time (to our knowledge) that dietary specialization of herbivore species is associated with reduced bird predation across an herbivore phylogeny, and that dietary specialization of herbivores increases the antipredator effects of camouflage and aposematism. Second, this study develops and finds support for the novel hypothesis that the proportion of dietary specialist species in a plant’s herbivore community predicts the degree of antiherbivore protection birds provide to plants.


Introduction

Ecological and evolutionary outcomes of species interactions can only be fully understood after considering the multi-trophic setting in which species are embedded. For example, phytophagous insects in terrestrial ecosystems go through periodic outbreaks in North America and Europe, destroying millions of hectares of forest each year (McManus et al. 1992 Li et al. 2015 ). These outbreaks are often driven by both the loss of natural enemies (parasitoids, predators or pathogens), which would otherwise keep herbivore populations in check (Turchin et al. 1999 ), as well as by changes in host plant resistance and nutritional quality (Turchin et al. 1991 ). Similarly, highly damaging algal blooms in aquatic systems worldwide are driven both by increases in algal resources from eutrophication, as well as by natural enemy suppression of herbivorous zooplankton that otherwise would regulate algal density (Carpenter et al. 1985 Micheli 1999 ). But critically, the effects of these multiple drivers can also interact, resulting in emergent properties across multiple trophic levels that cannot be predicted from separately analysing each component pairwise interaction for example, tree defences can alter predation or parasitism of herbivores by reducing herbivore performance (Elderd et al. 2013 ), whereas nutrient-driven algal blooms can lengthen food chains that feedback to increase predator top-down control (Oksanen et al. 1981 Power 1990 ). Accordingly, these and numerous other so-called tri-trophic interactions (TTIs) determine the population biology and evolutionary dynamics of species at all trophic levels and drive fundamental aspects of community structure and ecosystem dynamics. By improving our understanding of ecological and evolutionary processes, tri-trophic research provides opportunities to establish linkages across levels of biological organisation.

Despite its unifying potential, research on TTIs has been fragmented, following two distinct paths. On the one hand, researchers have adopted a ‘species interactions perspective’, focusing on the evolutionary ecology and population biology of simple food chains of interacting species consisting of herbivore and natural enemy species or guilds associated with one or a few plant species (e.g. Price et al. 1980 Mooney & Singer 2012 ). Concurrently, a separate ‘ecosystem perspective’ on TTIs has focused on the bottom-up (resource) and top-down (consumer) controls over the distribution of biomass across trophic levels and other ecosystem-level properties (e.g. Polis 1999 Borer et al. 2005 Hillebrand et al. 2007 ). Bridging these levels of organisation is not only a grand challenge but also a fundamental requirement for developing a full and predictive understanding of community and ecosystem functioning.

We argue that an expanded theory on TTIs can unify our understanding of biological processes across levels of organisation, from species interactions and evolution within simple food chains, to community structure and ecosystem function. Although tri-trophic research has been previously summarised within distinct subfields (see Box 1), no broad synthesis across all facets of research on TTIs has been offered. Here, we first review the history of research within the species interactions and ecosystem perspectives. Second, we point at gaps in tri-trophic research within each level of organisation and identify promising opportunities to bridge focal interactions and ecosystem processes, including the application of new technologies and data sources. A common challenge to all of biology (and science) is to link processes across scales and levels of organisation. We hereby argue that a tri-trophic framework is necessary to address such a challenge in ecology and evolutionary biology.

Box 1. Previously reviewed sub-fields of research on tri-trophic interactions

The study of TTIs reaches back more than four decades and has been synthesised by reviews focusing on two separate perspectives, one studying population dynamics and evolutionary ecology of species interactions in simple linear food chains and the other on ecosystem-level processes. A comprehensive synthesis across topics within each perspective or across perspectives has not yet been offered. Below, we provide representative examples of syntheses within sub-fields of each perspective.

  • Plant effects on herbivore development time influencing susceptibility to predation (i.e. ‘Slow-Growth, High-Mortality Hypothesis’ e.g. Williams 1999 ).
  • Dual effects of plants and natural enemies on herbivore behaviour and evolution (i.e. ‘Enemy Free Space Hypothesis’ and ‘Physiological Efficiency Hypothesis’ e.g. Singer & Stireman 2005 Mooney et al.2012 Vidal & Murphy 2018 ).
  • Plant indirect defences from traits attracting natural enemies that reduce herbivory (e.g. Kessler & Heil 2011 Turlings & Erb 2018 Pearse et al. in review ).
  • Trophic cascades involving natural enemy-induced changes in herbivore behaviour (Preisser et al.2005 ).
  • Indirect evolutionary effects of natural enemies on lower trophic levels, including natural enemy indirect effects on plant fitness (Romero & Koricheva 2011 ) and non-additive selection in tri-trophic systems (Estes et al.2013 Abdala-Roberts & Mooney 2015 ).
  • Elevational gradients in natural enemy effects and plant indirect defences (Moreira et al.2018b ).
  • Plant diversity effects on natural enemy abundance and diversity and its feedback on lower trophic levels (e.g. Letourneau et al.2011 Moreira et al.2016 ).
  • Ecosystem-level trophic cascades in aquatic or terrestrial systems involving vertebrate predators (e.g. Strong 1992 Pace et al.1999 Shurin et al.2002 Mooney et al.2010 Estes et al.2011 Dirzo et al.2014 Sydeman et al.2015 ).
  • Trophic cascades involving vertebrate and/or invertebrate natural enemies in terrestrial communities (e.g. Schmitz et al.2000 Halaj & Wise 2001 ).
  • Ecosystem consequences of trophic cascades involving predator effects on herbivore behaviour (e.g. Ripple & Beschta 2004 Schmitz et al.2004 ).
  • Effects of consumers and resources on biomass distribution across trophic levels (e.g. Borer et al.2006 Gruner et al.2008 ).

Linking the evolution and form of warning coloration in nature

Many animals are toxic or unpalatable and signal this to predators with warning signals (aposematism). Aposematic appearance has long been a classical system to study predator–prey interactions, communication and signalling, and animal behaviour and learning. The area has received considerable empirical and theoretical investigation. However, most research has centred on understanding the initial evolution of aposematism, despite the fact that these studies often tell us little about the form and diversity of real warning signals in nature. In contrast, less attention has been given to the mechanistic basis of aposematic markings that is, ‘what makes an effective warning signal?’, and the efficacy of warning signals has been neglected. Furthermore, unlike other areas of adaptive coloration research (such as camouflage and mate choice), studies of warning coloration have often been slow to address predator vision and psychology. Here, we review the current understanding of warning signal form, with an aim to comprehend the diversity of warning signals in nature. We present hypotheses and suggestions for future work regarding our current understanding of several inter-related questions covering the form of warning signals and their relationship with predator vision, learning, and links to broader issues in evolutionary ecology such as mate choice and speciation.

1. Introduction

Many animals are toxic, unpalatable, or otherwise unprofitable, and advertise this to predators with conspicuous and/or distinctive warning signals (aposematism [1,2]). Aposematic appearance has been a classical system to study evolution and adaptation for over 150 years, and has received considerable empirical and theoretical investigation. However, research has centred on understanding the initial evolution of aposematism within an originally cryptic population (for which there are a wide range of non-mutually exclusive explanations [1,2]), but these studies generally tell us little about the form and diversity of real warning signals. In contrast, less attention has been given to the mechanistic basis of aposematic markings that is, ‘what makes an effective warning signal?’. As Rowe & Skelhorn [3] argue, studies of animal communication have been dominated by issues of signal cost and reliability, and have largely overlooked psychological mechanisms, which can explain the specific make-up of the vast range of signals that exist [4]. Furthermore, unlike some other areas of adaptive coloration research (such as camouflage and mate choice), studies of warning coloration have been slow to explicitly consider the role of predator vision (and how it will often differ substantially from human vision).

Here, we review current understanding of warning signal form, with an aim to understand the diversity of warning signals in nature. We focus on the following inter-related key issues:

— What makes an effective warning signal in different habitats and contexts?

— Why are some warning signals apparently only moderately conspicuous?

— Why do some aposematic species have intraspecific variation and polymorphism?

— How do other selection pressures (e.g. camouflage, mate choice) influence warning signal form and evolution?

2. What makes an effective warning signal?

Signals can be thought of as having a strategic aspect (the information content or ‘message’) and an efficacy aspect (the form or evolutionary ‘design’ of the signal) [4]. Signal efficacy relates to the way that a signal is structured in order to effectively influence the response of the receiver under different environmental conditions and constraints. For warning signals to be effective, they need to promote initial avoidance and/or avoidance learning in predators and strategic and efficacy aspects are important in this. Here, we consider what makes an effective warning signal in terms of efficacy.

(a) Conspicuousness and contrast

Conspicuousness has long been considered a key aspect of aposematism, and can be both a function of internal contrast of the markings within the body coloration, and contrast of the animal's coloration with the background [5,6]. Conspicuousness may also allow a predator to detect aposematic prey at a greater distance, perhaps reducing the likelihood of recognition errors [7].

Early experiments showed that non-cryptic colours and patterns promote both unlearnt avoidance and enhance avoidance learning in birds (see review by Ruxton et al. [2]), and work with domestic chicks (Gallus gallus) found that colour associations seem to be more readily learned than achromatic associations [8], whereas textural discrimination of small objects seems to be mediated primarily by luminance information [9]. Luminance contrast may primarily promote initial avoidance, owing to heightened detection, whereas specific colours (red and yellow) and colour contrast enhances avoidance learning. However, only limited work has tested this with properly controlled stimuli (in terms of predator vision). In addition, work with mantids as predators and milkweed bugs (Oncopeltus fasciatus) as prey indicate that achromatic contrast can be important in both the speed and persistence of aversion learning [6]. Most experiments have been carried out under laboratory conditions and we should also consider the visual environment. While achromatic signals may allow high contrast, colour signals may be particularly effective in heterogeneous or changeable environments because chromatic appearance may be relatively resistant to the effects of shadows and illumination changes, owing to visual processes such as colour constancy [10]. Under variable light conditions and heterogeneous environments luminance may become less reliable in avoidance learning and memory.

Given that many animals are thought to have red–green opponent processing mechanisms in their colour vision, this should make longwave (LW)-rich prey colours (e.g. reds and yellows) highly contrasting against many foliage backgrounds. Shortwave (SW)- and ultraviolet (UV)-rich colours are found in some aposematic species, but seemingly relatively infrequently. This may be because shortwave light is scattered more than longer wavelengths, making shadows appear ‘blue’ (to humans), so that such colours blend in rather than stand out. Although few controlled experiments exist, one study with great tits (Parus major) found no evidence that the presence of UV wavelengths would enhance either initial or learnt avoidance of other colours [11], and subsequent field experiments reveal increased predation in moths with UV reflectance compared with moths lacking UV [12]. Separating the role of specific colour types as opposed to contrast is challenging and most experiments looking at contrast have used categories of colour, such as green or brown (low contrast) or red/yellow (high contrast) against green/brown backgrounds. However, these are not testing contrast alone, but rather classes of colour, and work shows that birds group objects into different colour categories (such as ‘oranges’ and ‘blues’ to humans [13]). This has implications for the way that predators may categorize groups of aposematic prey based on appearance, and indicates that more than just visual contrast/distinctiveness may affect predator avoidance decisions.

Finally, few experiments have successfully manipulated conspicuousness without altering colour [14], and, in general, findings about prey generalization have been contradictory. This may be because stimuli in learning and memory experiments have rarely been designed with respect to predator vision, making it hard to know how different the appearance of prey types presented are to the relevant non-human predators. Experiments are needed holding colour constant but manipulating contrast. There is good evidence showing that contrast of the overall prey coloration with the background is important in aposematism (reviewed by Ruxton et al. [2]), and some recent evidence in studies with chicks suggest that contrast with the background is more important than contrast within the prey [15]. However, most experiments investigating internal contrast simply produce prey with and without patterns (e.g. uniform or striped) and are perhaps better thought of as a test as to whether pattern itself is important or not. A key design that has rarely been implemented is where the pattern is the same but the level of contrast varies in steps that are tightly quantified with respect to predator vision.

(b) Pattern

Relatively little work has been conducted into whether some types of pattern are better than others at enhancing warning signals. Many warningly coloured prey have markings comprising repeated pattern elements. Such arrangements in signal structure may increase redundancy in the signal but improve the likelihood that the strategic component will be detected by the receiver. In addition, repeated elements may be rare in many natural environments, thus increasing conspicuousness of the prey animal. Simple pattern components (such as stripes and spots) may facilitate detection and also speed up avoidance learning if they are easier to memorize. It would be interesting to test initial avoidance and learning when presenting predators with simple and complex pattern types.

Aronsson & Gamberale-Stille [16] performed experiments with domestic chicks to test the roles of colour and pattern (simple stripes or spots) in avoidance learning and generalization. They found that chicks attended more to colour than pattern, in that during generalization trials chicks would generalize from the stimulus they had learnt to avoid to a new one based on colour similarity, but not for pattern similarity. In other systems, patterns may make effective aposematic signals. Work with Plasticine models of venomous snakes indicates that although their characteristic zig-zag markings do not appear especially conspicuous, they are distinctive enough to promote avoidance behaviour by predators [17,18]. This work has compared different pattern arrangements, such as zig-zags, stripes and nominally disruptive camouflage. However, the experimental stimuli have not yet been related to predator vision or the composition of the background. Studies with dragonflies as predators show that they avoid potential prey with wasp-like black and yellow stripes more than either uniform black or uniform yellow, indicating that pattern is important [19]. However, this does not reveal whether it is the contrast of black and yellow, or the stripes themselves that is most important. In other work with chicks, yellow coloration increased avoidance in inexperienced chicks, but there was no difference between yellow prey with or without wasp-like stripes [20]. However, green prey were avoided more when presented with stripes than without, indicating that striped patterns can increase avoidance when coupled with colours not normally associated with aposematism. In addition, stripes but not colour seemed most important in increasing the speed of avoidance learning, possibly if stripes were more memorable [20]. Therefore, different components of pattern and colour could enhance aspects of initial and learnt avoidance and may also be context-dependent.

One aspect of marking arrangement that has been predicted to influence warning signal efficacy is pattern symmetry, which may enable animals to recognize objects from different positions and orientations. Aviary studies with chicks have shown that birds learn to avoid unpalatable prey more quickly when the prey had symmetrical as opposed to asymmetrically sized markings [21]. Furthermore, chicks' unlearned avoidance of palatable artificial prey was stronger when the prey had markings symmetrical for size, shape and colour [22]. However, the experiments presented prey simultaneously in pairs, whereas most prey encounters in nature will be sequential, and predators will not be able to directly compare and choose between two or more prey individuals. Instead, a predator must decide whether to attack a prey item at all or leave unrewarded. Recent field studies with artificial prey with a pair of markings that were either symmetric or asymmetric for size, shape and placement on the body, found no survival advantage of symmetric over asymmetric markings [23]. The majority of animal markings are symmetric, but perhaps the most parsimonious explanation is that this reflects genetic and developmental constraints rather than an underlying signalling function.

(c) Distinctiveness

As discussed above, high conspicuousness in aposematic prey may confer advantages in terms of exploiting predator sensory and cognitive systems. However, there is an alternative or additional explanation: undefended organisms are generally inconspicuous, and thus if a defended organism adopts an appearance that enhances its distinctiveness to predators from undefended species, that appearance is likely to be conspicuous. This suggestion is not new but has recently been supported by experiments using artificial prey on a computer screen and either human volunteers [24] or artificial neural networks [25] as predators. Under this mechanism conspicuousness is only a commonly selected means of achieving distinctiveness, because it is a trait that undefended prey cannot afford to possess.

The unresolved question is how important selection for distinctiveness has been in shaping conspicuous aposematic signals. To us, its attraction is in its lack of assumptions: it could act even if predators show no special sensory or cognitive biases. It may be that selection for distinctiveness was important in the initial evolution of aposematism, and then once defended prey were conspicuous this drove selection in predators towards the biases that are now seen these biases may then have driven selection for even higher levels of conspicuousness. An unresolved question is whether natural aposematic signals are more conspicuous than they need to be to ensure distinctiveness from cryptic undefended organisms. For this reason, we feel that exploration of the consequences for prey survival of variation in the strength of conspicuousness (rather than simply comparison of conspicuous with cryptic signals) would be useful.

(d) Why are warning colours often red, yellow and black?

One of the most immediately apparent things when inspecting the range of warning signals in nature is just how common it is for them to be red, yellow and black (figure 1). Based on the above, we can propose several (often related) hypotheses about why such colours dominate:

— They provide high contrast against the background (e.g. red/yellow against green foliage), which promotes detection.

— They are resistant to shadows (which are rich in blue-UV), and to changes in illumination (e.g. black should not change during day, whereas white could become ‘pink’ at sunset and sunrise). Therefore, they provide a reliable signal under varied habitats and light conditions.

— Yellow/red and black has both high chromatic and luminance contrast.

— Such colours may allow distance-dependent camouflage if yellow/red and black ‘blend’ to an average colour that matches the background at a distance when predator vision is no longer sufficient to discriminate individual marking components.

— Such colours are distinctive from profitable species.

Figure 1. Examples of the diversity of warning signals that exist in two groups, poison frogs and lepidopteran larvae. (a) Oophaga histrionica, (b) Phyllobates terribilis, (c) Ranitomeya fulgurita, (d) Ranitomeya bombetes, (e–g) unknown species. (a,b) Reproduced with permission from © Adolfo Amezquita (c,d) © Fernando Vargas (eg) © Martin Stevens.

These different hypotheses are not mutually exclusive, but it is important to test each of them. One approach is to model changes in colour and luminance contrast over the course of a day and under different light environments in terms of predator vision. We would predict that LW colours should fluctuate less than SW/UV colours as ambient light changes. This approach has been used in a different context to investigate differences between human and avian colour vision [26]. In addition, work should record and quantify more extensively the range of natural backgrounds against which prey are found, and to test in terms of predator vision how much the distribution of warning signals overlaps with background objects. A similar approach could be used to compare warning coloured prey to palatable species. In terms of distance-dependent effects on aposematism and camouflage, work could use models of predator vision, coupled with information on predator acuity (where available), to test the level of conspicuousness and camouflage at different distances of both the individual pattern components, and the average ‘colour’ of all components combined (as [27]).

3. Moderately conspicuous aposematic signals

Several recent theoretical papers suggest mechanisms that can select for aposematic signals to be less-than-maximally conspicuous (‘weak’ warning signals [28–30] figure 2). These models essentially assume that the benefit of a conspicuous aposematic signal is that it reduces the probability that detection by at least some potential predators leads to death of the prey. It is further assumed that this benefit increases with increasing conspicuousness, but that this increase decelerates and eventually saturates. This seems highly plausible, however, we would welcome empirical demonstration. The further key assumption of these studies is that there is a cost to aposematic signalling, and this cost increases relentlessly (or decelerates more gently than the benefit) with increasing signal conspicuousness. This cost may be imposed by a fraction of predators that attack even strongly signalling prey (perhaps because they have evolved to overcome the prey's defences, or simply because they have yet to learn to avoid the prey), and increasing prey conspicuousness increases the prey discovery rate and hence attack rate by such predators [28]. A similar effect of higher conspicuousness leading to higher rates of detection can still select for intermediate levels of aposematism when predators are uniform in behaviour, provided that the probability of such a discovery leading to attack and prey death is non-zero [29]. Such non-zero attack rates are to be expected even from predators that have learned the aposematic signal if they manage (rather than minimize) their exposure to prey defences (see below). Finally, the cost may be a physiological cost of the compounds required to produce the conspicuous signal [30] or conflict between signalling to predators and other processes influenced by appearance (e.g. interactions with prey, interactions with conspecifics, UV protection or thermoregulation). All these potential costs seem biologically plausible, but more purpose-designed empirical explorations are needed.

Figure 2. Examples of (a) Ontogenic changes in morphology and appearance with size in different instars of lepidopeteran larvae, where early instars of the lime swallowtail butterfly (Papilio demoleus) resemble bird droppings and later instars appear to combine camouflage and warning signals. (b) and (c) are examples of apparently weak warning signals in Ranitomeya fulgurita and Phyllobates aurotaenia, respectively. (a) Reproduced with permission from © Martin Stevens (b) © Fernando Vargas (c) © Adolfo Amezquita.

One of the most convincing examples of a less-than-maximally conspicuous aposematic signal is that of the European viper (Vipera berus). Using Plasticine models, Wüster et al. [18] demonstrate that individuals bearing the distinctive zig-zag pattern of this snake were attacked less by wild-living predators than plain models and (since this effect occurred even when models were placed on a plain background) that this effect was due to avoidance of the pattern rather than crypsis. This experiment was carried out in a locality with no other venomous snake species, and no other snake species of similar appearance, suggesting that mimicry or generalization across prey types are unlikely to be important factors. While the appearance of adders to humans is distinctive, it is far from conspicuous, and could be cryptic when viewed from a distance.

It has long been known that viewing distance may greatly influence signal function. Tullberg et al. [31] performed a study involving photographs of swallowtail butterfly (Papilio machaon) larvae. These caterpillars have a distinctive appearance with brightly coloured dots and have been shown to induce learned avoidance in a range of avian predators. Tullberg et al. manipulated photographs of the larvae to make them more or less conspicuous, and then demonstrated that when viewed at close range (by humans) larvae were not maximally cryptic, but were also not maximally conspicuous when viewed from a distance. These observations lead to the hypothesis that (because the resolution of the eye is limited) the same appearance might function as crypsis when viewed from a distance and aposematism when viewed from closer range. These results deserve follow-up study. First, it is important to demonstrate conclusively that larval appearance plays an important role in predator avoidance, through studies that manipulated such appearance. Then work should test if the appearance of such prey could be manipulated to make them more detectable to ecologically relevant predators when viewed from a distance, and less effective in deterring attacks when viewed at close range. At present, only Marshall [27] has explored distance dependent effects on coloration when considering realistic receiver (as opposed to human) vision. Finally, it would be interesting to design studies to explore whether there is a trade-off between the type of appearance that functions well in long-distance crypsis and that which functions well in close-range aposematism.

4. Intraspecific variation and polymorphism in aposematic signals

There seems to be variation in the conspicuousness of aposematic signals both within some species and sometimes between closely related species. Such variation requires explanation because one would expect that uniformity of signalling would aid learning and recognition by predators and thus benefit the prey. In addition, some species may even be polymorphic, with individuals falling into different discrete morphs. There are several potential non-mutually exclusive mechanisms to explain this, including that alternative phenotypes may have equal fitness, they may exist through negative frequency-dependent selection, or heterozygote dominance. Such processes may arise due to environmental variation (spatially or temporally) allowing different morphs to co-occur or to exist at different times or locations, if, for example, backgrounds differ in structure or coloration, which in turn differentially influences conspicuousness of the different morphs. Additionally, seasonal differences in predator communities could lead to variation. For instance, in temperate environments there may be more naive predators in the spring than summer, leading to greater costs of conspicuousness in the spring. Species may also be trading off multiple selection pressures acting on their coloration, only one of which is aposematism. Phenotypic plasticity may allow variation in how the balance between such trade-offs are expressed in individuals. Overall, these processes may lead to true polymorphisms in traditional terms of genetically distinct co-occurring morphs, or more commonly to continuous intraspecific variation or seasonal forms arising under different environmental conditions. Below, we focus mainly on two relatively well-studied systems that illustrate some of the above issues.

The costs and trade-offs of aposematic signal form are well illustrated by studies of the wood tiger moth (Parasemia plantaginis). In this species, continuous variation exists in terms of the colour and size of an orange spot on the otherwise black larvae, and also in the hindwings of the females, which vary in terms of how red–orange they are. The adult males, however, come in two morphs, with either white or yellow hindwings. Lindstedt et al. [32] demonstrated that larvae reared in cooler conditions had a smaller and duller spot, and this was linked to faster development time and growth rate at low temperatures. However, smaller, duller spots were less effective in promoting avoidance learning of larvae than larger, brighter spots, whereas brighter spots were more likely to incur predator detection [33].

Experiments have also shown that the coloration of adult P. plantaginis can be influenced by diet quality [34]. In addition, in aviary experiments with great tits (P. major), females with redder hindwings were avoided more than those with more orange hindwings, potentially selecting for reduced variation [35]. In contrast, in field trials, when presented to the entire community of potential predators, there was no significant difference in survival between red and orange forms. This could indicate that under more complex environments selection for a specific signal form is reduced [35]. However, although not significant, there was a trend for higher survival in the red compared with the orange forms. Therefore, more work is needed here, especially as the different colours may have different contrasts against different background types. Finally, in males, both field and aviary experiments show that yellow males are avoided more than white males, but that white males have higher mating success [36]. In P. plantaginis, therefore, various factors contribute to the colour variation of both larvae and adults, illustrating how many selection pressures may be influencing warning signal form.

In other species, variation is manifested in discrete morphs. A widely studied group are the poison frogs of Central and South America. The striking colours of poison frogs are iconic examples of aposematism (e.g. [37,38]), but the colour patterns are also used in mate choice [39]. Some species can be strongly polymorphic, often varying greatly geographically. In the polymorphic strawberry poison-dart frog (Oophaga pumilio) females seem to prefer to mate with males of the same colour morph [39,40]. Field experiments by Noonan & Comeault [41] with artificial clay models of Dendrobates tinctorius have shown that novel (‘immigrant’) phenotypes are attacked more by predators than locally occurring forms. Thus, the implication is that the appearance of some poison frogs acts as a ‘magic trait’, acting in both assortative mating and predation. In O. pumilio, incipient speciation may exist, with mating between morphs producing offspring with intermediate appearance phenotypes or inappropriate mate preferences, and thus reduced fitness, potentially leading to reinforcement reducing mating between morphs [42,43]. In populations where more than one morph occurs, females show stronger preferences for their own morph than females in populations with only one morph present, consistent with intraspecific reproductive character displacement [42]. Predation pressure is normally thought to constrain communication strategies used in mating, but here the opposite may be the case and the combination of apsosematism and mate choice could be driving geographical polymorphisms.

5. The informational content of conspicuousness

Above, we have discussed how variation in aposematic signal form and polymorphism may occur. Several recent theoretical studies have also explored whether there might be an association between levels of conspicuousness and levels of defence that could potentially provide useful information to predators hence we ask: are warning signals reliable with respect to the prey's defence levels?

Franks et al. [44] demonstrate with a mathematical model that the evolution of mimicry of highly defended model species is easier to achieve because predators will avoid even poor mimics of very strongly defended models. Thus, for a very highly defended species to avoid initially cryptic undefended prey from evolving towards them in appearance they must have a very conspicuous appearance. Intermediate appearances may exist where the costs of raised conspicuousness to the would-be mimic are greater than any benefits from approximate mimicry. Thus, Franks et al. predict a positive correlation (across species) between levels of defence and conspicuousness.

Franks et al. [44] also speculate that highly defended prey might be more conspicuous because they can offset the cost of increased encounter rates with predators if their defence allows them to better survive attacks or speeds aversion learning by predators. However, the theoretical work of Leimar et al. [45] predicted a negative correlation across species between conspicuousness and potency of defence. This arises in their model because prey with better defences can better survive attacks, and so benefit from reducing their investment in costly conspicuous signalling even if this decreases the rate of learning. Speed & Ruxton [30] demonstrate that the optimal combination of investments in aposematism and defences depends critically on how the cost and benefits are affected by the values of these two traits, and are also affected by population density and aspects of life-history strategy. Both negative and positive correlations (as well as no correlation) can be predicted under different sets of model assumptions. Thus, interspecies correlations between conspicuousness and potency of defences cannot be expected to be strong unless the species concerned are very similar in ecology.

Blount et al. [46] predict a negative correlation between conspicuousness and potency of defences between individuals within the same population, based on a model whose critical assumption is that both defence and appearance compete for some limited resource. They argue that for toxic defences, such a resource is likely to be anti-oxidant molecules that serve both as pigments and in protecting the individual from oxidative stress as they accumulate toxins within their body. Another important model assumption is that a predator's decision to attack a prey individual is influenced by the combined (interacting) levels of defence and conspicuousness and not the two independently. We would very much welcome the behavioural study of such attack decisions in real predators, and physiological study that might evaluate the importance of the presumed physiological competition between defence and signalling.

Speed et al. [47] present a model that offers another mechanism that could lead to a within-species positive correlation. They assume that individuals vary in level of defence and that this is environmentally conferred rather than being genetically determined (as might happen if individual host plants of herbivorous insect larvae vary in the levels of secondary chemicals that the larvae can sequester). They also assume that an individual can select its appearance once its defence level is determined, with greater conspicuousness attracting more encounters with predators. A predator's decision to attack is based on knowledge of the mean level of defence (across the prey population) associated with different levels of conspicuousness. The probability of the individual surviving any attack increases with its level of defence. Simulated prey populations evolved such that prey of each defence level varied in appearance, but on average there was a positive correlation between defence level conspicuousness, with predators being more likely to avoid attacking more conspicuous individuals. Thus, predators benefit from conspicuousness being at least a partially reliable signal of defence level.

Clearly, further empirical study is required and a number of pioneering studies may suggest suitable study groups. Cortesi & Cheney [48] report a positive correlation between conspicuousness and toxicity across 20 species of marine opisthobranches. This might be a particularly suitable group for further study since the animals themselves have limited vision and so their appearance is unlikely to be strongly influenced by within-species interactions. The next useful step would be to demonstrate that an ecologically relevant predator is sensitive to the measured variation in signal conspicuousness.

Summers & Clough [38] reported a positive correlation across species of dendrobatid frogs between conspicuousness to humans and alkaloid concentration from skin secretions. However, the situation in this group appears more complicated, since Darst et al. [37] report that closely related species appear to have either increased conspicuousness or toxicity, but not both, and that various work indicates that appearance is important in mate choice decisions (see above). Further progress with this study group may require overcoming the significant logistical challenges of exploring predation threats in the wild.

Within a single ladybird population, Bezzerides et al. [49] report strong variation in the extent of red coloration on the wing elytra that was correlated with levels of alkaloid defences. Again, exploration of whether predators are sensitive to this variation would be very worthwhile, although it will be important to remember that elytra coloration has been shown to be important in mate choice in the species concerned. Finally, some defended prey have minimal warning signals and may even be cryptic. Work with pine sawfly larvae (Neodiprion sertifer and Diprion pini), which are chemically defended, indicates that conspicuousness does not evolve because detectability costs of more conspicuous signals increases predator attacks and also because the chemical defences are not costly to produce [50]. We would welcome further tests of this finding in other groups.

6. Integrating warning signals more generally into behavioural and evolutionary biology

Warning signals do not exist in isolation from other traits that influence the fitness of individuals, and there are still interesting issues to explore to understand how such interactions occur. One area that would benefit from further study is predator foraging strategies and how they affect the evolution of signal form. For example, in some laboratory experiments, predators do not behave so as to minimize their exposure to toxic prey but rather to manage their exposure. Skelhorn & Rowe [51] and Barnett et al. [52] demonstrate that predators that have learnt an association between toxin load and appearance of a given prey type modulate their use of that prey type in ways that can be understood in terms of strategic utilization of the nutrients contained in that food while managing exposure to toxins. This suggests that predators do not simply categorize a particular prey as ‘bad’ but rather have a more nuanced representation of the costs and benefits. We would be interested in the expansion of this work to more complex prey environments involving many different prey types, in order to explore to what extent predators categorize prey, how they generalize between different types, and how aspects of aposematic signals influence this. It has also long been known that predators show innate unlearned biases against certain signalling traits and some of those can be associated with the appearance of dangerous animals (such as snakes) for which learned avoidance would be too costly. An interesting strand of research seeks to integrate such phenomena within a general theory of dietary conservatism by predators [53]. It is clear that predators can have a long-term reluctance to sample novel food items that can be interpreted in terms of controlling the risk posed by prey defences, and that the deactivation and reinstatement of such avoidance behaviours can be influenced by predator state, previous experience and environmental cues [54]. We would welcome further study into what drives variation in neophobia between predatory individuals, and the role of prey traits in influencing this behaviour.

Higginson & Ruxton [55] provide an attempt to predict how aposematism might be expected to change over the lifetime of an individual, and how it might be affected by such life-history traits as longevity and reproductive strategy. However, this work did not consider interactions between individuals with different strategies. This is important when it is known that aposematic signals and defences can both vary within a population. Further, predators' responses to a given signal are likely to be influenced by previous experience, which in turn is likely to be influenced by the signalling and defences of other prey in the same locality. Finally, individual prey can share limited resources and resource depletion is likely to often be an important mechanism by which individuals influence those around them.

Cryptic animals are often restricted to certain backgrounds and individuals may only be active at certain times because movement is often antipathetic to good crypsis. These opportunity costs are not generally considered to apply to aposematism. Speed et al. [56] make the important point that greater freedom to exploit resources may be an important selective pressure encouraging evolution of aposematism. We would also argue that aposematism might influence other aspects of life-history through this mechanism. For example, if aposematism allows greater freedom of movement and/or access to new resources then it might also allow faster growth rates and earlier maturation or larger size at maturation. There is a need to clarify these arguments in theoretical development (perhaps using Higginson & Ruxton's work as a foundation), but some of these ideas are already clear and logically sound enough to justify empirical testing. Ontogenic colour change (figure 2) may provide a useful phenomenon to study opportunity costs of crypsis for the adoption of aposematism, since it has been argued that organisms switch to aposematism in life-history stages where foraging or mating demand extensive movement that would reduce the effectiveness of crypsis [57,58]. In contrast, warning signals may be ineffective when body size (and thus signal size) is very small. In this instance, crypsis may be more effective.

Finally, aposematism and mate choice can interact in ways that have implications for macroevolution (see also discussion of poison frogs in §4). For instance, Heliconius butterflies are a diverse group with closely related species often differing greatly in appearance, while distantly related species often converge in appearance owing to Müllerian mimicry against predators (see reviews by Jiggins [59] and Mallet & Joron [60]). Jiggins et al. [61] have shown that two sister species, Heliconius melpomene and Heliconius cydno, differ in coloration and habitat use and have recently diverged to mimic two different models (Heliconius erato and Heliconius sapho, respectively). The colour patterns in each species are important in mate choice, and when the populations occur in sympatry individuals are less likely to court members of the other species than when found in allopatric populations. When hybridization does occur, intermediate phenotypes lack effective mimicry of either model, and are thus likely to be vulnerable to predation. At interspecific contact zones reinforcement may occur, leading to character displacement of mating preferences to prevent hybridization [62]. However, although mark–release–recapture experiments with different morphs of H. erato in different locations indicate that foreign morphs have lower survival than resident morphs owing to predation [63], predator selection against hybrids has rarely been explicitly demonstrated or even tested [59] and this remains a key piece of work needed to ‘complete’ the story. Finally, Heliconius butterflies can also provide important information about the genetics underpinning warning signal form. For example, recent work shows that a single gene (optix) drives variation in the red colour wing patterns across several species of Heliconius [64]. It will be valuable to discover more in a range of species about how specific genes may allow both diversification in signal form across populations and species, and how some colour types may be constrained.

7. Conclusion

There is growing consensus that we now have a robust understanding of the mechanisms underlying the evolution of aposematic signalling [1] hence, we feel that the time is ripe to extend this understanding to the diversity and functioning of naturally occurring aposematic signals. We have summarized the areas of current understanding and provided suggestions as to how the gaps within and between these areas might be bridged. We have also provided pointers as to how aposematism can be incorporated most effectively into the study of life-history strategy and how its relevance to foraging ecology and speciation might most usefully be explored. Despite many years of study, aposematism has much still left to tell us about evolution and ecology.


Introduction

Sleep is a widespread behavior, argued to provide essential restorative effects (Siegel 2005) and memory consolidation (Diekelmann and Born 2010). Many animals spend a large proportion of their time asleep, and can be especially vulnerable to predation and other environmental risks during this time (Lima et al.2005). Selecting a suitable sleeping site is therefore crucial for fitness, as it provides shelter and safety, and can facilitate social contact (Di Bitetti et al.2000 Hamilton 1982 Takahashi 1997). Studies of sleeping behavior in mammals generally find that either predation avoidance (e.g., degus, Octodon degus: Lagos et al.1995) or thermoregulation (e.g., koalas, Phascolarctos cinereus: Briscoe et al.2014), or both (e.g., pine martens, Martes martes: Birks et al.2005 Eastern spotted skunks, Spilogale putorius: Lesmeister et al.2008 North American porcupines, Erethizon dorsatum: Mabille and Berteaux 2014 and roe deer, Capreolus capreolus: Van Moorter et al.2009) are prominent factors affecting sleeping behavior, including site selection.

Predation risk appears to be the main factor driving sleeping site selection in primates. Olive baboons (Papio anubis) prefer to sleep in higher areas that are less accessible to leopards (Panthera pardus: Hamilton 1982) black-tufted marmosets (Callithrix penicillata) in urban areas choose tall trees to avoid predation from cats (Duarte and Young 2011) pileated gibbons (Hylobates pileatus) seek tall trees with few lower branches to avoid terrestrial predators (Phoonjampa et al.2010) and chimpanzees (Pan troglodytes ellioti) choose to build terrestrial nests only in areas where they are not under threat from humans (Last and Muh 2013). However, it is unlikely that predation risk exclusively influences where primates sleep, and some species such as pigtailed macaques (Macaca leonine) combine predation avoidance with other environmental factors (e.g., distance to food resources) when selecting sleeping sites (Albert et al.2011).

Microhabitat features known to influence primate sleeping site selection may offer antipredator benefits e.g., tree height (Albert et al.2011 Di Bitetti et al.2000 Rode et al.2013) offers a vantage point from which to spot terrestrial predators, and inaccessibility to predators greater tree diameter at breast height (DBH Cheyne et al.2013 Di Bitetti et al.2000 Hankerson et al.2007 Rode et al.2013) indicates structural stability in case of need for evasive or defensive action greater tree connectivity (Kenyon et al.2014) and density of undergrowth (Dagosto et al.2001) offer escape routes and canopy cover (Hankerson et al.2007 Rode et al.2013) may offer concealment, especially from aerial predators. By sleeping in dense foliage, animals such as Northern giant mouse lemurs (Mirza zaza: Rode et al.2013) and green monkeys (Cercopithecus sabaeus: Harrison 1985) remain cryptic yet able to sense vibrations from approaching scansorial and aerial predators. Dense vegetation is also favored by Neotropical primates for parasite avoidance (Nunn and Heymann 2005). Alternatively, dense ground vegetation may provide cover for terrestrial predators, thus increasing predation risk (Bettridge and Dunbar 2012 Cowlishaw 1997a, b). The relative importance of each of the foregoing factors is subject to the ecological pressures on the population, and to gain further insight into the sleeping site ecology of primates, repeated use of sites should be monitored (Anderson 1984). Individuals may trade off conflicting pressures, meaning that to reduce detection by predators, even the most desirable sleeping sites may not be used consistently (Day and Elwood 1999).

Thermoregulatory hypotheses, where animals adapt their sleeping site behavior for thermoregulatory advantages, also explain elements of primate sleeping site selection (Anderson 1984 Stewart et al.2018). Western chimpanzees (Pan troglodytes verus) use a humidity avoidance strategy when building arboreal nests (Koops et al.2012). Thermoregulation is likely to be a greater consideration for smaller primate species golden-brown mouse lemurs (Microcebus ravelobensis) use leaf nests more frequently in low temperatures (Thorén et al.2010) and Japanese macaques (Macaca fuscata) sleep on lower ground to facilitate larger groupings for huddling in cold winters (Takahashi 1997). Thermoregulatory pressures may also vary seasonally, or throughout an animal’s life. For example, the importance of thermoregulation in sleeping site choice of female gray mouse lemurs (Microcebus murinus) changes with seasonality and increases when they have offspring (Lutermann et al.2010). Some nocturnal primates may select particular microclimates to sleep in to reduce overheating from the sun. For example, mouse lemurs (Microcebus spp.) favor insulated sleeping sites with less extreme fluctuations in temperature when ambient daytime temperatures are high (Karanewsky and Wright 2015 Schmid 1998), and less insulated sites during periods of heavy rainfall (Lutermann et al.2010). Dense canopy cover can be an important factor in providing protection from the ambient temperature by shading animals from the sun (Duncan and Pillay 2013).

Much of the previous research into primate sleeping behavior has focused on diurnal primates. The earliest primates were thought to be small (Soligo and Martin 2006) and nocturnal (Ross et al.2007), similar to the nocturnal strepsirrhines of today (Crook and Gartlan 1966). Therefore, knowledge on the behavior and ecology of extant nocturnal primates aids our understanding of the selection pressures that acted on some of the earliest primate species before the appearance of diurnality. Some nocturnal primates (owl monkeys, Aotus spp. and mouse lemurs, Microcebus spp.) are “marathon sleepers”, spending a much greater time asleep than diurnal primates do (Nunn et al.2010). The importance of a safe sleeping site is therefore paramount in nocturnal primates, but detailed information on the sleeping behavior of many species in Asia and mainland Africa is unavailable (Bearder et al.2003 Svensson et al.2018).

Nocturnal primates are likely to be vulnerable to a different predator guild than their diurnal counterparts because of high levels of inactivity during daytime hours. Small, arboreal, nocturnal primates are estimated to be predated on at a greater rate than other primate groups (Hart 2007) but reports of predation on nocturnal primates are scarce (Burnham et al.2012 Hart 2007). Known predators of nocturnal primates include snakes, felids, nonfelid carnivores, raptors, and other primates including humans (Burnham et al.2012 Svensson et al.2018). Nocturnal primates may be especially vulnerable to predation during the daytime (Butynski 1982 Pruetz and Bertolani 2007) therefore a level of crypsis is required when sleeping (Bearder et al.2002 Burnham et al.2012 Nekaris and Bearder 2011 Svensson et al.2018).

Galagos are nocturnal, arboreal strepsirrhine primates distributed across sub-Saharan Africa, comprising six genera: Euoticus, Galago, Galagoides, Otolemur, Paragalago, and Sciurocheirus. Taxa vary in sleeping behavior and ecology (Svensson et al.2018), but generally, galagos sleep in groups with variable membership during the day and forage alone at night (Bearder 1999 Bearder and Doyle 1974 Bearder et al.2003 Charles-Dominique 1977 Harcourt and Nash 1986), with particular sleeping sites used repeatedly by different individuals (Bearder et al.2003). Galago nests, built by a number of species within the Galagoides, Galago, and Otolemur genera, are usually leaf and twig, open platform constructions within thorny trees, presumably to provide protection from predators (Bearder et al.2003). In addition, Galago spp. and the thick-tailed galago (Otolemur crassicaudatus) use tree cavities, dense tangles of vegetation, and branches as sleeping sites (Bearder et al.2003 Svensson et al.2018). Some species sleep in areas of dense forest canopy and understory cover (e.g., Allen’s squirrel galago, Sciurocheirus alleni and elegant needle-clawed galago, Euoticus elegantulus: Laurance et al.2008). Brief periods of torpor have been recorded in the Southern lesser galago (Galago moholi) but they largely favor behavioral and ecological adaptations, such as increased huddling behavior and choosing insulated sleeping sites (enclosed cavities and nests rather than open branches) over torpor use for survival in cold, dry winters (Nowack et al.2013).

Reptiles such as snakes (Svensson et al.2018), and raptors such as Verreaux’s eagle (Aquila verreauxii: Baker 2013, given in Svensson et al.2018) and hawks (Ambrose and Butynski, given in Svensson et al.2018), are either observed or suspected predators of galago species. Genets (Genetta spp.) are also predators of galagos (Burnham et al.2012 Mzilikazi et al.2006), but are more likely to hunt galagos at night or at dusk when they are active, rather than when they are sleeping (Bearder et al.2002). Western chimpanzees (Pruetz and Bertolani 2007) hunt Galago senegalensis from tree cavities but are not present at our study site, and researchers have observed vervet monkeys (Chlorocebus pygerythrus) eating (though not catching) a Northern lesser galago (G. senegalensis: Phyllis Lee, pers. comm. to C. Bettridge).

Galago senegalensis is the most widely distributed of the galagos, ranging across sub-Saharan Africa in a variety of habitats, such as woodland, bushland, savannah, and montane forest (Bearder et al.2008). Details of G. senegalensis sleeping site ecology and sociality featured in a review of galagos (Bearder et al.2003) and two short-term studies focused on the habitat ecology of populations in Kenya (Off et al.2008) and The Gambia (Svensson and Bearder 2013). However, no studies have addressed the sleeping site ecology of this species in great detail. In East Africa, populations of G. senegalensis are associated with Acacia spp. (Nash and Whitten 1989 Off et al.2008), which provide both sleeping sites (Haddow and Ellice 1964 Nash and Whitten 1989) and food sources (Acacia gum: Nash and Whitten 1989 Off et al.2008). Non-Acacia trees also provide suitable sleeping sites for the Kenyan sub-species G. s. braccatus (Nash and Whitten 1989). Known structure types to support sleep in G. senegalensis are nests (Bearder et al.2003), in tree cavities (Haddow and Ellice 1964 Svensson and Bearder 2013), on tree branches, or in dense tangles of vegetation (Nash and Whitten 1989 Svensson and Bearder 2013).

Here we describe the nesting behavior and sleeping site preferences of a population of Galago senegalensis in the Kwakuchinja wildlife corridor, Northern Tanzania, investigating the ecological importance of environmental variables on their sleeping site choice. If predation risk is a strong selective pressure influencing sleeping behavior galagos will sleep in trees with greater connectivity and canopy cover, and in areas with greater tree and mid-level vegetation density, but lower levels of ground cover. If thermoregulation is important to G. senegalensis we predict that cooler, more sheltered sites will be preferred. We aim to identify the levels of tree density, canopy cover, and vegetation cover that are preferred for sleeping sites with a view to establishing the habitat requirements for this and similar species.


When and where did bipedal hopping arise?

One of the most poorly understood aspects of bipedal hopping is the evolutionary origin. Although many bipedal hoppers presently inhabit arid or semi-arid habitats, fossil evidence indicates several lineages likely arose in humid, structurally complex forests. Marcropodoidea (the clade containing kangaroos, wallabies and potoroos) originated around 40 million years ago from a small, arboreal, possum-like ancestor (Burk and Springer, 2000 Burk et al., 1998 Meredith et al., 2009 Szalay, 1994). Bipedal hopping appears to have evolved once within this clade to the exclusion of one genus, Hypsiprymnodon, which utilizes quadrupedal bounding and may represent an intermediate in the evolution of bipedal hopping (Burk et al., 1998 Meredith et al., 2009 Szalay, 1994 Westerman et al., 2002). All macropodid species share at least some morphological features associated with bipedal hopping, including elongated feet and tarsal modifications that stabilize the ankle joint and limit motion to flexion–extension (Marshall, 1973 Warburton and Dawson, 2015 Warburton and Prideaux, 2009 Szalay, 1994). The ancestral habitat for this group was likely dense forest however, in the last 5–10 million years, macropodines underwent a rapid radiation (Meredith et al., 2009) and extant species now inhabit a diverse range of habitats. While the majority still live in forested environments, species have evolved to live in almost every niche available, including deserts, grasslands, rocky cliff faces and even trees (Van Dyck and Strahan, 2008). Macropods also encompass a wide size range, from 1 to 90 kg, although extinct species likely reached as much as 250 kg (Helgen et al., 2006). Much of this increase in body size appears to have coincided with Australia becoming cooler and drier, with rainforests giving way to grasslands and now deserts (Burk et al., 1998 Martin, 2006 Prideaux and Warburton, 2010).

Rodent bipedal hopping is often referred to as an adaptation to desert environments (Bartholomew and Caswell, 1951 Berman, 1980 Ford, 2006 Howell, 1932 Mares, 1975 Moore et al., 2017a Webster and Dawson, 2004) however, a large body of literature indicates bipedal ancestors of Heteromyids and Dipodidae first appeared in mesic to wet, structurally complex forests, grasslands and riparian environments (e.g. Voorhies, 1975 Wu et al., 2014). Ancestral and/or extinct bipedally hopping Heteromyidae include Prodipodomys, found extensively in the moist lowland savannahs of eastern Nebraska during the late Tertiary. This genus and Eodipodomys populated habitats in or near wetlands before North American deserts evolved, but already exhibited inflated auditory bullae and locomotor morphological traits similar to those of modern Dipodomys (Voorhies, 1975). Recent work suggests that ancestral jerboas were hopping before 14 million years ago in humid, forested environments and that dental morphology evolved to meet the demands of changing food resources in arid environments (Wu et al., 2014). Extant Pedetidae includes two species, Pedetes capensis from Southern Africa and Pedetes surdaster, which appears in Eastern Africa. The earliest known Pedetidae representatives, known as genus Megapedetes, appeared around 20 million years ago (Senut, 2016). As the name suggests, these rodents were more robust in body size as well as morphological features related to locomotion. Species in this genus exhibit five rather than four toes, shorter femoral shafts, tibias and calcaneums, and various skeletal features that suggest members of this genus were less agile than extant Pedetes (Senut, 2016). Megapedetes occupying warm, wooded Namibia during the middle Miocene were smaller and relatively more gracile compared with members of this genus living in forests of Kenya (Senut, 2016). In Australia, species of the hopping mice genus Notomys diverged in locomotor morphology from quadrupedal ancestors well before the recent appearance of true deserts however, the prevalent misconception that bipedal hopping evolved in arid environments often leads to a confounding timeline (Ford, 2006). The fossil record and paleoecological reconstruction suggest conflicting environments for the extinct, putatively bipedal hopping marsupial Microtragulus during the Pliocene. Hydrochoeridae and crocodile remains suggest warm, humid environments, but contemporaneous small rodents are more likely indicative of xeric environments (Ortiz et al., 2012).

Quadrupedal bounding species in the genera Zapus and Napeozapus are sister taxa to bipedal Dipododinae and are thought to represent intermediate morphological forms between bipedal hoppers and strictly quadrupedal rodents (Hamilton, 1935 Berman, 1980 Lebedev et al., 2013). Species in these genera exhibit long hindlimbs relative to forelimbs (but do not fall below the 0.43 forelimb length:hindlimb length ratio Fig. 2) and have been reported to leap up to 4 m away from potential predators (Hamilton, 1935). However, species in this clade lack secondarily simplified distal hindlimb skeletal elements (Berman, 1980 Lebedev et al., 2013), inhabit cluttered, forested environments (Hamilton, 1935) and only use bipedalism during rapid escape maneuvers (Harty, 2010). The intermediate forelimb:hindlimb ratio, bipedal escape behavior and use of forest or shrub environments suggest tradeoffs between bipedal hopping and effectively moving through dense, cluttered habitats.

Given the overwhelming paleoecological evidence, we conclude that mammalian bipedal hoppers likely first appeared in humid, structurally complex forests. At the very least, no evidence suggests bipedal hopping evolved in deserts (Burk and Springer, 2000 Ford, 2006 Meredith et al., 2009 Ortiz et al., 2012 Senut, 2016 Voorhies, 1975 Wu et al., 2014). Jaw, tooth and gut morphology evolved after bipedal hopping to meet the challenges of increasingly arid environments (Alhajeri et al., 2016 Burk et al., 1998 Hume, 1989 Wu et al., 2014). Specific adaptations are beyond the scope of this Review however, they are likely fundamental drivers of extant rodent and macropodid diversity.

Although bipedal hoppers did not arise in deserts, this mode of locomotion is clearly effective in this environment. For example, although bipedal hoppers are less species rich relative to quadrupedal fauna in North America, Dipodomys merriami is the most commonly encountered species in any North American desert (Kelt et al., 1999). Furthermore, bipedal hoppers are the most dominant mammals in the Gobi and Turan Desert regions (Kelt et al., 1999). In Australia, several species of macropods inhabit desert regions (Morton, 1979) where locomotor efficiency may enable them to access scarce water resources (Webster and Dawson, 2004). Given the conundrum that bipedal hopping did not evolve in deserts, but almost all extant bipedal hoppers are found in arid or semi-arid environments, we review the literature that corresponds to selective pressures inhibiting, maintaining and promoting diversification of bipedal hopping mammals.


Introduction

Juvenile animals are usually smaller and less agile than adults. As a consequence, young are often more vulnerable to attack by predators. Indeed, some predators take advantage of this and prefer to attack juveniles [1], [2]. This difference between juveniles and adults has led in many cases to the development of age-specific, passive and active defense strategies. For example, Thomson's gazelle fawns and young Iberian green frogs rely on crypsis more than adults, tolerating shorter approach distances of the predator before executing an escape response [3], [4]. In broad-headed skinks, on the other hand, the adults are the cryptic ones and the juveniles wave their brightly colored tails to deflect predators away from their body [5]. Another way of defending against predators is to display aggression. Adult American lobsters threaten and attack an approaching predator as opposed to the juveniles which prefer to retreat [6], [7]. In other animal species, the juveniles are the aggressors: some species of gall-forming aphids produce first or second-instar soldiers that defend the colony by clasping insect predators and piercing them with their stylets [8] in several snake species, juveniles, which suffer greater predator-induced mortality, are more likely to display aggressive-defensive behaviors [9], [10]. Juveniles may also compensate for their higher vulnerability to predators by escaping, more frequently than adults, to a different part of their habitat where they are camouflaged or less accessible, as demonstrated in grasshoppers [11] and freshwater snails [12].

Aphids (Homoptera: Aphididae) are good candidates for studying behavioral differences between young and mature individuals, for several reasons: they are rapidly reproducing, sedentary herbivorous insects that form colonies of mixed ages [13] they are subjected to a multitude of predators and parasitoids [14] they possess an array of defensive behaviors. Aphids may defend against their insect enemies (namely ladybugs, hoverfly larvae, lacewings, parasitic wasps, etc.) by secreting a sticky defensive substance that adheres to the predator's mouthparts, kicking, twitching, walking away or dropping off the host plant [15]–[19]. Dropping is the most effective way of escaping from enemies on the plant, but it also exposes the aphid to the risks of dying from high ground temperatures, being preyed upon by ground predators, or failing to find a new host plant [20]–[23]. Even if an aphid is successful in locating a new host plant, its fecundity may be impaired due to the expenditure of energy on searching and the loss of feeding time. Roitberg et al. [21] found that on the day after the dispersal of pea aphids, Acyrthosiphon pisum Harris, to new host plants following insect-predator disturbance, their fecundity dropped almost two thirds. Nelson [24] estimated the reduction in pea aphid total fecundity the day after a single predator-induced dispersal event at about 20%. An aphid is therefore expected to drop only when the cost of staying on the plant becomes greater than the cost of dropping [16], [17].

Another important threat to an aphid colony is being consumed by mammalian herbivores along with their host plant (incidental ingestion). The incidental ingestion of plant-dwelling insects by mammalian herbivores is a direct interaction that has been practically ignored by ecologists. It is probably a very common interaction [25], yet only a handful of studies have examined its ecological significance [26], [27]. Incidental ingestion by mammalian herbivores could profoundly affect plant-dwelling insects, and in at least a few aphid species has led to the development of an efficient defensive behavior: upon sensing the warm and humid breath of a mammalian herbivore, the aphids instantaneously drop off the plant in large numbers. In this way most of the adult aphids in the colony avoid being eaten by the herbivore [28], [29].

In addition to exhaling air, large herbivores also cause vibrational disturbances when brushing against or tearing off pieces of the plant. Hence, vibrations may also contribute to the aphids' mass dropping response [28], [29]. Substrate-borne vibrations have been shown to serve as indication to an approaching predator and to elicit an evasive dropping response in aphids [30], [31] and other animals. For example, larvae of a geometrid moth escape by hanging from silk threads when sensing the vibrations produced by insect enemies [32]. Embryos of the red-eyed treefrog hatch up to 30% earlier and drop from overhanging vegetation to the water, upon sensing the vibrations induced by egg-eating snakes [33]. The antipredator response of pea aphids increases when a simulated predator attack is composed of two cues: alarm pheromone secreted by conspecifics and vibrations [30]. The role of vibrational stimuli in the escape of aphids from mammalian herbivores, and the interplay between the response to mammalian breath and the response to vibration is, however, still unclear.

The cost of dropping off the plant is higher for young nymphs than it is for adults, because nymphs are more limited in their ability to walk and locate a new host plant [34] and are more susceptible, after dropping, to high air and ground temperatures than adults are [20], [23], [35]. Tokunaga and Suzuki [36] found that first-instar pea aphid nymphs walk, on average, 8 times more slowly than adults. Roitberg et al. [21] examined the dispersal of pea aphids to new host plants after escaping from ladybug attack, and found that first and second instar nymphs were 5 times more likely than apterous adults to die on the ground before reaching a new host plant. They also found that apterous adults were twice as likely to disperse to a new host plant as first and second instar nymphs, who tend to return to the original host. Due to the high cost of dropping, young nymphs are often less likely than adults to respond to a predator or parasitoid attack by dropping off the plant [17], [34], [37].

According to the threat-sensitive predator avoidance hypothesis [38], prey animals assess the risk of predation they perceive, and modulate their antipredator responses according to the level of risk. Presumably, this allows prey to balance the cost of predator avoidance with the danger of being caught.

We therefore hypothesized that because of the higher cost of dropping for the nymphs, they would require a more definitive indication of impending mammalian herbivory than would be needed by adults. Gish et al. [28], [29] have described the mass dropping of aphids in response to mammalian herbivore feeding, but have focused only on the behavior of adult aphids. In the current study we exposed pea aphids to simulated mammalian breath and to vibrational disturbance caused by automated leaf-picking. We quantified and compared the dropping responses of first-instar nymphs (henceforth referred to as “nymphs") and adults to different combinations of the two types of stimuli.


1 INTRODUCTION

The aim of this study was to test the ability to detect and react to dangers represented by European catfish chemical cues (Silurus glanis) among three model prey species: perch (Perca fluviatilis), roach (Rutilus rutilus), and rudd (Scardinius erythrophthalmus). Subsequent behavioral changes (activity, shoal cohesion, and use of refuge) were examined in the experiment. Furthermore, we evaluated the prey preferences of catfish when exposed to the same three prey species in an experimental laboratory setting. Finally, we review large-scale experiment data suggesting that European catfish might trigger change in prey fish community and encourage collecting more field evidence to verify the hypothesis that the direction of change is in accordance with behavioral response to chemical cues of tested prey species.


Predator avoidance and dietary fibre predict diurnality in the cathemeral folivore Hapalemur meridionalis

Though numerous mammalian taxa exhibit cathemerality (i.e. activity distributed across the 24-h cycle), this includes very few primates, exceptions being species from Aotinae and Lemuridae. Four non-mutually exclusive hypotheses have been proposed to explain the ultimate determinants for cathemeral activity in lemurs: thermoregulatory benefits, anti-predator strategy, competition avoidance and metabolic dietary-related needs. However, these have only been explored in the frugivorous genus Eulemur, with some species increasing nocturnality as a possible response to avoid diurnal raptors and to increase their ability to digest fibre during resource-scarce periods. Since Eulemur lack specializations for digesting bulk food, this strategy would allow for processing fibres over the full 24-h. The folivorous lemurids, i.e. genus Hapalemur, provide a divergent model to explore these hypotheses due to gastrointestinal adaptations for digesting dietary fibre and small body size compared to Eulemur. We linked continuous activity data collected from archival tags with observational behaviour and feeding data from three groups of adult Hapalemur meridionalis from January to December 2013. We tested the effects of thermoregulation, predator avoidance and the weighted proportion of digestible dietary fibre on the daily diurnal/nocturnal activity ratio using a Linear Mixed-Model. Our best-fit model revealed that increased canopy exposure and dietary fibre predicted greater diurnality. Our findings partly contrast with previous predictions for frugivorous lemurids. We propose a divergent adaptive explanation for folivorous lemurids. We suggest that the need to avoid terrestrial predators, as well as longer digestive bouts during bulk food periods, may override cathemerality in favour of diurnality in these bamboo lemurs.

Significance statement

Southern bamboo lemurs are active throughout the 24-h day, with high proportions of dietary fibre increasing diurnality, in contrast to other cathemeral primates. They also increase diurnality on days when using areas with greater canopy exposure, potentially avoiding nocturnal predators in risky foraging areas. We suggest that folivorous lemurids may require long periods of inactivity to conserve energy and digest dietary fibre, thus limiting activity to periods of optimal foraging efficiency over the 24-h cycle.


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Keywords: predator recognition, learning, alarm cue, social facilitation, size-structure, trophic, sensory

Citation: Meekan MG, McCormick MI, Simpson SD, Chivers DP and Ferrari MCO (2018) Never Off the Hook—How Fishing Subverts Predator-Prey Relationships in Marine Teleosts. Front. Ecol. Evol. 6:157. doi: 10.3389/fevo.2018.00157

Received: 27 March 2018 Accepted: 18 September 2018
Published: 16 October 2018.

Ann Valerie Hedrick, University of California, Davis, United States

Shawn M. Wilder, Oklahoma State University, United States
Mike S. Allen, University of Florida, United States
Rebecca Lee Selden, Rutgers University, The State University of New Jersey, United States

Copyright © 2018 Meekan, McCormick, Simpson, Chivers and Ferrari. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.


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