Plants and animals clearly have different sensory structures and capabilities, yet both may perceive cues related to the risk of attack by herbivores or parasites, respectively, in similar ways—just as for their perception of predators (Sheriff et al., 2020a). These natural enemies may be perceived pre-contact, during physical contact before consumption occurs, or even after some minor attack that has not yet incurred meaningful energetic costs to the victim. Because herbivores and parasites take some time to establish a successful feeding (consumptive) relationship compared to predators of animals (Raffel et al., 2008), this post-contact (but pre-consumption) time lag may represent a source of NCEs that is fairly unique to these two types of natural enemy, but also affects victim reliance on pre- vs. post-contact risk cues. Importantly, if consumption does not almost immediately begin after enemy contact, then potential victims of parasites or herbivores could still have time to react as compared to animal prey (Rigby et al., 2002), and thus rely relatively less on pre-contact signals of increased risk.

Pre-contact, plants and animals may perceive cues emanating from the enemy itself, e.g., chemicals such as kairomones (Ruther et al., 2002), or from conspecifics that have made contact or are undergoing consumption (Hart, 1990; Kant et al., 2015; Behringer et al., 2018). While the latter can clearly result in direct fitness reductions (CEs) for the individual(s) being consumed (and their kin), there is enormous potential to generate cues that contain information about the threat posed by shared enemies, thereby causing enemy RITRs which can cause NCEs in other individuals not under attack. Actual physical contact is also perceived by potential victims through various means, and can trigger responses to avoid progression into the consumption phase. Lacking eyes and ears, plants primarily rely on chemical and tactile cues related to herbivore presence.

There are a variety of ways by which plants can directly perceive their herbivorous natural enemies (see reviews by Howe and Jander, 2008; Fürstenberg-Hägg et al., 2013; Aljbory and Chen, 2018). Some of these cues do not require physical contact between the plant and herbivore, while others come into play after initial contact has been made, but before consumption begins (or in its initial stages before a plant response curtails the attack). Pre-contact, plants can perceive herbivore-generated chemicals used for intraspecific communication, meaning that pheromones can also act as kairomones if they have interspecific effects (Ruther et al., 2002). For instance, cotton plants exhibited a defensive response to boll weevil aggregation pheromones (Magalhães et al., 2019).

Post-contact, chemical and tactile cues appear to play roles in directly detecting risks from herbivory, such as snail mucous trails that induced a defensive response in thale cress (Falk et al., 2014). Other important post-contact chemical signals include arthropod oral secretions and excrement (frass), as well as plant cell wall fragments (Howe and Jander, 2008; Fürstenberg-Hägg et al., 2013; Ray et al., 2015, 2016; Aljbory and Chen, 2018). A heightened risk of herbivory can be sensed by tactile cues alone. Plants can detect various vibrations emanating from herbivores, such as those generated by chewing (e.g., Kollasch et al., 2020). Even light touches by arthropod feet can be perceived via plant epidermal hairs (trichomes) and elicit defensive responses (e.g., Peiffer et al., 2009). Not surprisingly, oviposition by herbivorous arthropods induces defense-related trait responses, following from both chemical (such as adherents) and tactile elements (reviewed by Hilker and Meiners, 2006).

Plants can gather information about the threat posed by herbivores through indirect means as well. Chemical cues from other individuals undergoing attack may play a particularly important role in enemy RITRs. Notably, plants rapidly emit biogenic volatile organic compounds (VOCs) in response to the first signs of consumption by herbivores (reviews by Howe and Jander, 2008; Aljbory and Chen, 2018; Ameye et al., 2018). Of herbivore-induced plant volatiles (HIPVs), green leaf volatiles (GLVs), which are comprised of six-carbon compounds (e.g., alcohols, aldehydes and esters), represent a particularly important subgroup. HIPVs in this subgroup can act as repellents in herbivore defense, but also induce or prime plant resistance against herbivory (Ameye et al., 2018).

The primary function of such HIPVs appears to be the rapid communication of risk to other parts of the same individual not yet under attack; internal chemical signals are less effective given the modular structure of most plants, thus airborne volatiles convey information faster (Fürstenberg-Hägg et al., 2013). In addition, plant parts that are in similar spatial locations may not share much vascular connection (e.g., two leaves from separate main-stem branches can be next to each other spatially but far apart vascularly). Recognition of these airborne chemicals in turn triggers molecular and physiological cascades that can induce trait changes related to resistance. Intriguingly, there is evidence that other plants (of the same or different species) may “eavesdrop” on such chemical signals, exhibiting trait changes in response to perceived enemy risk (reviews by Karban et al., 2014; Ameye et al., 2018; Bouwmeester et al., 2019). For example, undamaged, neighboring lima bean plants were able to recognize HIPVs from attacked plants, activating a defensive response in the form of extra-floral nectaries to attract enemies of herbivores (Kost and Heil, 2006).

In a similar vein, chemicals are thought to play a large role in animal perception of parasite risk considering that hosts are invariably larger than parasite infective stages (Lafferty and Kuris, 2002), and the latter are typically limited in their motility and generation of audiovisual cues. Whereas plants do not have eyes and ears to detect herbivores, such sensory structures, while present in animals, may be of limited use for gauging risk from minute infective stages of parasites. Chemical and tactile cues are thus expected to be more important signals of parasite presence than audiovisual cues. Like plants, potential animal victims respond to pre-contact chemical signals directly generated by the natural enemy, as well as those from conspecifics being attacked or consumed (Curtis, 2014; Buck et al., 2018).

In terms of chemical cues, animals may use parasite-associated proxies to gauge infection risk (Curtis, 2014; Buck et al., 2018). An inherent “disgust response” to fecal matter can serve to reduce contact with parasite infectious stages such as helminth eggs or larvae if their direct detection through odor or other means is difficult (Curtis et al., 2011; Sharp et al., 2015). A heterogenous “landscape of disgust” may thus drive spatial use decisions by potential hosts in response to proxies signaling parasite presence (Weinstein et al., 2018a; Kavaliers et al., 2019). That being said, direct chemical detection of parasites by potential hosts occurs. For instance, larval amphibians respond to dead trematode (parasitic fluke) infectious stages in the water through spatial avoidance (Koprivnikar and Penalva, 2015). This research supports the view that parasite risk can be perceived via parasite-derived chemical cues given the absence of other possible signals (e.g., vibrations).

Notably, animals under attack by parasites can emit chemical cues that transmit information about this danger to other individuals. Just as the breach of plant cell membranes can trigger the release of specific chemicals (Fürstenberg-Hägg et al., 2013), similar chemical releases can occur when animal tissues are damaged. The release of “alarm cues” as a result of predator-induced physical damage has been well-studied for certain prey, especially in aquatic habitats, and these alarm cues are readily perceived by conspecifics (see review by Ferrari et al., 2010). Some parasites cause damage to external host tissues that may generate chemical cues, as reported for parasites penetrating fish epidermis containing specialized alarm or club cells (Chivers et al., 2007). Conspecifics react to such chemicals—juvenile trout exhibited distinct behaviors in response to tank water from other trout exposed to a skin-penetrating trematode (Poulin et al., 1999). Beyond perceiving chemical cues associated with attack of a conspecific by parasites attempting to establish, it is also possible to detect individuals with already-established infections through chemosensory means. This has been observed with various animals, including amphibians, crustaceans, and rodents (e.g., Kiesecker et al., 1999; Behringer et al., 2006; Kavaliers et al., 2020).

Pre-contact, potential hosts can likely detect the presence of parasites in other ways. For instance, larval amphibians avoid areas with live infectious stages of trematode parasites, possibly detecting water vibrations generated by these free-swimming parasites in addition to potential chemical cues (Rohr et al., 2009). There are also reports of terrestrial animals reacting to parasites in the absence of contact where the sensory mechanisms involved are unknown. As an example, fruit flies (Drosophila) respond to the mere presence of parasitic mites separated by a fine mesh screen, but it is not clear whether these enemies are detected through chemical or visual means (Horn and Luong, 2018).

Physical contact with parasites during the pre-consumption phase, or in the initial stages of consumption, is thought to be perceived by potential animal hosts through various tactile means (see review by Kupfer and Fessler, 2018). Contact with ectoparasites, such as ticks and mites, quickly results in behavioral responses in a variety of animal species, from insects to mammals (see reviews by Zhukovskaya et al., 2013; Hart and Hart, 2018). Such immediate behavioral responses also occur in response to penetrating endoparasites. For example, larval amphibians respond to initial contact with free-swimming trematode infectious stages by engaging in characteristic defensive behaviors (e.g., Koprivnikar et al., 2006).

So, how do plants and animals compare in their perception of risk cues associated with their respective herbivore and parasite natural enemies? Chemical cues clearly play a large role for plants pre- and post-contact, and compound-specific attributes may allow plants to perceive specific risk associated with particular herbivores (Agrawal, 2005; Duran-Flores and Heil, 2016). Importantly, herbivores often exhibit species-specific feeding preferences (Bernays and Graham, 1988), and can be grouped into different feeding guilds (e.g., chewers vs. piercers). Plants respond differently to herbivores from different feeding guilds (Ali and Agrawal, 2012), and stronger responses to oviposition by specialist vs. generalist herbivores have been reported (Pashalidou et al., 2013). HIPVs released by plants under attack seemingly convey specific information as to the nature of the threat (Kant et al., 2009; Ameye et al., 2018). Other plants “eavesdropping” on these chemicals may therefore fine-tune their induced response(s) (Kant et al., 2009), and specific HIPVs may selectively attract appropriate enemies of the attacking herbivore (De Moraes et al., 1998).

Like plants and herbivory risk, various animals perceive parasite threat through chemical cues (Behringer et al., 2018; Kavaliers et al., 2020), although most studies to date have focused on particular host taxa, especially nematodes, honeybees, amphibians, and rodents (Sarabian et al., 2018). There is also evidence that animals, like plants, may be able to gauge more subtle aspects of risk through chemosensory means, such as parasite transmission potential and host compatibility (Sharp et al., 2015). For instance, uninfected guppies avoided both chemical and visual cues associated with conspecifics harboring an ectoparasite only in the later stages of infection when direct transmission was most likely (Stephenson et al., 2018).

In studying risk-associated chemical cues, it is also important to consider receptors to highlight the molecular and physiological pathways that are engaged in eliciting responses, and to further elucidate which taxa have evolved specific capability of perceiving enemy risk through chemosensory means. For plants, a receptor has been identified for only one HIPV (ethylene), and finding others represents a key area of further study (Ameye et al., 2018; Karban, 2020). Similarly, the olfactory structures involved with animal detection of parasite-associated chemical cues have been identified only in a few species, primarily rodents and fish (e.g., Wisenden, 2014; Boillat et al., 2015).

Although plants and animals are unlikely to share actual compounds and receptors involved in perceiving enemy risk, broad comparisons of these two victims are still possible to consider the ecological and evolutionary context for features of reliable enemy cues. These comparisons suggest a number of interesting questions, some of which we propose below:

Although resistance against natural enemies can involve constitutive and/or induced traits, only the latter are of relevance for causing NCEs, i.e., there are specific fitness costs associated with expressing phenotypic plasticity as a response to changed risk (Peacor et al., 2020). Induced trait changes encompass a broad suite of strategies used by potential victims to reduce enemy encounter, and/or the likelihood of a successful attack resulting in consumption. While the latter represent adaptive responses that may have associated costs, there is presumably a net benefit; however, maladaptive responses are also possible if the overall costs outweigh the benefits (e.g., Sih et al., 2010; Orrock et al., 2015). For instance, predator-induced increases in prey stress-associated hormones could be beneficial in some ways as a pre-emptive defense (e.g., readiness to fight or flee; Sapolsky et al., 2000), but not in others, such as chronic hormone elevations that take a physiological toll and reduce reproduction (e.g., Sheriff et al., 2009).

Here, we follow the standardized framework and terminology suggested by Peacor et al. (2020) for induced trait responses of prey to predation risk (RITRs), but include herbivores and parasites within this context in terms of potential effects on their victims without or prior to consumption. Critically, enemy RITRs are not interchangeable with NCEs. Rather, RITRs brought about by victim perception of increased natural enemy threat can result in NCEs if these reduce victim abundance or fitness through direct means (e.g., energy reallocation), or affect victim interactions with others in ways that reduce fitness indirectly (Peacor et al., 2020). In other words, all NCEs require costly RITRs, but not all RITRs lead to NCEs if these costs do not demonstrably reduce victim fitness or abundance. Additionally, victim trait alterations could affect the fitness and abundance of a third species, with possible cascading effects involving yet other species; these latter two consequences represent TMIEs (Peacor et al., 2020). To compare the potential for herbivores and parasites to cause NCEs for their plant and animal victims, respectively, it is thus necessary to first consider the scope and nature of RITRs.

We consider research on animal hosts first to highlight a major contrast with plant responses; namely, studies of induced responses to a perceived threat of parasitism have heavily focused on behavioral resistance. These defensive behaviors include those that reduce parasite encounter, or remove parasites before they can establish and incur costs (see reviews by Hart, 1990; Hart and Hart, 2018). Spatial avoidance behavior of hosts to parasite infectious stages, or to proxies such as feces, is well-documented. For instance, grazing mammals forego foraging near patches containing fecal matter (see reviews by Hutchings et al., 2000; Coulson et al., 2018), especially if the fecal material is relatively “fresh” (e.g., Hutchings et al., 1998). Such avoidance behavior can be well-matched to the species’ risk of infection by the parasites in question (Sharp et al., 2015; Weinstein et al., 2018b). There are many excellent examples of behavioral avoidance of parasites by animals (see reviews by Hart, 1990; Behringer et al., 2018); we have limited our discussion of this trait expression here given that adult plants obviously have little capacity for movement in order to avoid contact with herbivores.

Post-contact behavioral resistance by animals is also common, especially for those under attack by ectoparasites (Hart and Hart, 2018). Grooming to remove these parasites before they can establish a prolonged consumptive relationship is a particularly important defensive behavior. Self-grooming is seen in many potential hosts, from insects to mammals and birds (Mooring et al., 2004; Zhukovskaya et al., 2013; Bush and Clayton, 2018), and allo-grooming by members of the same species is also seen in various taxa (e.g., Akinyi et al., 2013). Also, interspecific mutualisms can be critical for ectoparasite removal. For instance, cleaner fish and shrimp are highly effective at removing a variety of ectoparasites from their clients (reviewed by Vaughan et al., 2017), with clients spending a considerable amount of time engaged in cleaning activities if heavily infected (e.g., Grutter, 2001). Here, the behavior of the host is critical in moving to, or remaining at, a cleaning station. Conversely, plants recruit their mutualists (enemies of herbivores) through chemical cues, and not by moving to them (see below).

Compared to parasite risk-induced behavioral changes, there are fewer studies of morphological or physiological trait alterations in animal hosts. As a result, relatively less is known about potential changes in such traits, but recent investigations are broadening our knowledge. For instance, the simple presence of parasites in the vicinity has been reported to alter metabolic activity in potential hosts. Drosophila exposed to parasite mites separated by a screen (i.e., no contact possible) increased their metabolic rate (Luong et al., 2017), and this was also seen in fish exposed to motile trematode infectious stages (Nadler et al., 2021). Conversely, larval amphibians with non-contact exposure to trematodes did not exhibit changes in hormones associated with a stress response (Marino et al., 2014).

In contrast to animals and parasite risk, it is not surprising that studies of RITRs in plants primarily involve morphology or physiology given the limited scope of plants for behavioral resistance in response to increased herbivory risk. Of these, changes in the levels of endogenous chemicals representing plant secondary metabolites (PSMs) are well-known (Chen, 2008; Carmona et al., 2011). These metabolites encompass a wide array of compounds, but many (e.g., alkaloids and terpenes) defend against herbivory via deterrent or toxic effects (reviews by Bennett and Wallsgrove, 1994; Fürstenberg-Hägg et al., 2013; Erb and Kliebenstein, 2020). In response to cues signaling early or imminent attack by herbivores (see preceding subsection), specific physiological pathways are rapidly activated in plants. The phytohormones jasmonic acid and salicylic acid play key roles, along with the VOC ethylene, triggering the transcription of various defense-related genes (detailed reviews by Howe and Jander, 2008; Fürstenberg-Hägg et al., 2013; Kant et al., 2015).

Beyond induced changes in chemicals such as secondary metabolites, plants that perceive an elevated risk of herbivory can initiate morphological trait alterations that increase their resistance. These include increasing leaf toughness and producing more trichomes to limit herbivore contact through mechanical interference (Fürstenberg-Hägg et al., 2013; Kant et al., 2015). However, it is important to note that cues signaling a threat of herbivory may not result in immediate trait changes, but rather, cause “priming” that allows for a rapid response if the threat continues or an actual attack begins (see Frost et al., 2008; Karban, 2011). This is similar to the “immune-priming” shown by insects if they are exposed to, but not successfully infected by, parasites (reviewed by Sheehan et al., 2020), or in response to cues signaling heightened infection risk, such as crowded conditions, a.k.a. density-dependent prophylaxis (see Wilson and Cotter, 2009).

While plants cannot engage in behavioral resistance to avoid herbivore encounter (but see Dicke, 2009), they still have effective ways to remove these before significant damage occurs. Just like certain animals trying to rid themselves of ectoparasites by soliciting assistance, plants can do so by involving another species. Notably, HIPVs released in response to herbivore attack are not only perceived by other plants, but are known to serve as signals to enemies of those herbivores, including parasitoids and predators (see reviews by Aljbory and Chen, 2018; Pearse et al., 2020). Such interactions among plants, herbivores, and enemies of herbivores represent well-established examples of enemy-related trophic cascades (see Turlings and Erb, 2018). Removal of herbivores by soliciting another species could thus be considered as a type of induced behavioral response by plants.

In highlighting key findings related to enemy RITRs for plant-herbivore and animal host-parasite systems, it is obvious that the traits primarily considered to date differ considerably, i.e., principally behaviors for animals, and morphology or physiology for plants. However, broad patterns can be informative when considering the potential for RITRs to cause NCEs; here we highlight select questions regarding relationships among defense components:

As detailed above, enemy RITRs must cause reductions in victim fitness or abundance to be considered as NCEs (Peacor et al., 2020). Based on these criteria, surprisingly few studies have actually demonstrated NCEs related to natural enemy presence, even for predator-prey interactions (Sheriff et al., 2020b). Various logistical hurdles make it difficult to directly assess how natural enemy presence affects victim fitness (reproduction, recruitment, and mortality), and especially abundance, for most systems (Sheriff et al., 2020b). However, inconsistency in terminology also poses problems because “non-consumptive effect” has been widely used to describe a trait change in a potential victim that occurs prior to actual meaningful consumption by a natural enemy (Peacor et al., 2020). In the absence of direct measures of victim fitness or abundance when evaluating the costs(s) of enemy RITRs, the strongest case for potential NCEs can thus be made when evaluating traits that serve as good proxies for fitness (e.g., condition or growth rate—Sheriff et al., 2020b).

Many studies have examined whether plants experience fitness reductions as a result of induced defensive responses to actual herbivory; however, those studies often consider costs by measuring traits correlated with fitness, especially growth or development (e.g., plant size and seed germination), or physiological aspects such as photosynthesis (see Cipollini et al., 2003; Züst and Agrawal, 2017). When evaluating herbivore NCEs on plants in response to heightened risk alone (i.e., no consumption), these same correlative traits should be relevant for inferring potential fitness costs. For instance, the growth of maize seedlings was significantly reduced if these were exposed to GLVs emitted by neighbors (Engelberth and Engelberth, 2019). In contrast, wild tobacco plants exposed to HIPVs emanating from damaged sagebrush actually produced more seeds relative to controls (Karban and Maron, 2002). This latter response might have been a form of terminal investment preceding herbivory.

Costs may occur through direct means, such as energy reallocation to herbivore resistance, or manifest as ecological or opportunity costs by altering inter- or intraspecific interactions (Cipollini et al., 2003). Notably, plants eavesdropping on HIPVs may undergo trait changes that make them inferior or superior competitors against the same or different species (reviewed by Dicke and Baldwin, 2010). Herbivore RITRs, such as increased lignin content after plant exposure to GLVs, can also affect plant susceptibility to pathogens and parasites (e.g., Kishimoto et al., 2006), thereby influencing plant fitness.

In terms of parasite RITRs in animals, very few studies have reported direct reductions in fitness or abundance. As previously mentioned, Drosophila show increased metabolic rates in the presence of physically-separated parasitic mites, and this caused reductions in both fly fecundity and longevity (Horn and Luong, 2018). Overall, it is likely that fitness costs (i.e., NCEs) are associated with changes in victim traits if the latter involve substantial energy use that cannot be compensated for, such as through increased feeding. With this in mind, it is probable that behavioral RITRs to parasite threat are associated with fitness costs. As individuals of many species forego foraging opportunities in order to reduce their chances of parasite encounter (e.g., Fritzsche and Allan, 2012; Koprivnikar and Penalva, 2015; Weinstein et al., 2018b), this avoidance may reduce energy intake—similar to predator effects (Peacor et al., 2020). More work is needed to determine whether such avoidance behaviors often have negative effects on direct fitness measures or reasonable proxies.

The fitness costs of enemy RITRs have been more straightforward to evaluate from plants than from animals. Direct negative effects on plant reproduction or population abundance as a result of herbivore RITRs have been reported (e.g., Yip et al., 2019), but net benefits have also been seen, such as for neighboring plants exposed to HIPVs (Karban et al., 2012). Fitness consequences in plants are easier to infer because good proxies are available (Cipollini et al., 2003). In contrast, relatively few studies have demonstrated parasite RITRs translating into NCEs for animals. Future investigations should specifically consider reasonable fitness correlates of RITRs, similar to plant-herbivore studies.

Our focus thus far has been on enemy RITRs in plant-herbivore and animal parasite-host systems in terms of their potential to cause NCEs, but we briefly note ways in which trait changes could have community-level consequences by affecting victim interactions with other species, i.e., trait-mediated indirect effects (TMIEs). Potential TMIEs related to parasite risk have been reviewed (Buck and Ripple, 2017), thus we limit our discussion here to noting the general pathways involved, and how these compare for plants and herbivores. One way in which parasite risk affects a third species is when altered foraging behavior by potential victims increases food resources for other consumers, especially competing species (Buck et al., 2018). For example, invasive ant species are often successful by dominating food resources through aggression; however, the presence of parasitoids that use the invasive ants as hosts alters the invaders’ foraging behaviors such that competing endemic ant species are no longer at a disadvantage (Feener, 2000).

When it comes to TMIEs broadly involving plant-herbivore interactions, most work has considered reductions in plant damage owing to altered herbivore behaviors when the natural enemies of these herbivores (predators and parasitoids) are recruited (e.g., Culshaw-Maurer et al., 2020). But enemy RITRs in plants themselves could also result in TMIEs. For instance, the negative effects of stinkbug predators on hornworm caterpillars were reduced if the latter consumed tomato plants that were induced to express high levels of jasmonate (Kaplan and Thaler, 2010). HIPVs released in response to herbivore attack are not only subject to eavesdropping by other plants, or useful in recruiting herbivore enemies—these cues can attract other herbivore species to the area, with implications for neighboring plants and herbivore competitive interactions (reviewed by Dicke and van Loon, 2000). Remarkably, plant HIPVs can even affect the reproduction of nearby herbivores by suppressing pheromone detection and mate location (Hatano et al., 2015). Lastly, different plant species can exhibit divergent trait changes when exposed to the same HIPVs, with either increased or decreased fitness, thereby influencing plant community composition (Freundlich and Frost, 2019).

One way in which plant-herbivore and animal host-parasite systems are distinct from prey-predator is that the latter has relatively distinct pre-consumption and consumption phases of the interaction, and limited potential for different avenues of adaptation by the victim (i.e., prey must engage in pre-emptive defenses or risk having a fitness of zero). In contrast, plant and animal victims of herbivores and parasites, respectively, can experience a “gray zone” in terms of a post-contact time period during which NCEs may occur while their enemies try to establish feeding, and have not yet altered host energy balance (Buck and Ripple, 2017). In other words, NCEs could frequently occur post-contact for these two natural enemy systems, whereas this seems unlikely for prey-predator interactions (i.e., consumption begins immediately after contact). Given this possibility for post-contact NCEs, it will be important to standardize whether the definition of NCEs should be restricted to pre-encounter influences by parasites and herbivores. To aid in this, it would be very useful to conduct studies that specifically look for costly trait alterations during this gray zone period, as well as develop some criteria to define a shift from NCEs to CEs (Buck and Ripple, 2017). Such criteria will have to include the extent to which the trait response can be viewed as defensive (i.e., adaptive) rather than simply a side effect of consumption.

When considering how plants and animals may perceive their herbivore and parasite enemies, respectively, it would appear that both victim types commonly rely on chemical cues which either directly emanate from the enemy (kairomones), or are released by conspecifics under attack (alarm cues). Because invertebrate herbivores and parasite infectious stages are likely difficult for their victims to perceive through audiovisual cues, as compared to prey which often can detect predators in this manner (Brown et al., 1999; Wirsing et al., 2021), reliance on chemical signals in both victim systems is not surprising. Notably, many studies of parasite avoidance behavior in animals have been conducted with aquatic species, and chemical cues are particularly well-suited for this type of environment (Behringer et al., 2018). Terrestrial animals also could be adept at detecting infection risk through chemical means, thus the greater number of examples from aquatic systems may reflect relative study effort rather than say anything about a victim’s ability based on its habitat. Further work with terrestrial animal host-parasite systems is necessary for a broader comparison to chemical cues used by plants for herbivore detection.

In terms of enemy RITRs, the focus to date has been on behavioral alterations shown by animals in response to perceived parasite threat. For obvious reasons, studies of trait changes in plants have instead considered various aspects of morphology and physiology. Some of these are directly relevant for evaluating the cost(s) of induced resistance in terms of reduced victim fitness or abundance, with other measures often serving as good proxies (e.g., plant growth or development). It will be essential to obtain similarly relevant measures for animals in order to determine how parasites may exact costs irrespective of actual consumption. This represents a particularly critical and urgent area for future work.

Studies of plant-herbivore interactions are increasingly utilizing genetic and molecular approaches to examine how cues signaling enemy risk may translate into trait changes (Johnson, 2011; Züst and Agrawal, 2017). Such tools for animal host-parasite work would be very useful, not only to better understand the mechanistic pathways involved in RITRs, but also potential alterations of many traits at once (e.g., via pleiotropic genes). As plants often exhibit “defense syndromes” for resistance-related traits (Agrawal and Fishbein, 2006), such possibilities should be investigated for parasite RITRs in animals. Using “synthetic” means by which to induce herbivore risk-related responses in plants has been an important tool in this area of study (Cipollini et al., 2003; Howe and Jander, 2008)—this approach could prove useful for examining animal responses to parasite risk if the precise cues used to gauge risk can be identified. Animal host-parasite work should further consider variation among natural populations in terms of RITRs, as well as potential differences between domesticated and wild species—both of which have been explored with plants (Cipollini et al., 2003; Züst and Agrawal, 2017).

For both natural enemy risk perception and RITRs, there may be particular value in comparing plant-herbivore and animal-host parasite systems comprised of colonies, particularly if individuals are kin-related. Various woody and herbaceous flowering plants can form clonal colonies (Fischer and Van Kleunen, 2001). While clonal colonies of animals are less common (e.g., some sponges and corals), social insects have a high degree of relatedness, and engage in a number of cooperative hygienic behaviors to protect the colony against parasites and pathogens (Wilson-Rich et al., 2009). In such cases, it would be valuable for related conspecifics to quickly perceive and respond to chemical cues released by individuals under attack. What might otherwise be considered as “eavesdropping” by other individuals so as to gain a defensive advantage could actually be beneficial (Karban, 2011), making this type of enemy-associated cue particularly important in the context of RITRs and subsequent NCEs. Group-living plants and animals, especially those often surrounded by close kin with similar vulnerability, may thus be particularly sensitive to conspecific-generated cues signaling enemy presence, and also more likely to display RITRs.

When considering the chain of events leading to NCEs, sessile animals (e.g., bivalves) may particularly share key features with plants in terms of how these two victim types perceive parasitism or herbivory risk, respectively. Such comparisons have proposed for their anti-predator defenses (Sheriff et al., 2020a), and likely apply to other natural enemies. Notably, many sessile animals have limited audiovisual sensory capability; just like plants, this may make them relatively reliant on chemical cues signaling parasite risk, or especially sensitive to even slight contact. For instance, blue mussels quickly retract their filtering siphons and close their shells in the presence of free-swimming trematode infectious stages, but it is not clear to which enemy-related cues they react (Selbach and Mouritsen, 2020).

Throughout, we discussed the likelihood of documenting costly pre-emptive defenses through trait changes in response to natural enemy cues in two victim systems (plant-herbivore and animal-parasite). We showed that enemy cues in those two systems are seemingly detected, and invoke RITRs that can be considered as pre-emptive defense. We currently do not know how frequent or costly these are relative to RITRs of prey, or to consumption-induced trait changes of the same two victim systems under study. Costly pre-emptive defenses by prey, and consumption-based defensive responses of plants and animal hosts to herbivores and parasites, respectively, are well-documented in comparison. Future work should thus consider the interplay between pre-emptive (risk-induced) and consumption-induced trait changes in the two victim systems, particularly as it relates to applying NCE knowledge for natural enemy control (e.g., Culshaw-Maurer et al., 2020), and the population viability of focal organisms in habitats where herbivore or parasite threat may be either diminished or heightened (e.g., Rusch et al., 2013; Gottdenker et al., 2014).

Looking for both parallels and contrasts between different enemy-victim systems is valuable to advance the general field of natural enemy ecology, especially for understanding the importance of NCEs for victim populations and the importance of TMIEs for affecting communities. NCEs may be more common in particular victim-enemy systems based on their shared inherent biological potential for perceiving and responding to altered risk; however, certain ecological or evolutionary factors also could drive NCE occurrence. For instance, co-evolved species could be more likely to exhibit NCEs than novel consumer-victim systems, as seen for predator-prey interactions (Sih et al., 2010). Valuable insights regarding natural enemy ecology, especially the “ecology of fear,” have been gained by integrating concepts and knowledge for animal host-parasite and prey-predator interactions (e.g., Raffel et al., 2008; Buck et al., 2018; Weinstein et al., 2018a; Daversa et al., 2021). By broadly synthesizing and contrasting key aspects of plant and animal trait responses to the risks posed by herbivores and parasites, respectively, we hope that similar benefits have been seen in terms of advancing our understanding of NCEs.