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The Behavioral Ecology of Venom

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A special issue of Toxins (ISSN 2072-6651).

Deadline for manuscript submissions: closed (31 October 2021) | Viewed by 52702

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Prof. Dr. William K. Hayes

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Guest Editor

Department of Earth and Biological Sciences, Loma Linda University, Loma Linda, CA, USA
Interests: predator-prey relationships; behavioral ecology of toxins; coevolution; interspecific communication; aposematism; aversive conditioning; mimicry; risk assessment between venomous arthropods and and their enemies; conservation biology; science pedagogy

Prof. Dr. Matthew P. Rowe

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Guest Editor

Department of Biology, University of Oklahoma, Norman, OK 73019, USA
Interests: predator-prey relationships, coevolution, interspecific communication, aposematism, aversive conditioning, mimicry, and risk assessment of venomous arthropods and grasshopper mice; conservation biology; science pedagogy

Special Issue Information

Dear Colleagues,

The theme of this Special Issue is the behavioral ecology of all things that relate to venomous animals, which, by definition, are critters that inject their toxins by biting or stinging another organism.

Biting and stinging are behaviors, of course, and there is a growing literature detailing how and when venomous animals deliver their toxins, in both predatory and defensive contexts. Because venom production has both energetic and ecological costs, it is not surprising that venomous animals as different as scorpions and snakes meter their venom when attempting to deter a predator, injecting more of the precious slurry, or a more potent and expensive version thereof, when predatory risk is higher. These taxa and other groups also meter their venom offensively by injecting less venom, or none, when a prey item can easily be subdued. Venom can also be used for other functions, such as communication, reproduction, intraspecific and interspecific competition, and antimicrobial immunity. Bees spray their venom to alert others of a threat to the hive; male scorpions sting their mates during courtship; anemones sting their neighbors as they jostle for space; and ants spray venom on their nest and eggs to inhibit microbes.

Some animals acquire their toxins from others, either through their diet, or more perversely, via theft. Other animals, such as ants and social spiders, even use their venom cooperatively to procure larger meals than they could acquire individually. We welcome submissions, either reviews or original research, that add to our understanding of the behavior and ecology of venomous organisms themselves.

However, we want this Special Issue to be richer, more diverse, and thus more engaging than solely focusing on the behavior of venom producers. The prey of venomous organisms also behave so as not to be envenomated. Colonial ground squirrels, for example, adjust their mobbing behavior based on the rattling sounds of a rattlesnake enemy, responding more cautiously to the rattling from a larger, warmer, and more dangerous snake. Likewise, predators of venomous organisms also behave! When feeding on venomous scorpions, whiptail lizards repeatedly bite, shake, and throw a scorpion but simply bite and eat a non-venomous cricket. Thus, we encourage contributions exploring the behavior of any and all potential victims of envenomation, be they predators or prey.

But wait! We’re not done yet. There is yet another player in this community of critters interacting with a venomous member. These are the imitators, the mimics who benefit from their resemblance to a venomous organism, be they harmless hoverfly mimics of painful bumblebees, or benign milk snakes whose banding patterns of red, yellow, and black can easily be confused with the similar markings of potentially deadly coral snakes. While the behavior of such imposters themselves can be used to enhance their mimicry, as in the head flattening of gopher snakes when imitating rattlesnakes, it is the behavior of the predators, the dupes, that makes such mimicry possible. Behavior, thus, is integral to understanding mimicry complexes, and submissions on this topic would be welcomed.

Lastly, we would enjoy contributions from researchers studying animals that are frequently overlooked as being venomous, such as the hematophagous animals, the vampires. By most definitions, vampire bats, mosquitoes, biting flies, ticks, and assassin bugs are venomous, and they can have dramatic impacts on the evolution, ecology, and yes, even the behavior of their hosts. Original research or thoughtful reviews dealing with the behavioral ecology of any of these vampires or their targets would also be valued.

We look forward to a diverse and engaging volume dealing broadly with the behavioral ecology of venom!

With warm regards,

Prof. Dr. William K. Hayes
Prof. Dr. Matthew P. Rowe
Guest Editors

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Keywords

Venom
Toxin
Behavior
Ecology
Venom metering
Risk assessment
Bites and stings
Predatory and defensive
Mimicry
Hematophagous

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Published Papers (9 papers)

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Research

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15 pages, 1130 KiB

Open AccessArticle

Risky Business: The Function of Play in a Venomous Mammal—The Javan Slow Loris (Nycticebus javanicus)

by Meg Barrett, Marco Campera, Thais Q. Morcatty, Ariana V. Weldon, Katherine Hedger, Keely Q. Maynard, Muhammad Ali Imron and K. A. I. Nekaris

Toxins 2021, 13(5), 318; https://doi.org/10.3390/toxins13050318 - 28 Apr 2021

Cited by 12 | Viewed by 4690

Abstract

Immature mammals require opportunities to develop skills that will affect their competitive abilities and reproductive success as adults. One way these benefits may be achieved is through play behavior. While skills in developing use of tusks, antlers, and other weapons mammals have been linked to play, play in venomous animals has rarely been studied. Javan slow lorises (Nycticebus javanicus) use venom to aid in intraspecific competition, yet whether individuals use any behavioral mechanisms to develop the ability to use venom remains unclear. From April 2012 to December 2020, we recorded 663 play events and studied the factors influencing the frequency of play and the postures used during play in wild Javan slow lorises. Regardless of the presence of siblings, two thirds of play partners of young slow lorises were older and more experienced adults. Young lorises engaged in riskier behaviors during play, including using more strenuous postures and playing more in riskier conditions with increased rain and moonlight. We found that play patterns in immature lorises bear resemblance to venom postures used by adults. We suggest that play functions to train immature lorises to deal with future unexpected events, such as random attacks, as seen in other mammalian taxa with weapons. Given the importance of venom use for highly territorial slow lorises throughout their adult lives and the similarities between venom and play postures, we cannot rule out the possibility that play also prepares animals for future venomous fights. We provide here a baseline for the further exploration of the development of this unique behavior in one of the few venomous mammals. Full article

(This article belongs to the Special Issue The Behavioral Ecology of Venom)

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8 pages, 1168 KiB

Open AccessCommunication

Electric Eels Wield a Functional Venom Analogue

by Kenneth C. Catania

Toxins 2021, 13(1), 48; https://doi.org/10.3390/toxins13010048 - 10 Jan 2021

Cited by 1 | Viewed by 5515

Abstract

In this paper, I draw an analogy between the use of electricity by electric eels (Electrophorus electricus) to paralyze prey muscles and the use of venoms that paralyze prey by disrupting the neuromuscular junction. The eel’s strategy depends on the recently discovered ability of eels to activate prey motor neuron efferents with high-voltage pulses. Usually, eels use high voltage to cause brief, whole-body tetanus, thus preventing escape while swallowing prey whole. However, when eels struggle with large prey, or with prey held precariously, they often curl to bring their tail to the opposite side. This more than doubles the strength of the electric field within shocked prey, ensuring maximal stimulation of motor neuron efferents. Eels then deliver repeated volleys of high-voltage pulses at a rate of approximately 100 Hz. This causes muscle fatigue that attenuates prey movement, thus preventing both escape and defense while the eel manipulates and swallows the helpless animal. Presumably, the evolution of enough electrical power to remotely activate ion channels in prey efferents sets the stage for the selection of eel behaviors that functionally “poison” prey muscles. Full article

(This article belongs to the Special Issue The Behavioral Ecology of Venom)

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18 pages, 1357 KiB

Open AccessArticle

Physiological Stress Integrates Resistance to Rattlesnake Venom and the Onset of Risky Foraging in California Ground Squirrels

by Matthew L. Holding, Breanna J. Putman, Lauren M. Kong, Jennifer E. Smith and Rulon W. Clark

Toxins 2020, 12(10), 617; https://doi.org/10.3390/toxins12100617 - 27 Sep 2020

Cited by 11 | Viewed by 4919

Abstract

Using venom for predation often leads to the evolution of resistance in prey. Understanding individual variation in venom resistance is key to unlocking basic mechanisms by which antagonistic coevolution can sustain variation in traits under selection. For prey, the opposing challenges of predator avoidance and resource acquisition often lead to correlated levels of risk and reward, which in turn can favor suites of integrated morphological, physiological and behavioral traits. We investigate the relationship between risk-sensitive behaviors, physiological resistance to rattlesnake venom, and stress in a population of California ground squirrels. For the same individuals, we quantified foraging decisions in the presence of snake predators, fecal corticosterone metabolites (a measure of “stress”), and blood serum inhibition of venom enzymatic activity (a measure of venom resistance). Individual responses to snakes were repeatable for three measures of risk-sensitive behavior, indicating that some individuals were consistently risk-averse whereas others were risk tolerant. Venom resistance was lower in squirrels with higher glucocorticoid levels and poorer body condition. Whereas resistance failed to predict proximity to and interactions with snake predators, individuals with higher glucocorticoid levels and in lower body condition waited the longest to feed when near a snake. We compared alternative structural equation models to evaluate alternative hypotheses for the relationships among stress, venom resistance, and behavior. We found support for stress as a shared physiological correlate that independently lowers venom resistance and leads to squirrels that wait longer to feed in the presence of a snake, whereas we did not find evidence that resistance directly facilitates latency to forage. Our findings suggest that stress may help less-resistant squirrels avoid a deadly snakebite, but also reduces feeding opportunities. The combined lethal and non-lethal effects of stressors in predator–prey interactions simultaneously impact multiple key traits in this system, making environmental stress a potential contributor to geographic variation in trait expression of toxic predators and resistant prey. Full article

(This article belongs to the Special Issue The Behavioral Ecology of Venom)

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22 pages, 2683 KiB

Open AccessArticle

Risk Assessment and the Effects of Refuge Availability on the Defensive Behaviors of the Southern Unstriped Scorpion (Vaejovis carolinianus)

by David R. Nelsen, Emily M. David, Chad N. Harty, Joseph B. Hector and Aaron G. Corbit

Toxins 2020, 12(9), 534; https://doi.org/10.3390/toxins12090534 - 20 Aug 2020

Cited by 6 | Viewed by 3795

Abstract

Selection should favor individuals that acquire, process, and act on relevant environmental signals to avoid predation. Studies have found that scorpions control their use of venom: both when it is released and the total volume expelled. However, this research has not included how a scorpion’s awareness of environmental features influences these decisions. The current study tested 18 Vaejovis carolinianus scorpions (nine females and nine males) by placing them in circular arenas supplied with varying numbers (zero, two, or four) of square refuges and by tracking their movements overnight. The following morning, defensive behaviors were elicited by prodding scorpions on the chelae, prosoma, and metasoma once per second over 90 s. We recorded stings, venom use, chelae pinches, and flee duration. We found strong evidence that, across all behaviors measured, V. carolinianus perceived prods to the prosoma as more threatening than prods to the other locations. We found that stinging was a common behavior and became more dominant as the threat persisted. Though tenuous, we found evidence that scorpions’ defensive behaviors changed based on the number of refuges and that these differences may be sex specific. Our findings suggest that V. carolinianus can assess risk and features of the local environment and, therefore, alter their defensive strategies accordingly. Full article

(This article belongs to the Special Issue The Behavioral Ecology of Venom)

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9 pages, 1108 KiB

Open AccessCommunication

Behavioral, Physiological, Demographic and Ecological Impacts of Hematophagous and Endoparasitic Insects on an Arctic Ungulate

by Kyle Joly, Ophélie Couriot, Matthew D. Cameron and Eliezer Gurarie

Toxins 2020, 12(5), 334; https://doi.org/10.3390/toxins12050334 - 20 May 2020

Cited by 20 | Viewed by 5220

Abstract

Animals that deliver a toxic secretion through a wound or to the body surface without a wound are considered venomous and toxungenous, respectively. Hematophagous insects, such as mosquitoes (Aedes spp.), meet the criteria for venomous, and some endoparasitic insects, such as warble flies (Hypoderma tarandi), satisfy the definition for toxungenous. The impacts of these insects on their hosts are wide ranging. In the Arctic, their primary host is the most abundant ungulate, the caribou (Rangifer tarandus). The most conspicuous impacts of these insects on caribou are behavioral. Caribou increase their movements during peak insect harassment, evading and running away from these parasites. These behavioral responses scale up to physiological effects as caribou move to less productive habitats to reduce harassment which increases energetic costs due to locomotion, reduces nutrient intake due to less time spent foraging, and can lead to poorer physiological condition. Reduced physiological condition can lead to lower reproductive output and even higher mortality rates, with the potential to ultimately affect caribou demographics. Caribou affect all trophic levels in the Arctic and the processes that connect them, thus altering caribou demographics could impact the ecology of the region. Broadening the definitions of venomous and toxungenous animals to include hematophagous and endoparasitic insects should not only generate productive collaborations among toxinologists and parasitologists, but will also lead to a deeper understanding of the ecology of toxic secretions and their widespread influence. Full article

(This article belongs to the Special Issue The Behavioral Ecology of Venom)

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17 pages, 1792 KiB

Open AccessArticle

Defensive Venoms: Is Pain Sufficient for Predator Deterrence?

by Crystal N. Niermann, Travis G. Tate, Amber L. Suto, Rolando Barajas, Hope A. White, Olivia D. Guswiler, Stephen M. Secor, Ashlee H. Rowe and Matthew P. Rowe

Toxins 2020, 12(4), 260; https://doi.org/10.3390/toxins12040260 - 17 Apr 2020

Cited by 17 | Viewed by 6976

Abstract

Pain, though unpleasant, is adaptive in calling an animal’s attention to potential tissue damage. A long list of animals representing diverse taxa possess venom-mediated, pain-inducing bites or stings that work by co-opting the pain-sensing pathways of potential enemies. Typically, such venoms include toxins that cause tissue damage or disrupt neuronal activity, rendering painful stings honest indicators of harm. But could pain alone be sufficient for deterring a hungry predator? Some venomologists have argued “no”; predators, in the absence of injury, would “see through” the bluff of a painful but otherwise benign sting or bite. Because most algogenic venoms are also toxic (although not vice versa), it has been difficult to disentangle the relative contributions of each component to predator deterrence. Southern grasshopper mice (Onychomys torridus) are voracious predators of arthropods, feeding on a diversity of scorpion species whose stings vary in painfulness, including painful Arizona bark scorpions (Centruroides sculpturatus) and essentially painless stripe-tailed scorpions (Paravaejovis spinigerus). Moreover, southern grasshopper mice have evolved resistance to the lethal toxins in bark scorpion venom, rendering a sting from these scorpions painful but harmless. Results from a series of laboratory experiments demonstrate that painful stings matter. Grasshopper mice preferred to prey on stripe-tailed scorpions rather than bark scorpions when both species could sting; the preference disappeared when each species had their stingers blocked. A painful sting therefore appears necessary for a scorpion to deter a hungry grasshopper mouse, but it may not always be sufficient: after first attacking and consuming a painless stripe-tailed scorpion, many grasshopper mice went on to attack, kill, and eat a bark scorpion even when the scorpion was capable of stinging. Defensive venoms that result in tissue damage or neurological dysfunction may, thus, be required to condition greater aversion than venoms causing pain alone. Full article

(This article belongs to the Special Issue The Behavioral Ecology of Venom)

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Review

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12 pages, 267 KiB

Open AccessReview

Venom and Social Behavior: The Potential of Using Spiders to Evaluate the Evolution of Sociality under High Risk

by Laura Gatchoff and Laura R. Stein

Toxins 2021, 13(6), 388; https://doi.org/10.3390/toxins13060388 - 28 May 2021

Cited by 1 | Viewed by 4356

Abstract

Risks of sociality, including competition and conspecific aggression, are particularly pronounced in venomous invertebrates such as arachnids. Spiders show a wide range of sociality, with differing levels of cannibalism and other types of social aggression. To have the greatest chance of surviving interactions with conspecifics, spiders must learn to assess and respond to risk. One of the major ways risk assessment is studied in spiders is via venom metering, in which spiders choose how much venom to use based on prey and predator characteristics. While venom metering in response to prey acquisition and predator defense is well-studied, less is known about its use in conspecific interactions. Here we argue that due to the wide range of both sociality and venom found in spiders, they are poised to be an excellent system for testing questions regarding whether and how venom use relates to the evolution of social behavior and, in return, whether social behavior influences venom use and evolution. We focus primarily on the widow spiders, Latrodectus, as a strong model for testing these hypotheses. Given that successful responses to risk are vital for maintaining sociality, comparative analysis of spider taxa in which venom metering and sociality vary can provide valuable insights into the evolution and maintenance of social behavior under risk. Full article

(This article belongs to the Special Issue The Behavioral Ecology of Venom)

26 pages, 4341 KiB

Open AccessReview

Venom Use in Eulipotyphlans: An Evolutionary and Ecological Approach

by Krzysztof Kowalski and Leszek Rychlik

Toxins 2021, 13(3), 231; https://doi.org/10.3390/toxins13030231 - 22 Mar 2021

Cited by 8 | Viewed by 7117

Abstract

Venomousness is a complex functional trait that has evolved independently many times in the animal kingdom, although it is rare among mammals. Intriguingly, most venomous mammal species belong to Eulipotyphla (solenodons, shrews). This fact may be linked to their high metabolic rate and a nearly continuous demand of nutritious food, and thus it relates the venom functions to facilitation of their efficient foraging. While mammalian venoms have been investigated using biochemical and molecular assays, studies of their ecological functions have been neglected for a long time. Therefore, we provide here an overview of what is currently known about eulipotyphlan venoms, followed by a discussion of how these venoms might have evolved under ecological pressures related to food acquisition, ecological interactions, and defense and protection. We delineate six mutually nonexclusive functions of venom (prey hunting, food hoarding, food digestion, reducing intra- and interspecific conflicts, avoidance of predation risk, weapons in intraspecific competition) and a number of different subfunctions for eulipotyphlans, among which some are so far only hypothetical while others have some empirical confirmation. The functions resulting from the need for food acquisition seem to be the most important for solenodons and especially for shrews. We also present several hypotheses explaining why, despite so many potentially beneficial functions, venomousness is rare even among eulipotyphlans. The tentativeness of many of the arguments presented in this review highlights our main conclusion, i.e., insights regarding the functions of eulipotyphlan venoms merit additional study. Full article

(This article belongs to the Special Issue The Behavioral Ecology of Venom)

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30 pages, 37773 KiB

Open AccessReview

Distribution, Ecology, Chemistry and Toxicology of Plant Stinging Hairs

by Hans-Jürgen Ensikat, Hannah Wessely, Marianne Engeser and Maximilian Weigend

Toxins 2021, 13(2), 141; https://doi.org/10.3390/toxins13020141 - 13 Feb 2021

Cited by 17 | Viewed by 8545

Abstract

Plant stinging hairs have fascinated humans for time immemorial. True stinging hairs are highly specialized plant structures that are able to inject a physiologically active liquid into the skin and can be differentiated from irritant hairs (causing mechanical damage only). Stinging hairs can be classified into two basic types: Urtica-type stinging hairs with the classical “hypodermic syringe” mechanism expelling only liquid, and Tragia-type stinging hairs expelling a liquid together with a sharp crystal. In total, there are some 650 plant species with stinging hairs across five remotely related plant families (i.e., belonging to different plant orders). The family Urticaceae (order Rosales) includes a total of ca. 150 stinging representatives, amongst them the well-known stinging nettles (genus Urtica). There are also some 200 stinging species in Loasaceae (order Cornales), ca. 250 stinging species in Euphorbiaceae (order Malphigiales), a handful of species in Namaceae (order Boraginales), and one in Caricaceae (order Brassicales). Stinging hairs are commonly found on most aerial parts of the plants, especially the stem and leaves, but sometimes also on flowers and fruits. The ecological role of stinging hairs in plants seems to be essentially defense against mammalian herbivores, while they appear to be essentially inefficient against invertebrate pests. Stinging plants are therefore frequent pasture weeds across different taxa and geographical zones. Stinging hairs are usually combined with additional chemical and/or mechanical defenses in plants and are not a standalone mechanism. The physiological effects of stinging hairs on humans vary widely between stinging plants and range from a slight itch, skin rash (urticaria), and oedema to sharp pain and even serious neurological disorders such as neuropathy. Numerous studies have attempted to elucidate the chemical basis of the physiological effects. Since the middle of the 20th century, neurotransmitters (acetylcholine, histamine, serotonin) have been repeatedly detected in stinging hairs of Urticaceae, but recent analyses of Loasaceae stinging hair fluids revealed high variability in their composition and content of neurotransmitters. These substances can explain some of the physiological effects of stinging hairs, but fail to completely explain neuropathic effects, pointing to some yet unidentified neurotoxin. Inorganic ions (e.g., potassium) are detected in stinging hairs and could have synergistic effects. Very recently, ultrastable miniproteins dubbed “gympietides” have been reported from two species of Dendrocnide, arguably the most violently stinging plant. Gympietides are shown to be highly neurotoxic, providing a convincing explanation for Dendrocnide toxicity. For the roughly 648 remaining stinging plant species, similarly convincing data on toxicity are still lacking. Full article

(This article belongs to the Special Issue The Behavioral Ecology of Venom)

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