Timber Rattlesnakes (Crotalus horridus) Use Chemical Cues to Select Ambush Sites

Chemicals left by organisms moving through the environment are used by other organisms to mediate interspecific interactions. Most studies of chemical eavesdropping focus on prey responding to chemical cues from predators, despite the fact that chemical cues are frequently used by predators as a source of information about prey. Crotalus horridus uses a foraging strategy that is widespread among sedentary predators: the snake chooses a site where it is likely to encounter prey and remains immobile for many hours. I investigated this ambush hunting behavior in captive-raised timber rattlesnakes and provide evidence that sit-and-wait predators may discriminate among prey chemical cues, even when they have no prior experience with the prey. Snakes explored chemical cues with chemosensory behaviors, and more frequently adopted a stereotyped ambush foraging posture toward chemical cues from prey sympatric with their population of origin than either allopatric prey or sympatric nonprey species that are eaten by other viperids. These results support the notion that intra- and interspecific variation in diet may be mediated proximally by innate recognition of cues from particular prey items. This system also describes a bioassay that may be used in the isolation and identification of prey-derived kairomones. Studies such as this can be used to determine more realistic parameters for models of predator-prey interaction and foraging behavior that involve secretive, less active predators.     

The role of olfaction in chemosensory-based predator recognition in the fathead minnow,Pimephales promelas

Solitary fathead minnows (Pimephales promelas) were rendered anosmic and exposed to chemical stimuli from a predatory northern pike (Esox lucius) to determine the role of olfaction in the minnow's ability to recognize predators on the basis of chemical stimuli. Anosmic fish did not respond to the pike stimuli with a typical fright reaction, while control fish, with intact olfactory receptors, did. These results demonstrate that the olfactory system is necessary for the ability of fathead minnows to recognize northern pike as a predator and that the gustatory and single-celled chemosensory systems are not sufficient for this recognition in the absence of olfactory input. Olfactory impairment was behaviorally confirmed by exposing minnows to alarm substance (Schreckstoff).     

Tasty but Protected—First Evidence of Chemical Defense in Oribatid Mites

Oribatid mites (Acari, Oribatida) represent one of the most abundant and speciose groups of microarthropods in the decomposer food webs of soils, but little is known of their top-down regulation by predators. Oribatids are relatively long-lived and have numerous morphological defensive adaptations, and so have been proposed to live in ‘enemy-free space’. Most also possess a pair of large exocrine oil glands that produce species-specific mixtures of hydrocarbons, terpenes, aromatics, and alkaloids with presumably allomonal functions, although their adaptive value has never been tested empirically. We developed a protocol that discharges the oil glands of the model oribatid species, Archegozetes longisetosus. and offered ‘disarmed’ individuals as prey to polyphagous Stenus beetles (Staphylinidae), using untreated mites as controls. Stenus juno fed on disarmed mites with behavioral sequences and success rates similar to those observed when they prey on springtails, a common prey. In contrast, mites from the control group with full glands were almost completely rejected; contact with the gland region elicited a strong reaction and cleaning behavior in the beetle. This is the first evidence of an adaptive value of oribatid mite oil gland secretions for chemical defense. The protocol of discharging oil glands should facilitate future studies on top-down control of oribatid mites that aim to differentiate between morphological and chemical aspects of defensive strategies.     

Attack cone avoidance during predator inspection visits by wild finescale dace (Phoxinus neogaeus): the effects of predator diet

When confronted by potential predators, many prey fishes engage in predator inspection behavior. Previous authors have argued that by selectively avoiding the predator's head during an inspection visit (attack cone avoidance), individual inspectors may reduce their local risk of predation. In field trials, we investigated the effects of predator diet cues on the presence of attack cone avoidance during predator inspection visits. Wild, free-ranging finescale dace (Phoxinus neogaeus) were exposed to the combined cues of a model predator and a distilled water control or the odor of a yellow perch (Perca flavescens) fed dace (with alarm pheromone), swordtail (Xiphophorus helleri) (lacking Ostariophysan alarm pheromone), or perch that were food deprived for four days. Finescale dace modified their predator inspection behavior following exposure to the odor of a perch fed dace (fewer dace present, reduced frequency of inspections, and an increased per capita inspection rate) compared to those exposed to the odor of a perch fed swordtails, perch that were food deprived, or a distilled water control. In addition, dace inspected the tail region more often only when the model predator was paired with the odor of a perch fed dace. In all other treatments, dace inspected the head region of the model predator more often. These data suggest that attack cone avoidance of inspecting prey fishes may be more likely to occur in high-risk situations, such as in the presence of conspecific alarm pheromones in the diet of potential predators.     

Acquired Predator Recognition by Fathead Minnows: Influence of Habitat Characteristics on Survival

In this study we conditioned fathead minnows (Pimephales promelas) to recognize the odor of a perch (Perca flavescens) by exposing them to perch odor coupled with minnow alarm cue. We then staged encounters between the predator and prey in order to assess whether the predator odor training had any effect on survival of the prey. We tested for a survival effect in the presence and absence of shelter. Our results indicate that fish trained with alarm signals to recognize predators gained a survival benefit during staged encounters with a predator and that habitat characteristics influenced the survival of conditioned fish.     

Chemical labeling of northern pike (Esox lucius) by the alarm pheromone of fathead minnows (Pimephales promelas)

In previous experiments, chemical stimuli from northern pike (Esox lucius) elicited fright responses from pike-naive fathead minnows (Pimephales promelas) only if the pike had recently eaten conspecific minnows. We used a behavioral assay to determine if the fright response is the result of the incorporation of the minnow alarm pheromone into the chemical signature of the pike. Because the alarm substance cells (epidermal club cells) of fathead minnows are seasonally lost by males, we used chemical stimuli from pike that had eaten breeding male minnows as a control stimulus. In independent laboratory and field experiments, pike-naive minnows exhibited fright reactions (e.g., increased shelter use, avoidance) when exposed to water from tanks containing pike that had eaten nonbreeding fatheads (with alarm substance cells), but not to water from tanks containing pike that had eaten breeding male fatheads (without alarm substance cells). These data indicate that the fathead minnow alarm pheromone chemically labels northern pike as dangerous to pike-naive receivers.     

Effect of predator diet on life history shifts of red-legged frogs,Rana aurora

Larval red-legged frogs (Rana aurora) are known to exhibit antipredator behavior in response to both chemical alarm cues released from injured conspecifics and chemical cues of predators. In some cases, the response to predators is dependent on the predator's diet. In this experiment, we tested whether long-term exposure to predator chemical cues and alarm cues resulted in alteration of life history characteristics of red-legged frogs. We raised groups of tadpoles in the presence of chemical cues of predators that were either fed conspecifics or heterospecific caddis-fly larvae, chemical cues of injured conspecifics, or a no-cue control. Tadpoles raised in the presence of either a predator fed conspecifics or cues of injured conspecifics metamorphosed earlier and at a smaller size than those exposed to predators fed heterospecifics or the no-cue control. The result suggests that red-legged frogs exhibit a life history shift in response to predatory cues and that this response is dependent on the diet of predators.     

Avoidance response of juvenile Pacific treefrogs to chemical cues of introduced predatory bullfrogs

Bullfrogs (Rana catesbeiana), native to eastern North America, were introduced into Oregon in the 1930's. Bullfrogs are highly efficient predators that are known to eat a variety of prey including other amphibians. In laboratory experiments, we investigated whether juvenile Pacific treefrogs (Hyla regilla) recognize adult bullfrogs as a predatory threat. The ability of prey animals to acquire recognition of an introduced predator has important implications for survival of the prey. We found that treefrogs from a population that co-occurred with bullfrogs showed a strong avoidance of chemical cues of bullfrogs. In contrast, treefrogs from a population that did not co-occur with bullfrogs, did not respond to the bullfrog cues. Additional experiments showed that both populations of treefrogs use chemical cues to mediate predation risk. Treefrogs from both populations avoided chemical alarm cues from injured conspecifics.     

Chemical discrimination by tongue-flicking in lizards: A review with hypotheses on its origin and its ecological and phylogenetic relationships

Tongue-flicking is a synapomorphy of squamate reptiles functioning to sample chemicals for vomerolfactory analysis, which became possible in primitive squamates when ducts opened from the vomeronasal organs to the roof of the mouth. Extant iguanian lizards in families that do not use the tongue to sample chemical prey cues prior to attack partially protrude it in two feeding contexts: during capture by lingual prehension and after oral contact with prey. These lizards do not exhibit strike-induced chemosensory searching. Lingual prey prehension is present in iguanian lizards and inSphenodon, the sister taxon of Squamata. During attempts to capture prey, the tongues of primitive squamates inevitably made incidental contact with environmental substrates bearing chemicals deposited by prey, conspecifics, and predators. Such contact presumably induced selection for tongue-flicking and ability to identify biologically important chemicals. Most iguanian lizards are ambush foragers that use immobility as a major antipredatory defense. Because tongue-flicking at an ambush post would not allow chemical search beyond the vicinity of the head and would render them easier for predators and prey to detect, typical iguanians tongue-flick neither while foraging nor to identify predators. They do detect pheromones by tongue-flicking. Scleroglossan lizards are typically active foragers that rely on speed to escape. Being freer to move the tongue, they have evolved lingual sampling allowing detection of chemical cues of conspecifics, predators, and prey, as well as strike-induced chemosensory searching, some can follow pheromone trails by tongue-flicking. Some families have lingual morphology and behavior specialized for chemosensory sampling. In varanids and snakes, the taxa showing the greatest lingual specialization, additional prey-related chemosensory behaviors have evolved. In iguanian and scleroglossan families that have secondarily adopted the foraging mode typical of the other taxon, prey chemical discrimination involving tongue-flicking and strike-induced chemosensory searching are typical for the foraging mode rather than the taxon. Because foraging mode and state of prey chemical discrimination are stable within squamate families and to a large extent in higher taxa, both features have been retained from the ancestral condition in most families. However, in three cases in which foraging mode has changed from its ancestral state, the state of prey chemical discrimination has also changed, indicating that prey chemical discrimination is adaptively adjusted to foraging mode. Indeed, acquisition of lingually mediated prey chemical discrimination may have made feasible the evolution of active foraging, which in turn appears to have profoundly influenced the further evolution of squamate chemosensory structures and behavior, placing a selective premium on features enhancing the tongue's efficiency as a chemical sampling device. The advent of tongue-flicking to sample prey chemicals and thus detect hidden prey may have allowed generalist (cruise) or ambush foragers, if early squamates were such, to become specialists in active foraging. Alternatively, if the common ancestors of squamates were active foragers, the adoption of ambush foraging would have selected against participation of the tongue in locating prey. Acting jointly, tongue-flicking and active foraging have had momentous consequences for squamate diversification. Specialization for active foraging would appear to have had ramifying effects on antipredatory defenses, body form, territoriality, mating systems, and reproductive physiology.     

Olfactory Experience Modifies Semiochemical Responses in a Bark Beetle Predator

A typical feature of forest insect pests is their tendency to undergo large fluctuations in abundance, which can jeopardize the persistence of their predaceous natural enemies. One strategy that these predators may adopt to cope with these fluctuations would be to respond to sensory cues for multiple prey species. Another possible adaptation to temporal variation in the prey community could involve the learning of prey cues and switching behavior. We conducted three experiments to investigate the ability of the generalist bark beetle predator Thanasimus dubius (F.) (Coleoptera: Cleridae) to respond to different prey signals and to investigate the effect of olfactory experience. We first conducted a field choice test and a wind tunnel experiment to examine the kairomonal response of individual predators toward prey pheromone components (frontalin, ipsenol, ipsdienol, sulcatol) along with the pine monoterpene α-pinene, which is a volatile compound from the host of the prey. We also presented semiochemically naive predators with two prey pheromone components, frontalin and ipsenol, alone or associated with a reward. Our results showed that T. dubius populations are composed of generalists that can respond to a broad range of kairomonal signals. Naive T. dubius also were more attracted to ipsenol following its association with a reward. This work constitutes the first evidence that the behavior of a predatory insect involved in bark beetle population dynamics is influenced by previous olfactory experience, and provides a potential explanation for the pattern of prey switching observed in field studies.     

Field Verification of Predator Attraction to Minnow Alarm Substance

Fishes such as minnows in the superorder Ostariophysi possess specialized alarm substance cells (ASC) that contain an alarm cue. Alarm substance can only be released by damage to the epidermis; thus, the release of alarm substance is a reliable indicator of predation risk. When nearby minnows detect the cue, they adopt a range of antipredator behaviors that reduce their probability of predation. Predator–predator interactions afford prey an opportunity to escape and, thus, a fitness benefit that maintains alarm substance calls over evolutionary time. Here, we present data from a simple field experiment verifying that nearby predators are attracted to minnow alarm substance because it signals an opportunity to pirate a meal. Fishing lures were baited with sponge blocks scented with either (1) water (control for sponge odor and appearance), (2) skin extract from non-ostariophysan convict cichlids (superorder Acanthopterygii, Archocentrus Cichlasoma nigrofasciatus) to control for general injury-released cues from fish, or (3) skin extract from fathead minnows (superorder Ostariophysi, Pimephales promelas). Predator strike frequency on each sponge type was 1,1, and 7 for water, cichlid, and minnow cues, respectively. These data provide the first field test using fish predators of the predator-attraction hypothesis for the evolution of Ostariophysan alarm substance cells.     

Brook Char (Salvelinus fontinalis) Can Differentiate Chemical Alarm Cues Produced by Different Age/Size Classes of Conspecifics

A wide diversity of aquatic organisms release chemical alarm cues when captured by a predator. For most animals, it is not known whether the specific chemicals that comprise the alarm cue are conserved as prey animals age. In this study, we tested whether brook char (Salvelinus fontinalis) can differentiate alarm cues produced by individuals of different ages/sizes. In separate laboratory experiments we exposed small brook char and large brook char to chemical alarm cues from small brook char, large brook char, and a control of swordtails (Xiphophorus helleri). Both small and large brook char responded with antipredator behavior to chemical alarm cues from both small and large char, but not to those from swordtails. Small char responded with a greater response intensity to cues of small char than to cues of large char. In contrast, large char responded with a greater response intensity to cues of large char than to cues of small char. These results suggest that chemical(s) that act as the alarm cue for fish of different age/size classes may be: (1) identical and that there may be other chemical(s) that allow the test fish to distinguish between cues from fish of different ages/sizes, or (2) the cues are not identical, but similar enough to be recognized.     

Real-Time Monitoring of (E)-β-Farnesene Emission in Colonies of the Pea Aphid, Acyrthosiphon pisum, Under Lacewing and Ladybird Predation

Aphids (Homoptera) are constantly under attack by a variety of predators and parasitoids. Upon attack, most aphids release alarm pheromone that induces escape behavior in other colony members, such as dropping off the host plant. In the pea aphid, Acyrthosiphon pisum Harris (Aphididae), the only component of this alarm pheromone is the sesquiterpene (E)-β-farnesene (EBF). EBF is thought to act as a kairomone by attracting various species of parasitoids and predators including lacewings and ladybirds. Lately, it also was proposed that EBF is constantly emitted in low quantities and used by aphids as a social cue. No study has focused on emission dynamics of this compound over a long time period. Here, we present the first long-time monitoring of EBF emission in aphid colonies using real-time monitoring. We used a zNose^TM to analyze the headspace of colonies of the pea aphid, under lacewing (Neuroptera: Chrysopidae) and ladybird (Coleoptera: Coccinellidae) predation, over 24 hr. We found no emission of EBF in the absence of predation. When either a ladybird adult or a lacewing larva was placed in an aphid colony, EBF was detected in the headspace of the colonies in the form of emission blocks; i.e., periods in which EBF was emitted alternating with periods without EBF emission. The number of emission blocks correlated well with the number of predation events that were determined at the end of each experiment. There was no circadian rhythm in alarm pheromone emission, and both predators were active during both night and day. Our results show that alarm pheromone emission pattern within an aphid colony is driven by the feeding behavior of a predator.     

Chemically Mediated Predator-free Space: Herbivores Can Synergize Intraspecific Communication Without Increasing Risk of Predation

Natural enemies of herbivores often locate cryptic insects by responding to volatiles associated with the prey's feeding and mating. For example, predators of bark beetles (Coleoptera: Scolytidae) exploit the aggregation pheromones that their prey use to attract mates and secure hosts. Bark beetles are cryptic insects that feed and develop in the subcortical tissues of trees and spend all but a portion of their life history within this habitat. The pine engraver, Ips pini, produces the pheromone ipsdienol throughout its transcontinental range. Predators of I. pini exploit this chemical as a kairomonal cue. Eastern and Midwestern I. pini populations also produce lanierone, which synergizes their attraction to ipsdienol. We evaluated the effects of varying amounts of lanierone, in combination with a constant amount of racemic ipsdienol, on the relative attraction of I. pini and its major predators in Wisconsin. Higher numbers of I. pini were captured with increasing release rates of lanierone. In contrast, the numbers of the major predators, such as Thanasimus dubius, Enoclerus nigrifrons, Platysoma cylindrica, and P. parallelum, did not differ among different lanierone release rates. The response of I. pini but not their predators to lanierone at ecologically realistic release rates may be part of a coevolving interaction between predators and prey and offers new strategies for semiochemically based pest management by selectively removing pests and leaving predators.     

Glyphosate-Based Herbicide Has Contrasting Effects on Prey Capture by Two Co-Occurring Wolf Spider Species

Anthropogenic substances have the potential to affect animal behavior either because they present a novel stimulus or because they interfere with natural chemical communication pathways. Such shifts can alter the dynamic between predators and potential prey, which might affect population success as well as the strength of food web linkages. We examined the foraging of two wolf spiders, Tigrosa helluo and Pardosa milvina (Araneae, Lycosidae), that are abundant in agroecosystems where they are routinely exposed to herbicides. We tested the hypothesis that the presence of a commercial formulation of a glyphosate-based herbicide would affect the prey capture behavior of these two wolf spiders. We tested the larger Tigrosa foraging on Pardosa or crickets (Acheta domesticus) and the smaller Pardosa foraging on crickets. Tigrosa subdued crickets more quickly and with fewer lunges than it took them to capture Pardosa. The presence of herbicide allowed Tigrosa to orient toward and capture both prey species more quickly but it did not affect the number of lunges required to subdue either prey. Herbicide did not affect the timing of prey capture for Pardosa but it did cause them to use more lunges in the process. Thus, herbicide had contrasting effects on foraging behavior of these two agrobiont predators, which means that it could shift the direction and strength of food web linkages in complex ways.     

Discrimination of Prey, But Not Plant, Chemicals by Actively Foraging, Insectivorous Lizards, the Lacertid Takydromus sexlineatus and the Teiid Cnemidophorus gularis

Sampling environmental chemicals to reveal prey and predators and to provide information about conspecifics is highly developed in lizards. Actively foraging lizards can discriminate between prey chemicals and control stimuli, but ambush foragers do not exhibit prey chemical discrimination. Recent experiments on a few species of herbivorous lizards have also demonstrated an ability to identify plant food chemicals. We studied chemosensory responses to chemicals from prey and palatable plants in two species of actively foraging, insectivorous lizards. Both the lacertid Takydromus sexlineatus and the teiid Cnemidophorus gularis exhibited strong responses to prey chemicals, but not to plant chemicals. These findings increase confidence in the relationship between prey chemical discrimination and foraging mode, which is based on data for very few species per family. They also provide data showing that actively foraging insectivores in two families do not respond strongly to plant cues. Such information is essential for eventual comparative studies of the relationship between plant diet and responses to food chemicals. The traditional method of presenting stimuli by using hand-held cotton swabs worked well for T. sexlineatus but could not be used for C. gularis due to repeated escape attempts. When stimuli were presented to C. gularis on ceramic tiles and no experimenter was visible, the lizards responded readily. Presentation of stimuli on tiles in the absence of a visible experimenter may be a valuable approach to study of food chemical discrimination by active foragers in which antipredatory behavior interferes with responses to swabs.     

5种新型杀菌剂对4种鱼的急性毒性及安全性评价

为评价5种新型杀菌剂的环境安全性,采用半静态法测定了其对4种鱼的急性毒性。结果表明,氟醚菌酰胺对斑马鱼、稀有鮈鲫和凤尾鲫的LC_(50)(96 h)均大于100 mg/L,对青鳉的LC_(50)(96 h)为35.25 mg/L,其急性毒性均为低毒;氟吡菌胺对斑马鱼、青鳉、稀有鮈鲫和凤尾鲫的LC_(50)(96 h)分别为1.49、0.56、0.35、1.04 mg/L,其对斑马鱼和凤尾鲫急性毒性为中毒,对青鳉和稀有鮈鲫为高毒;苯噻菌胺对斑马鱼、稀有鮈鲫和凤尾鲫的LC_(50)(96 h)均大于100 mg/L,对青锵的LC_(50)(96 h)为88.23mg/L,其急性毒性均为低毒;嘧菌酯对斑马鱼、青鳉、稀有鮈鲫和凤尾鲫的LC_(50)(96 h)分别为106.80、0.44、85.96、4.61 mg/L,其对斑马鱼和稀有鮈鲫急性毒性为低毒,对青鳉急性毒性为高毒,对凤尾鲫为中毒;醚菌酯对斑马鱼、青鳝、稀有鮈鲫和凤尾鲫的LC_(50)(96 h)分别为0.77、0.66、0.51、0.81 mg/L,其对4种鱼急性毒性均为高毒。明确这些药剂的环境安全性对指导其科学使用,保护环境生物均有较大意义。     

Effects of Hunger and Predation Risk on Foraging Behavior of Graybelly Salamanders, Eurycea multiplicata

We examined the effects of predation and hunger levels on foraging behavior of adult neotenic graybelly salamanders, Eurycea multiplicata griseogaster. Hungry and satiated salamanders were exposed to chemical stimuli from a predatory fish (sculpin, Cottus carolinae) and from two nonpredatory species, golden redhorse fish (Moxostoma erythrurum) and tadpoles of leopard frogs (Rana sphenocephala). Latency to attack prey was lengthened in the presence of chemical stimuli from predators regardless of hunger levels, but hungry salamanders had shorter latency times than satiated salamanders. There was no interaction between hunger and threat levels. In addition, salamanders distinguished between chemical stimuli from predatory (sculpin) and nonpredatory (redhorse) fishes; responses to redhorse and tadpole stimuli were not different. Handling times were not affected by either predator treatment or hunger level. In summary, graybelly salamanders can (1) recognize sculpin predators based solely on chemical cues, (2) distinguish between chemical stimuli from predatory and nonpredatory fish, and (3) adjust their foraging behavior according to both hunger and predation risk.     

Shifts in Life History as a Response to Predation in Western Toads (Bufo boreas)

Larval western toads (Bufo boreas) are known to exhibit antipredator behavior in response to both chemical alarm cues released from injured conspecifics and chemical cues of predatory invertebrates. In this study, we tested whether long-term exposure to predator and alarm cues resulted in an adaptive shift in life history characteristics of the toads. We raised groups of tadpoles in the presence of: (1) predatory backswimmers (Notonecta spp.) that were fed toad tadpoles, (2) nonpredatory water boatman (Corixidae), and (3) chemical alarm cues of injured conspecifics. Tadpoles raised in the presence of both chemical alarm cues and cues of predators fed tadpoles metamorphosed in significantly shorter time than those raised in the presence of the nonpredator control. Reducing time taken to reach metamorphosis would reduce exposure to aquatic predators. There was no difference among treatments in the size at metamorphosis. Our results suggest that this shift in metamorphic characteristics may represent a facultative alteration in life history.     

Lipid Content and Fatty Acid Profile of Muscle,Brain and Eyes of Seven Freshwater Fish: a Comparative Study

The fatty acid and lipid content of the eyes, brain and muscle were determined for the following seven freshwater fish species in China: black carp, grass carp, silver carp, bighead carp, common carp, crucian carp, and Wuchang bream. Lipid contents of all seven freshwater fish were in the order of brain > eyes > muscle. Most of the freshwater fish demonstrated much lower n-3 PUFA than n-6 PUFA in all tissues with n-3/n-6 ratios varying between 0.07 and 0.40, while silver carp and bighead carp had much higher n-3 PUFA than n-6 PUFA. The percentage of PUFA in the muscle of all species are the highest compared to those of the eyes and brain, while no significant difference was observed in PUFA concentration between eyes and brain (p > 0.05). Multivariable analyses indicate that the fatty acid composition of the filter-feeder fish (silver carp and bighead carp) was distinct from the other four species.