Vitamin a deficiency modifies response of predatory miteAmblyseius potentillae to volatile kairomone of two-spotted spider mite,Tetranychus urticae

A volatile kairomone of the two-spotted spider mite,Tetranychus urticae, elicits a searching response of the phytoseiid predatorAmblyseius potentillae, only when the predator is reared on a carotenoid-free diet. However, after addition of crystalline -carotene or vitamin A acetate to the predator's rearing diet this searching response was absent. Because vitamin A and -carotene are indispensable nutrients for diapause induction, the carotenoid-deficient predators increase their fitness by searching for two-spotted spider mites, when other spider mites are unavailable. Two-spotted spider mites, among others, contain the carotenoids required for diapause induction, but are an inferior prey due to the dense webbing they produce. When the predators have carotenoids at their disposal, they do better by searching for other spider mites that are more profitable in terms of reproductive success. Such a prey is the European red spide mite,Panonychus ulmi. The volatile kairomone of this prey elicits a searching response of the predator whether it has a carotenoid deficiency or not.     

Insect predator-prey coevolution via enantiomeric specificity in a kairomone-pheromone system

Insect predators can be guided to their prey by a kairomonal response to the prey pheromone. We found this phenomenon to be highly specific in the bark beetle predatorThanasimus dubius. Olfactory responses and behavioral tests revealed that the predator is guided to its major preyDendroctonusfrontalis by the primary enantiomer of the pheromone of the prey, (1S, 5R)-(–)-frontalin. These and other findings suggest the co-evolution of a kairomone system of the predator and the pheromone system of its prey.Texas Agricultural Experiment Station paper No.TA17770. The work was funded in part by McIntire-Stennis project 1525 (TAES) and the USDA program entitled The Expanded Southern Pine Beetle Research and Applications Program through TAES-CSRS grant 680-15-10. The findings, opinions, and recommendations reported herein are those of the authors and not necessarily those of the United States Department of Agriculture.     

Enantiomeric Specificity in a Pheromone–Kairomone System of Two Threatened Saproxylic Beetles, Osmoderma eremita and Elater ferrugineus

The scarab beetle Osmoderma eremita and its larval predator, the click beetle Elater ferrugineus, are threatened saproxylic beetles regarded as indicators of the species-richness of insect fauna of hollow deciduous trees. Male O. eremita produce the pheromone (R)-(+)-γ-decalactone to attract conspecific females, and this compound is also utilized by E. ferrugineus as a kairomone, presumably for detection of tree hollows containing prey. We have investigated enantiomeric specificity to γ-decalactone in this pheromone–kairomone system by electrophysiological and field trapping experiments. In single-sensillum recordings from male and female O. eremita, which used the (R)-enantiomer and the racemic mixture of γ-decalactone as odor stimuli, numerous olfactory receptor neurons (ORNs) responding to both stimuli were found. No neurons responded preferentially to the racemic mixture, showing that these beetles seem to lack receptors specific for the (S)-enantiomer. The enantiomeric specificity of ORNs was confirmed by gas chromatography-linked single-sensillum recordings where the two enantiomers in a racemic mixture were separated on a chiral column. Furthermore, in field experiments that used the (R)-enantiomer and the racemic mixture as lures, the attraction of O. eremita females corresponded to the amount of (R)-enantiomer released from lures with the (S)-enantiomer displaying no antagonistic effects. Trap catch data also suggested that the (S)-enantiomer is not a behavioral antagonist for E. ferrugineus. The odor-based system can be highly efficient in attracting the larval predator where trap catch in 1 yr almost equaled the total number of specimens collected in Sweden until 1993. Our study shows that racemic γ-decalactone could be used for cost-effective monitoring of both beetles.     

Effects on behavior ofApanteles melanoscelus females caused by modifications in extraction,storage, and presentation of Gypsy moth silk kairomone

Choice experiments were performed to investigate details of femaleApanteles melanoscelus (Ratzeburg) behavior when exposed to gypsy moth silk kairomone [Lymantria dispar (L.)] and to host larvae when kairomone is present. Female parasites only responded to the kairomone when it had been placed on thin strands such as cotton fibers. Both gypsy moth silk and silk glands contain the same or similar kairomones. Silk gland extracts were more active than head, alimentary canal, or hemolymph extracts of host larvae. Female responses decreased when low concentrations of silk gland extract or small numbers of treated fibers were presented to them. Silk gland extract was stable when frozen for 2 weeks, heated to 100 °C for 0.5 hr, freeze dried, or treated with 95% ethanol. The active component was nondialyzable. Silk deposited on the substrate increased host contacts and oviposition attempts, more so if wider areas were covered with silk, and even if the areas having silk were separated from the host. A theory of host selection inA. melanoscelus is proposed.Hymenoptera, Braconidae. Lymantria dispar L. (Lepidoptera: Lymantriidae).     

Laboratory Evaluation of Predator Odors for Eliciting an Avoidance Response in Roof Rats (Rattus rattus)

We evaluated eight synthetic predator odors and mongoose (Herpestes auropunctatus) feces for eliciting avoidance responses and/or reduced feeding by wild captured Hawaiian roof rats (Rattus rattus). In a bioassay arena, we recorded: (1) time until each rat entered the arena, (2) time elapsed until first eating bout, (3) time spent in each half of the arena, (4) number of eating bouts, and (5) consumption. Rats displayed a response to the predator odors in terms of increased elapsed time before initial arena entry and initial eating bout, a lower number of eating bouts, and less food consumption than in the respective control groups. The odor that produced the greatest differences in response relative to the control group was 3,3-dimethyl-1,2-dithiolane [from red fox (Vulpes vulpes) feces and mustelid anal scent gland]. Mongoose fecal odor produced different responses in four of the five variables measured while (E,Z)-2,4,5-trimethyl-³-thiazoIine (red fox feces) and 4-mercapto-4-methylpentan-2-one (red fox urine and feces) odors were different from the control group in three of the five variables measured. These laboratory responses suggest that wild Hawaiian roof rats avoid predator odors.     

Effects of diet on localized defecation by Northern Pike,Esox lucius

Fathead minnows (Pimephales promelas) are able to detect conspecific alarm pheromone in the feces of northern pike (Esox lucius) and have been shown to avoid areas labeled with the feces of pike that were fed minnows. The minnows did not avoid areas labeled with the feces of pike that were fed swordtails (Xiphophorous helleri), which lack ostariophysan alarm pheromone. In laboratory experiments, pike fed a diet of minnows localized their defecation away from their foraging area. It has been suggested that in doing so, pike may remove chemical cues that label their foraging area as dangerous to prey species. As yet there has been no conclusive evidence to support this hypothesis. In this experiment, we test the effects of different predator diets on localized defecation by pike. Pike were fed minnows, swordtails, or mice (Mus musculus). Swordtails and mice lack ostariophysan alarm pheromones. Area use and location of feces were recorded. Pike fed minnows spent significantly more time in the home area (i.e., area of the test tank where they were fed) and defecated significantly more often in the opposite end of the tank. Pike fed swordtails also exhibited a significant preference for the home area in area use, while those fed mice showed no such preference. When fed either swordtails or mice, there was no significant difference between the proportion of time spent and proportion of feces in each area of the test tank. These data suggest that pike localize their defecation only when consuming prey items containing alarm pheromone. The current findings support the hypothesis that pike localize their defecation to remove chemical cues from the foraging area of the home range in order to avoid chemically labeling their foraging area as dangerous to prey.     

Wolf Spiders Show Graded Antipredator Behavior in the Presence of Chemical Cues from Different Sized Predators

The wolf spider, Pardosa milvina, displays effective antipredator behavior (reduced activity) in the presence of silk and excreta cues from adults of another cooccurring wolf spider, Hogna helluo. However, Pardosa and Hogna engage in size-structured intraguild predation, where Pardosa may be either the prey or predator of Hogna. We tested the ability of adult female Pardosa to vary antipredator responses toward kairomones produced by Hogna that vary in size. Hogna were maintained on filter paper for 24 hr. We then presented the paper to adult female Pardosa simultaneously paired with a blank sheet of paper. One treatment had two sheets of blank paper to serve as a control. The Hogna stimulus treatments were as follows (N = 15/treatment): (1) 1 Hogna half the mass of Pardosa; (2) 1 Hogna of equal mass of a Pardosa; (3) 1 adult Hogna, 30 times the mass of Pardosa; and (4) 8 Hogna each 0.25 the mass of Pardosa. Pardosa decreased activity in the presence of kairomones from Hogna of equal or larger size, but showed no change in activity in the presence of a blank control or from a single Hogna smaller than itself. Pardosa showed a reduction in activity in the presence of cues from eight small Hogna. Pardosa avoided substrates with adult Hogna cues, but showed no avoidance response to any other treatment. These results suggest that Pardosa is showing graded antipredator behavior relative to the quantity of predator kairomones present rather than directly discriminating among the different sizes of the predator.     

Intensification and prolongation of host searching inLeptopilina heterotoma (Thomson) (Hymenoptera: Eucoilidae) through a kairomone produced byDrosophila melanogaster

A chemical cue (kairomone) of the host, larvae ofDrosophila, was found to influence patch-time allocation of the parasiteLeptopilina heterotoma. This kairomone is soluble in water and chloroform. The kairomone was purified using thin-layer chromatography. The concentration of the kairomone increases with an increasing number of hosts. The parasites may use presence and concentration of the kairomone as cues to determine patch-time allocation.     

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.     

Why are predator urines aversive to prey?

Predator odors often repel prey species. In the present experiments, we investigated whether changes in the diet of a predator, the coyote (Canis latrans) would affect the repellency of its urine. Furthermore, because predator odors have a high sulfur content, reflecting large amounts of meat in the diet, we investigated the contribution of sulfurous odors to repellency. Our results were consistent with the hypothesis that diet composition and sulfurous metabolites of meat digestion are important for the repellency of predator odors to potential prey.     

Specific foraging kairomones used by a generalist parasitoid

In general, it is assumed that generalist natural enemies do not innately use specific cues for the location of their host or prey species. This hypothesis was tested using naïve females of the generalist parasitoid Lariophagus distinguendus Förster and two of its hosts, larvae of the lesser grain borer Rhyzopertha dominica (F.) and of the granary weevil Sitophilus granarius L., feeding in wheat grains. In a four-chamber olfactometer, female parasitoids were attracted to volatiles emanating from the feces of both host species. Chemical analysis of the volatiles from the feces of R. dominica revealed the presence of dominicalure 1 and 2, the species specific aggregation pheromones of R. dominica. The main compounds in the volatiles from feces of S. granarius were identified as chemicals related to mites that are associated with hosts of L. distinguendus. Because these mites are not specific for S. granarius but also co-occur with other hosts, the mite chemicals have to be considered as general cues. In bioassays, synthetic dominicalure was attractive to naïve L. distinguendus, explaining the attraction of feces volatiles from R. dominica. Synthetic mite chemicals and sitophilate, the aggregation pheromone of S. granarius, had no effect on naïve parasitoids. It remains to be determined which innate chemical cues from feces of S. granarius are used by L. distinguendus. In contrast to our initial hypothesis, the generalist L. distinguendus is innately using specific cues for foraging. Two ideas are provided to explain this result.     

The Involvement of Volatile Infochemicals from Spider Mites and from Food-Plants in Prey Location of the Generalist Predatory Mite <Emphasis Type="Italic">Neoseiulus californicus</Emphasis>

We investigated volatile infochemicals possibly involved in location of the generalist predatory mite Neoseiulus californicus to plants infested with spider mites in a Y-tube olfactometer. The predators significantly preferred volatiles from lima bean leaves infested with Tetranychus urticae to uninfested lima bean leaves. Likewise, they were attracted to volatiles from artificially damaged lima bean leaves and those from T. urticae plus their visible products. Significantly more predators chose infested lima bean leaves from which T. urticae plus their visible products had been removed than artificially damaged leaves, T. urticae, and their visible products. These results suggest that N. californicus is capable of exploiting a variety of volatile infochemicals originating from their prey, from the prey-foodplants themselves, and from the complex of the prey and the host plants (e.g., herbivore-induced volatiles). We also investigated predator response to some of the synthetic samples identified as volatile components emitted from T. urticae-infested lima bean leaves and/or artificially damaged lima bean leaves. The predators were attracted to each of the five synthetic volatile components: linalool, methyl salicylate, (Z)-3-hexen-1-ol, (E)-2-hexenal, and (Z)-3-hexenyl acetate. The role of each volatile compound in prey-searching behavior is discussed.     

Specificity of Pheromonal and Kairomonal Response of the Israeli Pine Bast Scale Matsucoccus josephi and Its Predator Elatophilus hebraicus

It has been demonstrated previously that the sex pheromone of the Israeli pine bast scale, Matsucoccus josephi, (2E,5R,6E,8E)-5,7-dimethyl2,6,8-decatrien-4-one (1) is also a potent kairomone of the scale insect's predator Elatophilus hebraicus. Surprisingly, the sex pheromones of M. feytaudi (2) and M. matsumurae (3) also attract E. hebraicus. These results have prompted us to prepare a series of analogs of 1 with variations in the two moieties attached to the C=O group (4–9) in order to probe the structure–activity relationship of the pheromonal/kairomonal response of M. josephi and E. hebraicus. The most selective and active pheromone analog is 8, attracting only M. josephi males and the most selective and active kairomone analog is the M. feytaudi pheromone 2, attracting only adults of E. hebraicus. A dose–response field test of these analogs and the chiral and racemic M. josephi pheromone 1 indicates that the specificity is maintained at a broad range between 25 and 400 g corresponding to 1. Analog 5, which is neither a parapheromone nor a kairomone, and analog 8, which is only a parapheromone, are not inhibitory to M. josephi or to E. hebraicus. Our study indicates that alterations in the diene side chain of 1, common to all three Matsucoccus pheromones, strongly reduce the kairomonal activity while structural changes in the second side chain significantly reduce the pheromonal activity. The discovery of selective analogs of 1 has practical implications and enables specific monitoring of M. josephi or E. hebraicus. Particularly important is the possibility to mass-trap males of M. josephi without reducing the population of E. hebraicus.     

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.     

Influence Of Diet-Related Chemical Cues from Predators on the Hatching of Egg-Carrying Spiders

Previous studies have shown that animals may make adaptive adjustments in response to chemical cues from predators, but hatching responses to diet-related chemical cues from predators have not been previously demonstrated. In the system studied here, the predator is an araneophagic jumping spider (Salticidae), Portia labiata, and the prey organism is a subsocial spitting spider, Scytodes pallida (Scytodidae). The spitting spider carries its eggs in its chelicerae, and carrying eggs is known to make it more vulnerable to predators. It is also known from an earlier study that the prior diet of the predator alters how dangerous the individual predator is to the spitting spider. In the experiments reported here, incubation time was shorter when volatile cues from the predator were present and longer in control tests when no chemical cues from the predator were present. The previous predators diet also influenced incubation time: when in the presence of volatile cues from individuals of P. labiata that had previously fed on individuals of S. pallida, incubation time was shorter than when in the presence of volatile cues from individuals of P. labiatathat had been feeding instead on house flies.     

Identification and Synthesis of a Kairomone Mediating Host Location by Two Parasitoid Species of the Cassava Mealybug Phenacoccus herreni

Two encyrtid species, Acerophagus coccois and Aenasius vexans, parasitoids of the cassava mealybug Phenacoccus herreni use a contact kairomone from the body surface of their host as a host-location stimulant. The kairomone was synthesized and identified as O-caffeoylserine based on a combination of chromatographic methods. The synthetic compound was determined to be active.     

The Egg Parasitoid <Emphasis Type="Italic">Trissolcus basalis</Emphasis> uses <Emphasis Type="Italic">n</Emphasis>-nonadecane,a Cuticular Hydrocarbon from its Stink Bug Host <Emphasis Type="Italic">Nezara viridula</Emphasis>, to Discriminate Between Female and Male Hosts

Contact kairomones from adult southern green stink bugs, Nezara viridula (L.) (Heteroptera: Pentatomidae) that elicit foraging behavior of the egg parasitoid Trissolcus basalis (Wollaston) were investigated in laboratory experiments. Chemical residues from tarsi and scutella of N. viridula induced foraging by gravid female T. basalis. Residues from body parts of female N. viridula elicited stronger responses than those from the corresponding body parts of males. Deproteinized tarsi still elicited searching responses from wasps, indicating that the kairomone was not proteinaceous. Hexane extracts of host cuticular lipids induced searching responses from T. basalis, with a strong preference for extracts from female hosts. Extracts consisted primarily of linear alkanes from nC₁₉ to nC₃₄, with quantitative and qualitative differences between the sexes. Extracts of female N. viridula contained more nC₂₃, nC₂₄, and nC₂₅ than the corresponding extracts from males, whereas nC₁₉ was detected only in extracts from males. Direct-contact solid phase microextraction (DC-SPME) of N. viridula cuticle and of residues left by adult bugs walking on a glass plate confirmed gender-specific differences in nC₁₉. Trissolcus basalis females responded weakly to a reconstructed blend of the straight-chain hydrocarbons, suggesting that minor components other than linear alkanes must be part of the kairomone. Addition of nC₁₉ to hexane extracts of female N. viridula significantly reduced the wasps’ arrestment responses, similar to wasps’ responses to hexane extracts of male hosts. Overall, our results suggest that a contact kairomone that elicits foraging by T. basalis females is present in the cuticular lipids of N. viridula, and that the presence or absence of nC₁₉ allows T. basalis females to distinguish between residues left by male or female hosts. The ecological significance of these results in the host location behavior of scelionid egg parasitoids is discussed.     

Oviposition-deterring pheromone ofRhagoletis pomonella

We found that after the parasitoidOpius lectus has arrived on a fruit infested by eggs or early-instar larvae of its tephritid hostRhagoletis pomonella, the following stimuli act to retain it and elicit antennal tapping and oviposition probes: unidentified fruit chemical components; characteristic fruit shape, size and color; andR. pomonella oviposition-deterring pheromone. This is the first demonstration of an oviposition-deterring pheromone in a phytophagous insect serving as a kairomone to one of its parasitoids.O. alloeus, a parasitoid of lateinstar larvae ofR. pomonella, was not influenced by the pheromone. Possible use of the pheromone for management ofO. lectus in a multifacetedR. pomonella suppression program is discussed.     

A long-range attractant kairomone for egg parasitoidTrissolcus basalis,isolated from defensive secretion of its host,Nezara viridula

A short-chain ,-unsaturated aldehyde, (E)-2-decenal, present in the defensive metathoracic gland ofNezara viridula (L.) (Heteroptera: Pentatomidae), stimulates a behavioral response in the egg parasitoidTrissolcus basalis (Woll.) (Hymenoptera: Scelionidae). Preliminary studies showed thatT. basalis are attracted to an area containing adultN. viridula, but we also found that femaleT. basalis would examine and probe glass beads coated with an acetone extract of the metathoracic gland from males or females. Using this bioassay, the kairomone was isolated by bioassay directed by preparative gas chromatography and identified by NMR and mass spectrometry as (E)-2-decenal. The biological activity of the identified aldehyde was compared with analogs to determine specificity. An unstable Z isomer was found to be more active but not present in detectable or behaviorly relevant levels in the host, based on the bell-shaped dose-response curve of the two isomers. An investigation was also designed to determine if theE isomer was also responsible for the egg recognition kairomone activity previously reported. However, no 2-decenal isomers were detected in host egg extracts and the chemical characteristics of the 2-decenal isomers differ from the unidentified egg recognition kairomone. The role of the (E)-2-decenal in attracting femaleT. basalts toN. viridula was demonstrated in a Y-tube olfactometer; this alk-2-enal appears to act as a long-range kairomone orientingT. basalis toNezara populations.     

A complex,cross-taxon,chemical releaser of antipredator behavior in amphibians

Prey species show diverse antipredator responses to chemical cues signaling predation threat. Among terrestrial vertebrates, the red-backed salamander, Plethodon cinereus, is an important species in the study of these chemical defenses. During the day and early evening, this species avoids rinses from garter snakes, Thamnophis sirtalis, independent of snake diet, but late at night, avoids only those rinses from garter snakes that have recently eaten P. cinereus. We tested whether the selective, late-night response requires the ingestion or injury of salamanders. In three experiments, we tested P. cinereus for their responses to separate or combined rinses from salamanders (undisturbed, distressed, and injured P. cinereus) and snakes (unfed, earthworm fed, and salamander-fed T. sirtalis). When paired against a water control, only rinses from salamander-fed snakes were avoided. When salamander treatments (undisturbed or distressed) were combined with the snake treatments (unfed or earthworm-fed) and tested against a water control, the combinations elicited avoidance. When selected treatments were paired against the standard rinse from salamander-fed snakes, only the combined rinses from salamanders and snakes nullified the avoidance response to the standard rinse. These data reveal a prey defense mechanism involving chemical elements from both the predator and prey that does not require injury or ingestion of the prey in the formation of the cue.