Prey chemical discrimination and strike-induced chemosensory searching in the lizardLiolaemus zapallarensis

Summary Experimental tests were conducted to determine whether the ambush foraging iguanian lizard,Liolaemus zapallarensis, was capable of discriminating prey chemicals from control substances and whether this lizard exhibits strike-induced chemosensory searching (SICS) or its components after biting prey. The two components of SICS are a poststrike elevation in tongue-flicking rate (PETF) and apparent searching movements for relocation of prey that has been bitten, but released or escaped.Liolaemus zapallarensis failed to discriminate prey chemicals from control substances, but exhibited significant PETF lasting one minute. SICS was absent inL. zapallarensis because no post-strike movements were observed. The absence of both prey chemical discrimination and SICS exhibited byL. zapallarensis is common to all the insectivorous iguanians and ambush foraging lizards studied to date. However,L. zapallarensis is the first insectivorous iguanian species shown to exhibit PETF. The results suggest thatL. zapallarensis does not use the tongue for detection, identification, or relocation of prey while foraging. The possibility does remain thatL. zapallarensis may be capable of chemically identifying prey once the prey stimuli reach the oral cavity.     

Strike-induced chemosensory searching is absent in the cordylid lizard,Cordylus cordylus,a scleroglossan ambush forager

Summary Strike-induced chemosensory searching (SICS) was not detected experimentally in the cordylid lizard,Cordylus cordylus. Both components of SICS, a post-strike elevation in tongue-flick rate (PETF) and searching movements for attacked and released prey, were absent. The findings are consistent with previous data showing that PETF and/or SICS are lacking in all lizard families yet studied that forage primarily by ambush, but are present in actively foraging scleroglossan families and the herbivorous iguanian family Iguanidae. It is suggested that foraging behavior is a primary determinant of the presence or absence of SICS in lizards. Nevertheless, in most families in the two major clades, Iguania and Scleroglossa, the plesiomorphic foraging mode is retained. The findings agree with the prediction that SICS is absent in families lacking lingually mediated prey chemical discrimination (PCD), presumably due to selection against movement by ambush foragers that avoid being detected by either prey or predators because they remain motionless. Although PETF and SICS were absent, labial-licking and lingual movements similar to those observed after swallowing increased after biting prey, suggesting that the functions of these lingual movements may have been related to grooming. Locomotory movements did not increase following biting and appeared to represent avoidance of the experimenter.     

Strike-induced chemosensory searching by a teiid lizard,the golden tegu (Tupinambis nigropunctatus)

Summary Strike-induced chemosensory searching (SICS) is experimentally demonstrated in a teiid lizard,Tupinambis nigropunctatus. SICS consists of a concurrent post-strike elevation in tongue-flick rate (PETF) and searching movements after voluntary release or escape of bitten prey or removal of prey from the predator's mouth. The results are consistent with previous data showing that PETF and/or SICS occur in all families of scleroglossan lizards and snakes and all families of actively foraging lizards yet studied. The relatively short duration of SICS (2 min) in a lizard having lingual and vomeronasal structure highly specialized for chemosensory sampling and analysis suggests that phylogenetic and ecological factors may be more important than morphology in determining the duration. The greatest known durations occur only in the presumably monophyletic clade containing varanoid lizards and snakes, all of which have highly developed chemical sampling and chemoreceptor apparatus, but in addition feed on prey that has a high probability of being relocated by prolonged scent-trailing. Because only active foragers move through the habitat while tongue-flicking and exhibit lingually mediated prey chemical discrimination, only active foragers may be expected to use SICS. SICS would appear to be useless to an ambush forager and might disrupt its defensive crypticity, rendering it more detectable to predators and prey. Therefore, it may be predicted that SICS is adaptively adjusted to foraging mode.     

The peculiar case of an insectivorous iguanid lizard that detects chemical cues from prey

Summary. Ecological and phylogenetic factors determine which sensory modalities organisms use in their day-to-day activities. Among lizards, empirical studies indicate a tight association between foraging strategies and the ability to detect chemical cues from prey. Consequently, ambush insectivores do not detect food chemicals and these differences have a phylogenetic basis, as ambush lizards mainly belong to the Iguania clade. These data contrast, however, with the widespread uses of chemoreception in the Iguania genus Liolaemus, which are mostly insectivorous ambush predators. Moreover, observations from different Liolaemus species suggest a capability to find prey through chemoreception. In order to clarify the abilities of Liolaemus to detect chemical cues from prey, the chemoreceptive behavior of the insectivorous ambush predator, L. lemniscatus, was studied. Lizards were given the choice between areas with and without chemical cues from a food item (mealworms). Results show that test animals stayed for longer, moved more, and did more chemical exploration (tongue flicks) in the area where chemical cues from mealworms were present. Furthermore, in this area, more individuals displayed behaviors that suggest maintenance and defense of the prey patch. Thus, L. lemniscatus is the first insectivorous Iguania reported to be able to detect chemical cues from prey. Although I propose a mechanism for acquiring chemical detection of prey cues in Liolaemus, I also remark that it is necessary to reanalyze both the abilities to detect and use chemical foraging cues in Iguania at large, and the methodologies traditionally used to study these issues.     

Correlated evolution of prey chemical discrimination with foraging, lingual morphology and vomeronasal chemoreceptor abundance in lizards

Comparative data from ten families of lizards suggest that correlated evolution has occurred between the ability to identify prey chemicals and several aspects of lingual function and morphology, abundance of vomeronasal chemoreceptor cells, and foraging behavior. Ability to discriminate prey chemicals from control substances was measured experimentally and correlated with other variables by Felsenstein's method. This ability increased with evolutionary increases in degree of lingual protrusion during tongue-flicking, which may reflect the tongue's ability to reach substrates to be sampled. It increased with deepened lingual forking and greater lingual elongation, which may be important for scent-trailing and sampling ability, respectively. Discriminatory ability also increased with abundance of vomerolfactory chemoreceptors, which presumably reflects some aspects of analytical capacities of the vomeronasal system. Prey chemical discrimination increased with degree of active foraging. Natural selection for improved vomerolfactory sampling and analysis of prey chemicals by active, but not ambush, foragers appears to account for the observed relationships. In active foragers that use vomerolfaction to locate prey, natural selection favors increased abilities to lingually sample chemicals from environmental substrates, analyze the samples for prey chemicals, and respond appropriately if prey chemicals or possible prey chemicals are detected. Such selection can account for the observed relationships among the sampling device and its movements, the sense, the discriminations, and variations in foraging ecology. Received: 13 February 1997 / Accepted after revision: 12 June 1997     

Lingual and biting responses to prey chemicals by ingestively naive scincid lizards: discrimination from control chemicals,time course,and effect of method of stimulus presentation

Summary. We tested responses to prey chemicals by lizard hatchlings of an oviparous species and neonates of a viviparous species, neither of which had never eaten. Both species responded more strongly to prey chemicals than to odorous and odorless control stimuli presented on cotton swabs. Although only a few species have been examined, all that have been tested have an innate capacity for prey chemical discrimination, suggesting that this innate response to prey chemicals is widespread among lizards that use the lingual-vomeronasal system to locate and identify prey. Innate prey chemical discrimination has the great advantage of permitting lizards lacking prior experience with food to respond appropriately to chemical cues associated with food. Both species discriminated prey chemicals from control substances at age three days, earlier than previously known. Our data hint that Mabuya macularia may be capable of discrimination on its day of birth, but further study is needed to determine the exact onset. A stronger tendency to attack swabs bearing prey chemicals by Scincella lateralis than by M. macularia may be explained by differences in defensiveness near an experimenter or by differences in the importance of visual prey cues for confirmation of chemical cues in the natural habitats of these species. In M. macularia responses to the control stimuli declined over days of testing, suggesting habituation, but responses to prey chemicals did not habituate by the third day of testing, which is interpreted as a possible adaptive response to permit location of food. In the standard method of stimulus presentation, a cotton swab bearing a chemical stimulus is placed anterior to a lizard's snout. We tested a new method in which the swab was placed in continuous contact with the lizard's anterior labial scales. The new method elicited significantly stronger responses from M. macularia. We discuss reasons for this finding and applications for the new method. Received 2 September 1999; accepted 15 December 1999     

Locomotor impairment and defense in gravid lizards (Eumeces laticeps): behavioral shift in activity may offset costs of reproduction in an active forager

Summary Female Eumeces laticeps experience a substantial decrease in running speed (ca. 25%) and an even greater loss of endurance (slightly over 50%) while gravid. Because some widely foraging lizards, including E. laticeps, rely primarily on running to escape predators, the decreases in speed and stamina may contribute to an increased risk of predation. However, observations suggest that gravid females become less active or conspicuous on the surface. Ambush foraging lizards rely relatively more on crypsis associated with immobility to avoid predation and thus can have greater average relative clutch mass (RCM) than active foragers. Behavioral compensation for locomotor impairment by becoming less active or conspicuous may allow some species the advantages inherent in both high relative clutch mass when gravid and the increased energetic profitability of active foraging when not gravid. As females gain weight during the breeding season, they may forage actively until the risk due to increasing locomotor impairment becomes too great and then change defensive strategy to greater reliance on crypsis. Without such a shift, widely foraging squamate reptiles may be less able than ambush foragers to exploit life-historical strategies demanding high current investment in reproduction.     

Predatory behavior of Polybia sericea (Olivier), a tropical social wasp (Hymenoptera: Vespidae)

Summary Polybia sericea (Olivier) (Hymenoptera: Vespidae) foragers were trained to visit experimental foraging plots and tests were conducted to determine the role of visual, olfactory, and chemotactile cues in prey location. Foragers approached prey from downwind and hovered downwind of visual and olfactory stimuli. Olfactory cues were more likely to elicit landing than were visual cues. Biting of potential prey was most consistently elicited by a combination of visual, tactile, and chemotactile cues. Foragers encountering large prey carried a piece back to the nest and returned for prey remains. These returning foragers used visual cues to direct intensive aerial search; olfactory prey cues elicited landing.     

Prey odor discrimination by ingestively naive coachwhip snakes(Masticophis flagellum)

Summary Ingestively naive hatchling coachwhip snakes(Masticophis flagellum) detected integumentary chemicals from several potential prey species and discriminated them from chemical stimuli from other animals and from distilled water, strongly suggesting a genetic basis for these abilities. The strongest responses were to lizard and snake stimuli, which form a major part of the diet. Variable responses to chemical cues from other taxa are discussed. Responses by coachwhip snakes to prey chemicals appear to be highly specific, as suggested by the stronger reaction to vomodors of sympatric than of allopatric lizard species. The highly developed use of chemical cues by the diurnal, visually oriented coachwhip snake emphasizes the general importance of chemical senses to predation by nonvenomous snakes, regardless of the involvement of vision.     

Pursuit-deterrent communication between prey animals and timber rattlesnakes (Crotalus horridus): the response of snakes to harassment displays

A thorough understanding of communication requires an evaluation of both the signaler and receiver. Most analyses of prey–predator communication are incomplete because they examine only the behavior of the prey. Predators in these systems may be understudied because they are perceived as less tractable research subjects, due to their more cryptic hunting behaviors and secretive lifestyles. For example, research on interactions between rodents and rattlesnakes has focused on the behavior of rodent signalers, while responses of snakes have been virtually unexamined. Rattlesnakes are ambush predators, and capture rodents by waiting at foraging sites for long periods of time. In this study, I take advantage of the sedentary nature of this foraging strategy and use fixed videography to record natural encounters between timber rattlesnakes (Crotalus horridus) and their prey. Three different prey species were found to exhibit conspicuous visual displays to snakes, both when snakes were actively foraging, and when they were basking. After receiving displays, foraging snakes left their ambush sites and moved long distances before locating subsequent ambush sites, indicating that they responded to displays by abandoning attempts to ambush prey in the vicinity of signalers. This study represents the first quantitative analysis of the response of free-ranging snakes to signals from their prey, and elucidates a technique by which such quantitative data can be more easily obtained.     

Chemosensory recognition of the marbled whiptail lizard, Aspidoscelis marmorata (Squamata: Teiidae) to odors of sympatric lizards (Crotophytus collaris, Coleonyx brevis, Eumeces obsoletus and Uta stansburiana) that represent different predation risks

The ability of the whiptail lizard Aspidoscelis marmorata (Teiidae) to detect and discriminate chemical stimuli associated with the integument of a sympatric saurophagous lizard (Crotaphytus collaris) was tested. Females of A. marmorata were presented with cotton swabs containing chemical cues from C. collaris and three species of nonsaurophagous lizards, as well as water and cologne (pungency control), and total number of tongue-flick (TF) recorded. Other responses were assessed including directed TF rate, time from initial presentation of the stimulus to first TF (latency), time spent fleeing from the stimulus, and number of flight bouts. The number of TFs, directed TF rate, and number of attempts at fleeing exhibited by were significantly greater when females were presented with swabs containing cues from C. collaris as compared to nonsaurophagous lizards and both control treatments. A. marmorata required significantly less time to elicit their first TF when presented with cues from C. collaris as compared to all other treatments. Most previous studies have focused on the responses of lizards to cues associated with snake predators. This study provides the first available data on responses of a teiid to cues associated with a saurophagous lizard.     

Effects of movement and eating on chemosensory tongue-flicking and on labial-licking in the leopard gecko (Eublepharis macularius)

Summary Two forms of lingual protrusion, tongueflicking and labial-licking, were differentially affected by combinations of movement and eating conditions in a eublepharid gecko (Eublepharis macularius). Tongue-flicking, in which the tongue contacts substrates beyond the lizard's body, occurred at increased rates during locomotion and during locomotion was significantly more frequent after eating than in a baseline condition. Labial-licking, in which a protruded portion of the tongue touches the labial, mental or rostral scales that surround the mouth, increased after eating. Unlike tongue-flick rates, by far the highest labial-lick rates were observed in stationary lizards after eating. The elevated tongue-flicking rates during movement after eating may be a manifestation of a postingestive chemosensory search for prey. In addition to grooming, several possible chemosensory functions of labial-licking are discussed, including gustatory sampling, sampling prey chemicals on the labials for transfer to the vomeronasal system, and redistribution of chemicals on the tongue to enhance transfer. It is suggested that labial-licking might help motionless lizards maintain vigilance for visual prey stimuli associated with the specific chemical prey cues. Another possible explanation for the increased labial-lick rate while motionless after eating is that prey chemicals induce tongue-flicking, but that the distance protruded is lessened and the tongue does not contact environmental substrates. Tongue-flicking while stationary is unlikely to lead to detection of additional prey and might incur detection by the lizard's predators or prey.     

Size-based predation by kookaburras (Dacelo novaeguineae) on lizards (Eulamprus tympanum: Scincidae): what determines prey vulnerability?

Lizards and birds are both popular ”model organisms” in behavioural ecology, but the interactions between them have attracted little study. Given the putative importance of birds as predators of diurnal lizards, it is of considerable interest to know which traits (of lizards as well as birds) influence the outcome of a predatory attempt. We studied predation by giant terrestrial kingfishers (kookaburras, Dacelo novaeguineae: Alcedinidae) on heliothermic diurnal lizards (highland water skinks, Eulamprus tympanum: Scincidae), with particular reference to the role of prey (lizard) size. Our approach was twofold: to gather direct evidence (sizes of lizards consumed in the field, compared to those available) and indirect evidence (size-related shifts in lizard behaviour). We quantified the size structure of a natural population of skinks (determined by an extensive mark-recapture program), and compared it to the sizes of wild lizards taken by kookaburras (determined by analysis of prey remains left at the birds’ nests). Kookaburras showed size-based predation: they preyed mainly on small and medium-sized rather than large lizards in the field. However, the mechanism producing this bias remains elusive. It is not due to any distinctive behavioural attributes (locomotor ability, activity level, habitat usage) of the lizards of the size class disproportionately taken by the kookaburras. The greater vulnerability of subadult lizards may reflect subtle ontogenetic shifts in ecological and behavioural traits, but our data suggest that great caution is needed in inferring patterns of vulnerability to predation from indirect measures based on either the prey or the predator alone. Instead, we need direct observations on the interaction between the two. Received: 30 May 2000 / Revised: 29 July 2000 / Accepted: 26 August 2000     

The causes and consequences of partial prey consumption by wolves preying on moose

For a wide range of taxa, partial prey consumption (PPC) is a frequent occurrence. PPC may arise from physiological constraints to gut capacity or digestive rate. Alternatively, PPC may represent an optimal foraging strategy. Assessments that clearly distinguish between these causes are rare and have been conducted only for invertebrate species that are ambush predators with extra-intestinal digestion (e.g., wolf spiders). We present the first strong test for the cause of PPC in a cursorial vertebrate predator with intestinal digestion: wolves (Canis lupus) feeding on moose (Alces alces). Previous theoretical assessments indicate that if PPC represents an optimal foraging strategy and is not caused by physiological limitations, then mean carcass utilization is negatively correlated with mean kill rate and the utilization of individual carcasses is uncorrelated with time between kills. Wolves exhibit exactly this pattern. We explore how the typical portrayal of PPC by wolves has been not only misleading but also detrimental to conservation by promoting negative attitudes toward wolves.     

Effects of aggregation on feeding and survival in a communal wren

Summary Foraging by a social wren, Campylorhynchus nuchalis (Troglodytidae), in a tropical savanna habitat is not enhanced by aggregation. Data for marked individuals show that solitary foraging results in a higher capture rate than foraging near others. We find no evidence of imitative foraging, as individuals actively avoid successful foragers following a capture and successful foragers do not restrict their search to recently productive stations or techniques. Captures are seldom temporally clumped, and clumping is probably not pronounced enough to favor imitation. Juveniles show no greater tendency to respond to captures of others, or to succeed in foraging in a group, than do adults. Aggregation is probably disadvantageous for foraging because of dispersed, scarce, cryptic, and noneruptive prey and because of the searching technique of these foliage-gleaning insectivores. If predator avoidance is enhanced by aggregation, it does not result in either increased survival or increased foraging efficiency in large groups, even by juveniles.     

The role of thermoregulation in lizard biology: Predatory efficiency in a temperate diurnal basker

Summary Decreasing levels of simulated solar radiation have the following effects in the diurnal basking lizard Lacerta vivipara: (i) increase in time spent basking with a consequent decrease in time available for foraging (ii) decrease in speed of movement whilst foraging (iii) decrease in total foraging distance, and hence contact with potential prey (iv) decrease in searching efficiency in an experimental arena. Complete absence of simulated solar radiation accentuates these effects, and reduces the proportion of faster-moving prey in the diet. Time taken to swallow prey (handling time) increases exponentially with decreasing body temperature. It is concluded from these results that maintaining relatively high activity temperatures (30–36°C) is adaptive for the species because the loss of potential foraging time caused by lengthy periods of basking is offset by the following advantages: increased contact with and capture of prey, increased efficiency of prey handling, and availability of a wider range of prey types.     

Forager specialization and the control of nest repair in Polybia occidentalis Olivier (Hymenoptera : Vespidae)

We measured patterns of individual forager specialization and colony-wide rates of material input during periods of response to experimental nest damage and during control periods in three colonies of the tropical social wasp Polybia occidentalis.

Interpopulational variation in chemosensory responses to selected steroids from femoral secretions of male lizards, Podarcis hispanica, mirrors population differences in chemical signals

Chemical signals are important for mate and species recognition. If variation in chemical signals occurs between populations of the same species, these differences could later preclude mating between populations and lead to speciation. In the Iberian wall lizard, Podarcis hispanica, the lipophilic fraction of femoral secretions of males is mainly a mix of steroids and fatty acids. Among steroids, the most abundant compounds are cholesterol and cholesta-5,7-dien-3-ol, which are implicated in intraspecific communication and sexual selection. Interpopulational differences in chemical signals of males, and in response to these chemicals, could contribute to reproductive isolation between populations, which would explain the known genetic differences between these populations. Chemical analyses indicated that five distinct populations of this lizard from Madrid (Central Spain) differed in the proportions of two steroids (cholesterol and cholesta-5,7-dien-3-ol) in femoral secretions. Moreover, lizards discriminated and had high chemosensory responses (i.e., high tongue-flick rates) to these steroids, but showed interpopulational differences. Lizards from populations with cold temperatures and high relative humidity (i.e., northern Madrid) elicited higher responses to these steroids, whereas the converse occurred for lizards from populations occupying dry and hot habitats (i.e., southern Madrid). Interestingly, the magnitude of the chemosensory responses to cholesta-5,7-dien-3-ol in each population mirrored the abundance of this compound in secretions of males of that population. These results suggest that the importance of cholesta-5,7-dien-3-ol in males’ secretions might be lower for lizards from the southern populations. These differences in the relative importance of chemical signals could explain reproductive isolation and cryptic speciation between populations of this lizard.     

The interplay between foraging mode, habitat structure, and predator presence in antlions

Antlion larvae are sand-dwelling insect predators, which ambush small arthropod prey while buried in the sand. In some species, the larvae construct conical pits and are considered as sit-and-wait predators which seldom relocate while in other species, they ambush prey without a pit but change their ambush site much more frequently (i.e., sit-and-pursue predators). The ability of antlion larvae to evade some of their predators which hunt them on the sand surface is strongly constrained by the degree of sand stabilization or by sand depth. We studied the effect of predator presence, predator type (active predatory beetle vs. sit-and-pursue wolf spider), and sand depth (shallow vs. deep sand) on the behavioral response of the pit building Myrmeleon hyalinus larvae and the sit-and-pursue Lopezus fedtschenkoi larvae. Predator presence had a negative effect on both antlion species activity. The sit-and-wait M. hyalinus larvae showed reduced pit-building activity, whereas the sit-and-pursue L. fedtschenkoi larvae decreased relocation activity. The proportion of relocating M. hyalinus was negatively affected by sand depth, whereas L. fedtschenkoi was negatively affected also by the predator type. Specifically, the proportion of individual L. fedtschenkoi that relocated in deeper sand was lower when facing the active predator rather than the sit-and-pursue predator. The proportion of M. hyalinus which constructed pits decreased in the presence of a predator, but this pattern was stronger when exposed to the active predator. We suggest that these differences between the two antlion species are strongly linked to their distinct foraging modes and to the foraging mode of their predators. Reut Loria and Inon Scharf contributed equally to the paper.     

Individual specialization in the hunting wasp <Emphasis Type="Italic">Trypoxylon</Emphasis> (<Emphasis Type="Italic">Trypargilum</Emphasis>) <Emphasis Type="Italic">albonigrum</Emphasis> (Hymenoptera,Crabronidae)

Individual-level variation in resource use occurs in a broad array of vertebrate and invertebrate taxa and may have important ecological and evolutionary implications. In this study, we measured the degree of individual-level variation in prey preference of the hunting wasp Trypoxylon albonigrum, which inhabits the Atlantic Forest in southeastern Brazil. This wasp captures several orb-weaving spider genera to provision nests. Individuals consistently specialized on a narrow subset of the prey taxa consumed by the population, indicating the existence of significant individual-level variation in prey preferences. The population niche was broader in the wet season in terms of both prey size and taxa. In the case of prey size, the population niche expansion was achieved via increased individual niche breadths, whereas in the case of prey taxa, individual niches remained relatively constrained, and the population niche expanded via increased interindividual variation. The observed pattern suggests the possibility of functional trade-offs associated with the taxon of the consumed prey. The nature of the trade-offs remains unknown, but they are likely related to learning in searching and/or handling prey. We hypothesize that by specializing on specific prey taxa, individuals increase foraging efficiency, reducing foraging time and ultimately increasing reproductive success.