Out of the Frying Pan and into the Fire: a Novel Trade-Off for Batesian Mimics

A mimicry system was investigated in which the models were ants (Formicidae) and both the mimics and the predators were jumping spiders (Salticidae). By using motionless lures in simultaneous‐presentation prey‐choice tests, how the predators respond specifically to the static appearance of ants and ant mimics was determined. These findings suggest a rarely considered adaptive trade‐off for Batesian mimics of ants. Mimicry may be advantageous when it deceives ant‐averse potential predators, but disadvantageous in encounters with ant‐eating specialists. Nine myrmecophagic (ant‐eating) species (from Africa, Asia, Australia and North America) and one araneophagic (spider‐eating) species (Portia fimbriata from Queensland) were tested with ants (five species), with myrmecomorphic (ant‐like) salticids (six species of Myrmarachne) and with non‐ant‐like prey (dipterans and ordinary salticids). The araneophagic salticid chose an ordinary salticid and chose flies significantly more often than ants. Portia fimbriata also chose the ordinary salticid and chose flies significantly more often than myrmecomorphic salticids. However, there was no significant difference in how P. fimbriata responded to ants and to myrmecomorphic salticids. The myrmecophagic salticids chose ants and chose myrmecomorphic salticids significantly more often than ordinary salticids and significantly more often than flies, but myrmecophagic salticids did not respond significantly differently to myrmecomorphic salticids and ants.     

Conditional use of honest signaling by a Batesian mimic

Jumping spiders (Salticidae) usually avoid ants, but some specieswithin this family single out ants as preferred prey, whileothers (especially the species in the genus Myrmarachne) areBatesian mimics of ants. Field records show that ant-eatingsalticids sometimes prey on Myrmarachne, suggesting that theunwanted attention of predators that specialize on the modelmay be an important, but poorly understood, cost of Batesianmimicry. By staging encounters in the laboratory between livingant-eating salticids and Myrmarachne, we determined that ant-eatingsalticids attack Myrmarachne. However, when Myrmarachne detectsa stalking ant-eating salticid early enough, it adopts a distinctivedisplay posture (legs almost fully extended, elevated 45°,and held out to the side 45°), and this usually deters thepredator. When Myrmarachne detects an ant-eating salticid beforestalking begins, Myrmarachne makes preemptive displays thatappear to inhibit the initiation of stalking. Using immobilelures made from dead Myrmarachne that were either in a displayposture or a nondisplay posture, we ascertained that specificallythe display posture of Myrmarachne deters the initiation ofstalking (ant-eating salticids stalked nondisplaying more oftenthan displaying lures). In another experiment, we ascertainedthat it is specifically the interjection of display posturethat deters stalking. When ant-eating salticids that had alreadybegun stalking experienced lures that switched from a nondisplayto a display posture, they stopped stalking. Although the unwantedattentions of its models' predators may be, for Myrmarachne,a hidden cost of Batesian mimicry, Myrmarachne appears to havean effective defense against these predators.     

Effect of sex and bright coloration on survival and predator‐induced wing damage in an aposematic lantern fly with startle display

1. Aposematic coloration in prey promotes its survival by conspicuously advertising unpalatability to predators. Although classical examples of aposematic signals involve constant presentation of a signal at a distance, some animals suddenly display warning colours only when they are attacked. 2. Characteristics of body parts suddenly displayed, such as conspicuous coloration or eyespot pattern, may increase the survival of the prey by startling the predator, and/or by signalling unpalatability to the predators at the moment of attack. 3. The adaptive value of such colour patterns suddenly displayed by unpalatable prey has not been studied. We experimentally blackened the red patch in the conspicuous red–white–black hindwing pattern displayed by an unpalatable insect Lycorma delicatula White (Hemiptera: Fulgoridae) in response to predator's attack. 4. There was no evidence that the presence of the red patch increased prey survival over several weeks. We hypothesise that predators generalised from the red–white–black patches on the hindwings of unpalatable L. delicatula to any similar wing display as a signal of unpalatability. Because a higher proportion of males than females stay put at their resting sites, displaying their wings in response to repeated attacks by predators, wing damage was more frequent in males than in females. 5. To our knowledge, this is the first experimental test of an adaptive role of aposematic signals presented by unpalatable prey during sudden displays triggered by direct predatory attack.     

Predatory Attacks to the Head vs. Body Modify Behavioral Responses of Garter Snakes

An animal's response to predatory attack may depend upon which part of its body is the focus of that attack, because of differential vulnerability to injury. Many avian and mammalian predators direct attacks preferentially toward the prey's head, so simulated attacks that do not have this focus may elicit non‐natural responses. We ‘pecked’ 152 free‐ranging adult male garter snakes (Thamnophis sirtalis parietalis) in Manitoba either on the head or the midbody, and recorded their responses. The snakes’ antipredator tactics were affected not only by body size (larger snakes performed threat displays more often) and body temperature (hotter snakes were more likely to flee), but also by location of the attack. Pecks to the head generally resulted in snakes coiling and hiding their heads, often simultaneously elevating and wriggling their tails in an apparent distraction display. In contrast, pecks to the midbody stimulated either escape responses, or (in snakes that did not flee) open‐mouthed threat displays. More generally, antipredator tactics may respond in flexible ways to details of the predator–prey encounter (including attributes of the habitat as well as the morphology and behavior of both participants) and hence, experimental studies need to carefully simulate such details. The part of the body under attack may be an important factor in this respect.     

Comparative biology of Portia africana,P. albimana,P. fimbriata,P. labiata,and P. shultzi,araneophagic, web-building jumping spiders (Araneae: Salticidae): Utilisation of webs,predatory versatility,and intraspecific interactions

Abstract

Portia is a behaviourally complex and aberrant salticid genus. The genus is of unusual importance because it is morphologically primitive. Five species were studied in nature (Australia, Kenya, Malaysia, Sri Lanka) and in the laboratory in an effort to clarify the origins of the salticids and of their unique, complex eyes. All the species of Portia studied were both web builders and cursorial. Portia was also an araneophagic web invader, and it was a highly effective predator on diverse types of alien webs. Portia was an aggressive mimic, using a complex repertoire of vibratory behaviour to deceive the host spiders on which it fed. The venom of Portia was unusually potent to other spiders; its easily autotomised legs may have helped Portia escape if attacked by its frequently dangerous prey. Portia was also kleptoparasitic and oophagic when occupying alien webs. P. fimbriata from Queensland, where cursorial salticids were superabundant, used a unique manner of stalking and capturing other salticids. The display repertoires used during intraspecific interactions were complex and varied between species. Both visual (typical of other salticids) and vibratory (typical of other web spiders) displays were used. Portia copulated both on and away from webs and frequently with the female hanging from a dragline. Males cohabited with subadult females on webs, mating after the female matured. Adult and subadult females sometimes used specialised predatory attacks against courting or mating males. Sperm induction in Portia was similar to that in other cursorial spiders. Portia mimicked detritus in shape and colour, and its slow, mechanical locomotion preserved concealment. Portia occasionally used a special defensive behaviour (wild leaping) if disturbed by a potential predator. Two types of webs were spun by all species (Type 1, small resting platforms; Type 2, large prey-capture webs). Two types of egg sacs were made, both of which were highly aberrant for a salticid. Responses of different species and both sexes of Portia were quantitatively compared for different types of prey. Many of the trends in behaviour within the genus, including quantitative differences in predatory behaviour, seemed to be related to differences in the effectiveness of the cryptic morphology of Portia in concealing the spider in its natural habitat (‘effective crypsis’). The results of the study supported, in general, Jackson & Blest’s (1982a) hypothesis of salticid evolution which, in part, proposes that salticid ancestors were web builders with poorly developed vision and that acute vision evolved in conjunction with the ancestral spiders becoming proficient as araneophagic invaders of diverse types of webs.     

The biology of ant-like jumping spiders: intraspecific interactions of Myrmarachne lupata (Araneae, Salticidae)

Myrmarachne lupata is an ant-like salticid in which males have very large chelicerae. The display repertoire of this species is unusually large and complex for a salticid spider. Each individual male uses one of three different mating tactics depending on the female's maturity and location. With adult females outside nests type 1 courtship occurs which seems to be a form of visual communication and includes specialized movements and postures of the legs, palps and body. With adult females inside nests, males use type 2 courtship, which seems to be a form of non-visual communication and consists primarily of probing with the legs on the silk; males mate with receptive females inside the nests. With subadult females, males first use type 2 courtship then spin an adjacent silken chamber and cohabit. After she moults and matures, mating occurs inside the nest. Vacant nests of conspecific females, but not those of another sympatric salticid species, elicit courtship behaviour from males. During male-male interactions, embracing occurs with the large chelicerae spread apart. Females and subadults also display, and different displays occur in interactions depending on the sex/age classes of the spiders involved. Despite the unusual morphology of these spiders, their individual displays are similar to those of more typical salticids. During copulation males stand beside the female instead of over or on her as occurs with typical salticids.     

Prey classification by an araneophagic ant-like jumping spider (Araneae: Salticidae)

What to attack is one of the most basic decisions predators must make, and these decisions are reliant upon the predator's sensory and cognitive capacity. Active choice of spiders as preferred prey, or araneophagy, has evolved in several distantly related spider families, including jumping spiders (Salticidae), but has never been demonstrated in ant-like jumping spiders. We used prey-choice tests with motionless lures to investigate prey-choice behaviour in Myrmarachne melanotarsa , an East African ant-like salticid that normally lives in aggregations and often associates with other spider species. We show that M . melanotarsa chooses spiders as prey in preference to insects and, furthermore, discriminates between different types of spiders. Myrmarachne melanotarsa 's preferred prey were juvenile hersiliids and its second most preferred were other salticids. To date, all documented examples of araneophagic salticids have been from the basal subfamily Spartaeinae. Myrmarachne melanotarsa is the first non-spartaeine and also the first ant-like salticid for which araneophagy has been demonstrated.     

Aggressive use of Batesian mimicry by an ant-like jumping spider

Batesian and aggressive mimicry are united by deceit: Batesian mimics deceive predators and aggressive mimics deceive prey. This distinction is blurred by Myrmarachne melanotarsa, an ant-like jumping spider (Salticidae). Besides often preying on salticids, ants are well defended against most salticids that might target them as potential prey. Earlier studies have shown that salticids identify ants by their distinctive appearance and avoid them. They also avoid ant-like salticids from the genus Myrmarachne. Myrmarachne melanotarsa is an unusual species from this genus because it typically preys on the eggs and juveniles of ant-averse salticid species. The hypothesis considered here is that, for M. melanotarsa, the distinction between Batesian and aggressive mimicry is blurred. We tested this by placing female Menemerus sp. and their associated hatchling within visual range of M. melanotarsa, its model, and various non-ant-like arthropods. Menemerus is an ant-averse salticid species. When seeing ants or ant mimics, Menemerus females abandoned their broods more frequently than when seeing non-ant-like arthropods or in control tests (no arthropods visible), as predicted by our hypothesis that resembling ants functions as a predatory ploy.     

The seasonal distribution and characteristics of bush fly Musca vetustissima Walker populations in south-western Australia

In the agricultural region of south-western Australia the bush fly Musca ventustissima Walker was found to occur permanently in the north-eastern half but it died out during winter in the south-west. The abundance of bush flies increased rapidly throughout the overwintering zone in early spring as a result of local breeding. Flies then dispersed south-westwards, completely repopulating the region during October. Immigrant flies were large and therefore highly fecund, and of advanced reproductive maturity. Local breeding then rapidly increased the population. Maximum abundance occurred in mid-spring in the north and east and in early summer in the south and west. Abundance was greatest in the north where large overwintering populations occurred, and in the far south where repopulation occurred early in the seasonal cycle of pasture growth so that the more favourable cattle dung produced flies that were more fecund than their immigrant parents. The abundance of bush flies declined throughout the region in summer, to negligible levels near the south-west coast but, paradoxically, higher levels occurred inland where there were fewer cattle. On average, flies were smaller and reproductively younger in summer. In areas where irrigated pastures produced more favourable dung in summer, the patterns of abundance and other characteristics of flies did not differ substantially from those in comparable non-irrigated areas. The abundance and other characteristics of a bush fly population 10 km from a cattle-grazing breeding site were similar to those at the site, indicating that constant dispersal is the basis of the bush fly's ubiquity.     

Evidence for sexual isolation as a prezygotic barrier to gene flow between morphologically divergent species of Rhagoletis fruit flies

1. Certain groups of fruit flies in the genus Rhagoletis (Diptera: Tephritidae) are exemplars for sympatric speciation via host plant shifting. Flies in these species groups are morphologically similar and overlap in their geographic ranges, yet attack different, non‐overlapping sets of host plants. Ecological adaptations related to differences in host choice and preference have been shown to be important prezygotic barriers to gene flow between these taxa, as Rhagoletis flies mate on or near the fruit of their respective host plants. Non‐host‐related assortative mating is generally absent or present at low levels between these sympatrically diverging fly populations. 2. However, some Rhagoletis taxa occasionally migrate to ‘non‐natal’ plants that are the primary hosts of other, morphologically differentiated fly species in the genus. These observations raise the question of whether sexual isolation may reduce courtship and copulation between morphologically divergent species of Rhagoletis flies, contributing to their prezygotic isolation along with host‐specific mating. 3. Using reciprocal multiple‐choice mating trials, we measured sexual isolation among nine species pairs of morphologically differentiated Rhagoletis flies. Complete sexual isolation was observed in eight of the nine comparisons, while partial sexual isolation was observed in the remaining comparison. 4. We conclude that sexual isolation can be an effective prezygotic barrier to gene flow contributing to substantial reproductive isolation between many morphologically distinct Rhagoletis species, even in the absence of differential host plant choice and host‐associated mating.     

Bugs with backpacks deter vision-guided predation by jumping spiders

As a case study of how insects use masks as a defence against vision-guided predators, an experimental study was carried out using Acanthaspis petax , a reduviid bug ('ant bug') that covers itself with a 'mask', or 'backpack', made from carcasses of its preferred prey (ants), and three salticid spider species, Hyllus sp., Plexippus sp. and Thyene sp., salticids being predators with exceptionally acute vision. The ant bugs and the salticids were from the Lake Victoria region of East Africa. In each test, a salticid was presented with a live bug or a lure made from a dead bug, with the mask removed ('naked') or intact ('masked'). Salticids made predatory responses to naked bugs significantly more often than to masked bugs. These findings suggest that salticids readily identify naked bugs as prey, but fail to identify masked bugs as prey.     

Vibrio cholerae laboratory infection of the adult house fly Musca domestica

The present study was designed to test the hypothesis that house flies may be capable of specifically harbouring ingested Vibrio cholerae in their digestive tracts. Flies were continuously fed green fluorescent protein (GFP)‐labelled, non‐O1/non‐O139 environmental strains of V. cholerae. Bacterial burdens were quantitatively measured using plate counts and localization was directly observed using confocal microscopy. Vibrio cholerae were present in the fly alimentary canal after just 4 h, and reached a plateau of ～10⁷ colony‐forming units (CFU)/fly after 5 days in those flies most tolerant of the pathogen. However, individual flies were resistant to the pathogen: one or more flies were found to carry < 180 V. cholerae CFU at each time‐point examined. In flies carrying V. cholerae, the pathogen was predominantly localized to the midgut rather than the rectal space or crop. The proportion of house flies carrying V. cholerae in the midgut was dose‐dependent: the continuous ingestion of a concentrated, freshly prepared dose of V. cholerae increased the likelihood that fluorescent cells would be observed. However, V. cholerae may be a transient inhabitant of the house fly. This work represents the first demonstration that V. cholerae can inhabit the house fly midgut, and provides a platform for future studies of host, pathogen and environmental mediators of the successful colonization of this disease vector.     

Sequential Analysis Reveals Behavioral Differences Underlying Female‐Biased Predation Risk in Stalk‐Eyed Flies

Stalk‐eyed flies are classic models of how sexual selection can drive morphological and behavioral elaboration. Exaggerated ornaments born by stalk‐eyed flies could impose locomotor costs and increase susceptibility to predation; however, a previous study determined that behavior, not eye span, was the major influence on predation risk. Despite the importance of behavior, relatively little is known about how these flies avoid and deter predators. We created an ethogram of behaviors and used it to score individual interactions of male and female Teleopsis dalmanni paired with an actively foraging, generalist arachnid predator (Phidippus audax). Sequential analysis was employed to identify temporal patterns in behavior and determine how males and females differ in their approaches to avoiding predation. Our results indicate that males and females significantly differ when specific behaviors were employed. Patterns in the behavioral transitions suggest that males are more aggressive than females and are more likely to approach a predator to jab, abdomen bob, or display. Males elicited more retreat responses from the predator, whereas females elicited more attacks. Although the behavioral repertoires of male and female stalk‐eyed flies are indistinguishable, their uses of the behaviors differ, particularly the sequential order of presentation, suggesting a strong sex difference in anti‐predatory behavior.     

Neuromuscular and hormonal control of post-eclosion processes in flies

Flies (exemplified by Sarcophaga bullata) expand after eclosion from the puparium by processes of “pulsing” (slow rhythmical abdominal contractions) and “pumping” of air (fast rhythmical contractions of the cibarial pump). Pulsing and pumping are inhibited if a newly eclosed fly is kept in an enclosed space (sand, a glass tube, an empty puparium). This inhibition no longer applies if such flies are injected with either hemolymph from flies 10–15 min old or cAMP, or are confined at the age of 10 min. This suggests a hormonal control of pulsing and pumping. Pumping alone, without pulsing, occurs in flies treated with certain paralyzing agents like ether, tetrodotoxin, bee venom, or “FlyNap,” or have the connectives in the neck cut or interrupted by cauterization. Application of FlyNap or neck cauterization leads to excessive pumping which results in bloating. Expansion by bloating is confined to the soft membranes, leaving sclerites and wings largely unexpanded. The function of pulsing is probably that of “plasticizing” and stretching the cuticle to make it respond to increased steady pressure by air-pumping. Flies ligated at the proboscis show almost regular pulsing and pumping, but without intake of air, and consequently no expansion. Cuticle (sclerites) and wings, however, become plasticized. Some plasticization occurs even in the absence, or reduction, of pulsing (in a neck-cauterized fly), brought about by a hormonal process. Eclosion from the puparium is also initiated by a hormonal action. Thus, the following processes during fly emergence are controlled by hormones: eclosion proper, pulsing, pumping, plasticization, and tanning. These hormones are separate entities, with the possible exception of the pulsing/pumping hormone(s).     

Tracing the history and ecological context of Wolbachia double infection in a specialist host (Urophora cardui)—parasitoid (Eurytoma serratulae) system

The endosymbiotic bacterium Wolbachia is the most widespread bacteria in insects, yet the ecology of novel acquisitions in natural host populations is poorly understood. Using temporal data separated by 12 years, I tested the hypothesis that immigration of a parasitoid wasp led to transmission of its Wolbachia strain to its dipteran host, resulting in double‐strain infection, and I used geographic and community surveys to explore the history of transmission in fly and parasitoid. Double infection in the fly host was present before immigration of the parasitoid. Equal prevalence of double infection in males and females, constant prevalence before and after immigration in two regions, and increase in one region of immigration indicate little if no competition between strains. Double infection was present throughout the fly's distribution range, but proportions varied highly (0–0.71, mean = 0.26). Two fly‐specific MLST strains, observed in Eastern and Western Europe, respectively, differed at hcpA only. Flies with either fly‐strain could be double infected with the parasitoid's strain. The geographic distribution of double infection implies that it is older than the fly host's extent distribution range and that different proportions of double infection are caused by demographic fluctuations in the fly. The geographic data in combination with community surveys of infections and strains further suggest that the parasitoid strain was the fly's ancestral strain that was transmitted to the parasitoid, that is, the reverse transmission route as first hypothesized. Based on these findings together with a comparison of oviposition strategies of other hosts harboring related Wolbachia strains, I hypothesize that trans‐infection during an insect host's puparial metamorphosis might be important in promoting horizontal transmission among diverse holometabolic taxa.     

Operant Learning of Drosophila at the Torque Meter

For experiments at the torque meter, flies are kept on standard fly medium at 25°C and 60% humidity with a 12hr light/12hr dark regime. A standardized breeding regime assures proper larval density and age-matched cohorts. Cold-anesthetized flies are glued with head and thorax to a triangle-shaped hook the day before the experiment. Attached to the torque meter via a clamp, the fly''s intended flight maneuvers are measured as the angular momentum around its vertical body axis. The fly is placed in the center of a cylindrical panorama to accomplish stationary flight. An analog to digital converter card feeds the yaw torque signal into a computer which stores the trace for later analysis. The computer also controls a variety of stimuli which can be brought under the fly''s control by closing the feedback loop between these stimuli and the yaw torque trace. Punishment is achieved by applying heat from an adjustable infrared laser.     

SEXUAL SELECTION,VIABILITY SELECTION,AND DEVELOPMENTAL STABILITY IN THE DOMESTIC FLY MUSCA DOMESTICA

Associations between developmental stability, sexual selection, and viability selection were studied in the domestic fly Musca domestica (Diptera, Muscidae). Developmental stability of the wings and tibia of flies of both sexes, measured in terms of their level of fluctuating asymmetry, was positively associated with mating success in free ranging populations and in sexual selection experiments. Mated individuals may have obtained indirect fitness benefits from sexual selection of two different kinds. First, the entomopathogenic fungus Enthomophthora muscae (Zygomycetes, Entomophthorales) infects and kills adult domestic flies, and flies dead from fungus infections had more asymmetric wings than flies dead for other reasons. Experimental deposition of fungus spores on uninfected flies demonstrated that flies with asymmetric wings were more susceptible to fungus infections than flies with symmetric wings. Second, domestic flies were frequently eaten by insectivorous barn swallows Hirundo rustica, and flies depredated by birds had more asymmetric wings and tibia than surviving flies.     

Haltere and visual inputs sum linearly to predict wing (but not gaze) motor output in tethered flying Drosophila

In the true flies (Diptera), the hind wings have evolved into specialized mechanosensory organs known as halteres, which are sensitive to gyroscopic and other inertial forces. Together with the fly''s visual system, the halteres direct head and wing movements through a suite of equilibrium reflexes that are crucial to the fly''s ability to maintain stable flight. As in other animals (including humans), this presents challenges to the nervous system as equilibrium reflexes driven by the inertial sensory system must be integrated with those driven by the visual system in order to control an overlapping pool of motor outputs shared between the two of them. Here, we introduce an experimental paradigm for reproducibly altering haltere stroke kinematics and use it to quantify multisensory integration of wing and gaze equilibrium reflexes. We show that multisensory wing-steering responses reflect a linear superposition of haltere-driven and visually driven responses, but that multisensory gaze responses are not well predicted by this framework. These models, based on populations, extend also to the responses of individual flies.     

The biology of Tauala lepidus,a jumping spider (Araneae: Salticidae) from Queensland: display and predatory behaviour

Abstract

The display and predatory behaviour of Tauala lepidus Wanless, an abundant salticid in north Queensland rainforests, was investigated in the laboratory and, to a lesser extent, in nature. T. lepidus leapt and walked into alien webs to catch spiders and insects, and was captured and fed on by other spiders. Females ate each other’s eggs. During intraspecific interactions, a complex repertoire of displays was used. Courtship versatility occurred, each individual male having a conditional strategy of different behaviours depending on whether the female is at or away from her nest, and whether she is adult or subadult. Yet other combinations of displays occurred during male-male and female-female interactions. Apparently, pheromones on nests and draglines of females released male courtship. Abdomen twitching, a behaviour common to the display repertoires of many salticids, was an especially complex and pervasive behaviour of T. lepidus. T. lepidus also twitched its abdomen when it contacted alien webs and preyed on other species of spiders. The behaviour of T. lepidus is compared to that of Jacksonoides queenslandica Wanless, a species from the same group (Astieae).