Olfaction-based anthropophily in a mosquito-specialist predator

Evarcha culicivora is an unusual salticid spider because it feeds indirectly on vertebrate blood by choosing blood-carrying mosquitoes as preferred prey. Its preferred mosquitoes are Anopheles, the genus to which all human malaria vectors belong. Here, we show that human odour, which is known to be salient to malaria vectors, is also salient to the adults and juveniles of E. culicivora. Test spiders spent more time in the vicinity of a source of human odour (previously worn socks) when the alternative was unworn socks.     

Adaptive Timing as a Component of a Mosquito-Eating predator’s Specialization Profile

Evarcha culicivora, a salticid spider from East Africa, is a mosquito specialist which feeds indirectly on vertebrate blood by actively choosing blood-carrying mosquitoes as preferred prey and by actively choosing Anopheles as preferred mosquitoes. Here we investigate for the first time whether specialization by this predator is also expressed in the timing of its predatory activity. With data from field sampling and from systematically observing E. culicivora under semi-field conditions, we show that instances of predation tend to be most common in the early morning hours, this being when especially many night-feeding anthropophilic anopheline mosquitoes are resting while digesting blood acquired during the night. Experimental data show that E. culicivora is significantly more responsive to prey in the morning than in the afternoon, where ‘responsive’ includes being significantly more inclined to eat living prey, choose the preferred prey, approach a source of prey odor in the absence of visible prey and approach lures made from dead prey that can be seen but not touched or smelled. We found no significant diel pattern in E. culicivora’s inclination to mate and, although mate, plant and human odors are all known to be salient to E. culicivora, we found no significant diel pattern in response to any of these odors. Our findings suggest that E. culicivora’s innate pattern of predatory activity is adaptively adjusted in a way that facilitates predation on its preferred prey.     

Olfactory search-image use by a mosquito-eating predator

By choosing blood-carrying mosquitoes as prey, Evarcha culicivora, an East African salticid spider, specializes at feeding indirectly on vertebrate blood. It also has an exceptionally complex mate-choice system. An earlier study revealed that search-image use assists E. culicivora in finding prey and mates when restricted to using vision alone. Here we show that search-image use assists E. culicivora in finding prey and mates when restricted to using olfaction alone. After being primed with prey odour or mate odour (control: not primed with odour), spiders were transferred to an olfactometer designed to test ability to find a prey-odour or mate-odour source that was either ‘cryptic’ (i.e. accompanied by a masking odour source, Lantana camara) or ‘conspicuous’ (no L. camara odour). When tested with conspicuous odour, the identity of the priming odour had no significant effect on how many spiders found the odour source. However, when tested with cryptic odour, significantly more spiders found the odour source when primed with congruent odour and significantly fewer spiders found the odour source when primed with incongruent odour.     

Cross‐Modality Effects of Prey Odour During the Intraspecific Interactions of a Mosquito‐Specialist Predator

One of the predictions from evolutionary game theory is that individuals will increase their willingness (i.e. become primed) to escalate aggression when they detect the presence of a limiting resource. Here, we test this prediction in the context of prey odour priming escalation decisions during vision‐based encounters by Evarcha culicivora. This East African jumping spider (Salticidae) feeds indirectly on vertebrate blood by actively choosing blood‐carrying female mosquitoes as preferred prey. Unlike many salticid species, it also expresses pronounced mutual mate choice. As predicted, we show here that, in the presence of odour from their preferred prey, both sexes of E. culicivora escalate during vision‐based same‐sex encounters. This is further evidence that the odour of blood‐carrying mosquitoes is salient to this salticid. For both sexes of E. culicivora, this particular prey may be a resource that matters in the context of intrasexual selection.     

The Functioning of Species-Specific Olfactory Pheromones in the Biology of a Mosquito-Eating Jumping Spider from East Africa

Having unique, complex eyes and vision based on exceptional spatial acuity, salticid spiders are known for their vision-based predatory and mating strategies. Yet Evarcha culicivora, the salticid we consider here, is known for predatory and mating strategies based strongly on the interplay of vision and olfaction. This unusual East African species feeds indirectly on vertebrate blood by choosing blood-carrying female mosquitoes as preferred prey, which it can identify by sight and by smell. Moreover, E. culicivora’s mating strategy is unusual because, unlike the prevailing general pattern among spiders, where males are more active in courtship and females are more active in mate choice, both roles are characteristic of both sexes of E. culicivora. There is also an unusual relationship between diet and mating in this species, with blood meals making both sexes more attractive as potential mates. However, findings from the present study demonstrate that, regardless of source-spider diet and even when restricted to using chemoreception in the absence of seeing another spider, both sexes can discriminate between opposite-sex conspecifics and opposite-sex heterospecifics. Yet there is no evidence that diet (blood versus no blood) influences the attractiveness of opposite-sex heterospecific individuals to E. culicivora. Evidence that the odor of opposite-sex conspecifics is salient to E. culicivora comes from three different experimental designs (retention testing, choice testing and courtship-initiation testing). The effective odor source can be either the presence of the spider or the presence of the spider’s draglines alone.     

Complex display behaviour of Evarcha culicivora,an East African mosquito‐eating jumping spider

Abstract

Evarcha culicivora, an East African jumping spider (Salticidae), is an unusual predator because it feeds indirectly on vertebrate blood by choosing blood‐carrying mosquitoes as preferred prey. It also associates with particular plant species, Lantana camara and Ricinus communis. Here we document this species’ exceptionally complex display repertoire. In common with many other salticids, E. culicivora exhibits pronounced courtship versatility, with males using different tactics depending on the female's location and state of maturity. However, in contrast to most other salticids that have been studied, the males and the females of E. culicivora are both active at initiating and sustaining courtship, and both sexes are cannibalistic. Contrary to the emphasis in the literature on female spiders eating males, females of E. culicivora run a higher risk of being killed by males than vice versa during courtship. E. culicivora males also differ from other salticids that have been studied by adopting pronounced copulatory courtship. Male‐female interactions of E. culicivora are especially complex when encounters are in the foliage of L. camara and R. communis.     

Lack of prey switching and strong preference for mosquito prey by a temporary pond specialist predator

1. The strengths of trophic interactions within ecosystems can be mediated by complex mechanisms that require elucidation if researchers are to understand and predict population- and community-level stabilities. Where multiple prey types co-occur, prey switching (i.e. frequency-dependent predation) by predators may facilitate low-density prey refuge effects which promote coexistence. On the other hand, lack of switching and strong preferences by predators can strongly suppress prey populations, which is especially important considering vector species such as mosquitoes. 2. The present study quantifies prey switching and preference patterns of the temporary pond specialist copepod Lovenula raynerae towards larvae of the medically important Culex pipiens mosquito complex in the presence of different proportions of alternative Daphnia pulex prey. Further, it examines whether prey switching and preferences are contingent on the sex of the predator. 3. Lovenula raynerae exhibited a lack of prey switching and strong preference for larval mosquito prey overall, irrespective of predator sex. Also, when larval mosquitoes were available in higher proportions over daphniids, the strength of this positive selectivity increased. There was very little low-density refuge for mosquitoes where they were rare. 4. Lack of prey switching and strong preferences towards mosquitoes by predatory paradiaptomid copepods may enhance population-level regulation of disease vector mosquitoes that exploit temporary pond-style habitats. Accordingly, the conservation and promotion of these predators might enable better management of medically important species across landscapes.     

Seasonal Diet and Prey Preference of the African Lion in a Waterhole-Driven Semi-Arid Savanna

Large carnivores inhabiting ecosystems with heterogeneously distributed environmental resources with strong seasonal variations frequently employ opportunistic foraging strategies, often typified by seasonal switches in diet. In semi-arid ecosystems, herbivore distribution is generally more homogeneous in the wet season, when surface water is abundant, than in the dry season when only permanent sources remain. Here, we investigate the seasonal contribution of the different herbivore species, prey preference and distribution of kills (i.e. feeding locations) of African lions in Hwange National Park, Zimbabwe, a semi-arid African savanna structured by artificial waterholes. We used data from 245 kills and 74 faecal samples. Buffalo consistently emerged as the most frequently utilised prey in all seasons by both male (56%) and female (33%) lions, contributing the most to lion dietary biomass. Jacobs’ index also revealed that buffalo was the most intensively selected species throughout the year. For female lions, kudu and to a lesser extent the group “medium Bovidae” are the most important secondary prey. This study revealed seasonal patterns in secondary prey consumption by female lions partly based on prey ecology with browsers, such as giraffe and kudu, mainly consumed in the early dry season, and grazers, such as zebra and suids, contributing more to female diet in the late dry season. Further, it revealed the opportunistic hunting behaviour of lions for prey as diverse as elephants and mice, with elephants taken mostly as juveniles at the end of the dry season during droughts. Jacobs’ index finally revealed a very strong preference for kills within 2 km from a waterhole for all prey species, except small antelopes, in all seasons. This suggested that surface-water resources form passive traps and contribute to the structuring of lion foraging behaviour.     

Some population consequences of variation in preference among individual predators

A number of foraging studies have demonstrated that populations of predators rarely consist of individuals with identical preferences for particular types of prey. Variation among predators can lead to frequency-dependent changes in population preference, because those predators mat prefer the rarer type of prey generally have the greatest influence on population preference. In this study we develop a series of theoretical models which demonstrate how anti-apostatic selection (i.e. selection against the rare form) can arise out of (a) bimodal and (b) normal variation in preference among individuals of the same species. We show that population level anti-apostatic selection can occur even when individual predators show pro-apostatic selection (i.e. selection against the common form). Furthermore, patterns of population prey selection that arise out of variation in preference can potentially be pro-apostatic over one range of relative densities and anti-apostatic over another range of relative densities. Finally, we examine a case study involving predation by female waterboatmen Notonecta glauca and show that the variation in preference in this species is large enough to generate higher anti-apostatic selection than would be expected from the diet selected by the average individual.     

Prey preference of the predatory mite Neoseiulus womersleyi Schicha is determined by spider mite webs

Abstract:  We experimentally verified a proximate cause for the preference of prey species by the predatory mite Neoseiulus womersleyi , which prefers the eggs of Amphitetranychus viennensis Zacher to those of Tetranychus urticae Koch. To separate the effects of spider mite eggs and spider mite webs on the prey preference of the predatory mite, we manipulated combinations of eggs and webs of the two prey species. The number of eggs consumed by adult female N. womersleyi was compared with respect to two factors: eggs of the same species under webs of the different species and eggs of different species under webs of the same species. The results revealed that the prey preference of N. womersleyi was determined by the webs, and not by the eggs.     

Innate preference or opportunism: mosquitoes feeding on birds of prey at the Southeastern Raptor Center

The amplification of mosquito‐borne pathogens is driven by patterns of host use by vectors. While each mosquito species is innately adapted to feed upon a particular group of hosts, this “preference” is difficult to assess in field‐based studies, because factors such as host defenses and spatial and temporal overlap of mosquitoes and hosts affect which host animals actually get bitten. Here we examined patterns of host use by mosquitoes feeding on caged raptors at a rehabilitation and education center for birds of prey in Alabama, U.S.A. PCR‐based techniques were used to determine the host species fed upon. Of 19 raptor species at the facility, seven were found to be fed upon by mosquitoes. Feeding indices and linear regression indicated that no species or family of raptor were significantly preferred over another (R²=0.46). Relative abundance adjusted for bird size explained a statistically significant amount of the variation in relative host use (R²=0.71), suggesting that bird size is an important component of host selection by mosquitoes. These findings support the hypothesis that traits of host animals drive patterns of host use by mosquitoes in nature, an interaction that leads to amplification of mosquito‐borne viruses.     

The Attentive Spider: Search‐Image Use by a Mosquito‐Eating Predator

Evarcha culicivora, a jumping spider from East Africa, feeds indirectly on vertebrate blood by choosing blood‐carrying female mosquitoes as prey. It also has an unusually complex mate‐choice system. Here, we show that both sexes of E. culicivora can use mate‐finding search images and also use prey‐finding search images. In experiments, individuals were primed by seeing blood‐carrying mosquitoes, primed by seeing potential mates or not primed (control: saw neither). They were then introduced into an arena where the task was to find a blood‐carrying mosquito or a potential mate. In all instances, the prey or potential mates were dead individuals used as lures. The lure in the arena was either cryptic (i.e. hidden behind nylon netting and accompanied by distractors) or conspicuous (i.e. netting and distractors absent). When lures were conspicuous, the identity of the priming stimulus appeared to be irrelevant. However, when lures were cryptic, significantly more spiders found the lure that was congruent with the priming stimulus and significantly fewer spiders found the lure that was incongruent with the priming stimulus. On this basis, we conclude that the spiders were using search images for finding the lures and that search images were relevant only when the lure to be found was cryptic.     

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.     

Predation by odonates depresses mosquito abundance in water-filled tree holes in Panama

In the lowland moist forest of Barro Colorado Island (BCI), Panama, larvae of four common species of odonates, a mosquito, and a tadpole are the major predators in water-filled tree holes. Mosquito larvae are their most common prey. Holes colonized naturally by predators and prey had lower densities of mosquitoes if odonates were present than if they were absent. Using artificial tree holes placed in the field, we tested the effects of odonates on their mosquito prey while controlling for the quantity and species of predator, hole volume, and nutrient input. In large and small holes with low nutrient input, odonates depressed the number of mosquitoes present and the number that survived to pupation. Increasing nutrient input (and consequently, mosquito abundance) to abnormally high levels dampened the effect of predation when odonates were relatively small. However, the predators grew faster with higher nutrients, and large larvae in all three genera reduced the number of mosquitoes surviving to pupation, even though the abundance of mosquito larvae remained high. Size-selective predation by the odonates is a likely explanation for this result; large mosquito larvae were less abundant in the predator treatment than in the controls. Because species assemblages were similar between natural and artificial tree holes, our results suggest that odonates are keystone species in tree holes on BCI, where they are the most common large predators. Received: 4 November 1996 / Accepted: 11 April 1997     

Do phytoseiid mites select the best prey species in terms of reproductive success?

Optimal foraging theory predicts that predators prefer those prey species that are most rewarding in terms of reproductive success, which is dependent on prey quality and prey availability. To investigate which selection pressures may have moulded prey preference in an acarine system consisting of two prey species and three predator species, we tested whether prey preference of the predators is matched by the associated reproductive success.The predators involved areAmblyseius finlandicus (Oudemans),Am. potentillae (Garman) andTyphlodromus pyri Scheuten. The prey species are the apple rust mite (Aculus schlechtendali (Nalepa)) and the fruit-tree red spider mite (Panonychus ulmi (Koch)).Reproductive success was assessed in terms of intrinsic rate of increase and for one predator also in terms of diapause induction. All three predator species reached highest reproductive success on the same prey species: apple rust mite. This was most pronounced for the predatorAm. finlandicus, because its larval stage suffered severe mortality when feeding onP. ulmi.An independent study on prey preference of the three predator species (Dicke et al., 1988) revealed thatAm. finlandicus prefersAc. schlechtendali toP. ulmi, whereas the other two predator species have the reverse preference.Thus, on the basis of current data, prey preference ofAm. finlandicus can be understood in terms of reproductive success. However, this is not so for prey preference ofT. pyri andAm. potentillae. Investigations needed for a better understanding of prey preference of the last-named two predator species are discussed.     

Gape-limitation,foraging tactics and prey size selectivity of two microcarnivorous species of fish

Summary Patterns of prey size selectivity were quantified in the field for two species of marine microcarnivorous fish, Embiotoca jacksoni and Embiotoca lateralis (Embiotocidae) to test Scott and Murdoch's (1983) size spectrum hypothesis. Two mechanisms accounted for observed selectivity: the relative size of a fish in relation to its prey, and the type of foraging behavior used. Juvenile E. jacksoni were gape limited and newborn individuals achieved highest selectivity for the smallest prey size by using a visual picking foraging strategy. As young E. jacksoni grew, highest preference shifted to the next larger prey sizes. When E. jacksoni reached adulthood, the principal mode of foraging changed from visual picking to relatively indiscriminant winnowing behavior. The shift in foraging behavior by adults was accompanied by a decline in overall preference for prey size; sizes were taken nearly in proportion to their relative abundance. Adult E. lateralis retained a visual picking strategy and achieved highest selectivity for the largest class of prey. These differences in selectivity patterns by adult fish were not explained by gape-limination since adults of both species could ingest the largest prey items available to them. These results support Scott and Murdoch's (1983) hypothesis that the qualitative pattern of size selectivity depends largely on the range of available prey sizes relative to that a predator can effectively harvest.     

Prey preferences of six species of Carabidae (Coleoptera) and one Lycosidae (Araneae) commonly found in UK arable crop fields

Abstract: Laboratory experiments were used to determine the feeding preferences of six carabid beetles and one lycosid spider on aphid and collembolan prey. The first investigation used only five species of carabid Pterostichus melanarius Illiger, Pterostichus madidus F., Harpalus rufipes DeGeer, Nebria brevicollis F. and Carabus violaceus L., which had been caught most commonly in pitfall traps in the headland region of arable crop fields. When offered Brevicoryne brassicae L., Sitobion avenae F., Metopolophium dirhodum Walker and Rhopalosiphum padi L. as prey items, the species consistently consumed in high numbers was M. dirhodum . In subsequent experiments four carabids Pterostichus cupreus L., P. melanarius, P. madidus. H. rufipes and a lycosid spider Trochosa ruricola DeGeer whose distribution was shown by pitfall trapping to extend throughout the arable crop, were the chosen predators. These predators were offered a choice between M. dirhodum and entomobryid collembolans (a recognised alternative prey item) to gauge their preference between the two prey types. Both male and female P. cupreus and P. melanarius showed a significant preference for the aphid prey, while there was no significant preference displayed by the other species. The effect of temperature on the voracity of these five predators fed on M. dirhodum was investigated. There were significant differences in the number of aphids consumed by the species and sexes at the different temperatures. Regression analysis on the mean numbers of aphids eaten by each sex of the five predators, showed that in the majority of cases there was a significant increase in predation with increasing temperature. In considering the dietary preferences illustrated by these experiments, it appeared that P. cupreus and P. melanarius offered the greatest potential in controlling aphids on arable crops.     

Food imprinting and subsequent prey preference in the lynx spider,Oxyopes salticus (Araneae: Oxyopidae)

This object of this study was to determine if early feeding experience can affect subsequent prey choice in lynx spiderlings (Oxyopes salticus), and if so, is it evidence for food/olfactory imprinting. After emergence from the egg sac, three groups of 10 spiderlings were each fed exclusively for a 1-week period on one of three naturally-occurring prey species (crickets): group 1 fed on nymphs of Gryllotalpa hexadactyla; group 2 (Dialeurodes citrifoli); group 3 (Microcentrum rhombifolium). Following this, they were tested for subsequent prey preference in choice tests conducted in a plastic arena. Each spiderling was presented simultaneously with one individual of each prey species in a randomized design. Spiderlings exhibited a significant first preference for the original diet. Thus, experience with certain foods encountered by newly hatched spiderlings can affect subsequent prey preference in this species. Given the primacy of the early experience, the results are best interpreted in terms of imprinting and represent the first demonstration of olfactory imprinting in a spider.     

Prey selectivity of Piona exigua,a planktonic water mite

Summary Females, males and nymphs of Piona exigua were observed during prey capture and ingestion. The encounter radius of the mite was very small, allowing the escape of some crustaceans, such as the calanoid copepod Boeckella. Cladocerans, such as Bosmina or Chydorus, with little or no pre-contact escape response were the most vulnerable to mite predation. Preference values in size-selection experiments varied widely between individual mites. Adult mites presented with two sizes of Daphnia carinata generally preferred the smaller prey. When four sizes were presented simultaneously, however, the preferences of female mites for each size were not significantly different. Patterns of prey selection varied with predator age and sex; for example, female mites preferred Daphnia to Simocephalus, Ceriodaphnia and Chydorus, while nymphs showed a strong preference for Chydorus over Ceriodaphnia. When two prey types were present in equal proportions, differences in total prey density (range 5 or 10/1 – 30 or 50/1) did not alter preferences between the prey species. The preference of female mites for a particular prey type generally increased with increasing relative abundance of the prey type in each of three experiments (Daphnia: Ceriodaphnia, Ceriodaphnia: Chydorus, and Daphnia: Simocephalus). These results imply switching behaviour in these mites. Our results indicate the value of direct observation of predatory behaviour as an adjunct to prey selection experiments. It is also apparent that predatory behaviour in the presence of more than one prey type may not be predictable from that observed in single-prey situations. Predation rates on particular prey species were sometimes reduced in the presence of another species. The relative proportions of prey eaten when two species were present could not be predicted from the number of each species eaten when they were presented separately.