Intraguild predation: The dynamics of complex trophic interactions

There is a long-standing debate in ecology concerning the relative importance of competition and predation in determining community structure. Recently, a novel twist has been added with the growing recognition that potentially competing species are often engaged in predator-prey interactions. This blend of competition and predation is called intraguild predation (IGP). The study of IGP will lead to a reconsideration of many classical topics, such as niche shifts, species exclusion and cascading interactions in food webs. Theoretical models suggest that a variety of alternative stable states are likely in IGP systems, and that intermediate predators should tend to be superior in exploitative competition. Many field studies support these expectations. IGP is also important in applied ecological problems, such as the conservation of endangered species and fisheries management.     

Intraguild predation of Orius tristicolor by Geocoris spp. and the paradox of irruptive spider mite dynamics in California cotton

It is paradoxical when a community of several natural enemies fails to control a pest population when it can be shown experimentally that single members of the natural enemy community are effective control agents when tested individually. This is the case for spider mites, Tetranychus spp., in California cotton. Spider mites exhibit irruptive population dynamics despite that fact that experiments have shown that there are at least four predators (Galendromus occidentalis, Frankliniella occidentalis, Orius tristicolor, and Geocoris spp.) that, when tested singly, can suppress mite populations. One possible explanation for the paradox is intraguild predation, wherein one predator consumes another. Here, I evaluate the hypothesis that intraguild predation is a strong interaction among spider mite predators. I report manipulative field experiments, focal observations of freely foraging predators in the field, and population survey data that suggest that the minute pirate bug O. tristicolor, is subject to strong predation by other members of the predator community, and in particular by Geocoris spp. These results, combined with the results of prior work, suggest that pervasive intraguild predation among spider mite predators may explain the pest status of Tetranychus spp. in cotton.     

Intraguild predation by aphidophagous predators on parasitised aphids: the use of multiple video cameras

A video technique that allows simultaneous behavioural observations of several experimental replicates under field and laboratory conditions is described. The technique was used to analyse predation risk of parasitised aphids in a sugar beet field. The images of 16 black and white video cameras were recorded by a video multiplexer in combination with a time-lapse video recorder. Each camera was weather protected and equipped with a single infrared diode to allow observations during night times. Single leaves carrying aphid mummies only or mummies and unparasitised aphids were monitored. All colonies were exposed to predation and parasitation by the community of natural enemies in the field. Colonies with mummies and unparasitised aphids were visited significantly more often by predators than those without additional aphids. Predators also stayed significantly longer in patches with unparasitised aphids. Although an equal proportion of aphid mummies were destroyed in both treatments, the video analysis showed differences in predator species spectrum between treatments. In patches with aphids, coccinellid and hemipteran predators preyed on mummies, while in patches with only mummies, chrysopids accounted for most of the damage. The decrease in parasitoid survival could be attributed to the increasing number of predator visits in aphid patches and to a lesser extent to the decreasing number of unparasitised aphids (alternative prey). Parasitoid survival in colonies without alternative prey was correlated with the number of predator visits and the time predators spent on a leaf.Continuous video observations gave additional behavioural information for the interpretation of field data. Other prospective research fields for the use of the multi video camera technique are outlined and general advantages and disadvantages are discussed.     

Intraguild predation,invertebrate predators,and trophic cascades in lake food webs

The top-down and bottom-up properties of model food webs that include intraguild predation and self-limiting factors such as cannibalism are investigated. Intraguild predation can dampen or even reverse the top-down effects predicted by food chain theory. The degree of self-limitation among the intraguild prey is a key factor in determining the direction and strength of the top-down response. Intraguild predation and self-limiting factors can also substantially alter the bottom-up effects of enrichment. These results can help explain the disparate results of trophic cascade experiments in lakes, where cascades are usually seen when large Daphnia are the primary herbivores, but not when smaller-bodied herbivores are dominant. Top-down manipulations should cascade at least modestly to phytoplankton in those lakes whose food web can be reasonably approximated by a chain (typically, those where Daphnia is the dominant herbivore), as predicted by food chain theory. On the other hand, smaller-bodied zooplankton are often preyed upon heavily by invertebrate predators as well as by planktivorous fish, thereby introducing elements of intraguild predation into these food webs. In this case, conventional food chain theory is likely to give incorrect predictions. Very large cascade effects may be due primarily to regime shifts between intraguild predation-dominated food webs and those that more resemble food chains, rather than due to the simple food chain cascade usually considered.     

Wolbachia affects oviposition and mating behaviour of its spider mite host

Wolbachia bacteria are transmitted from mother to offspring via the cytoplasm of the egg. When mated to males infected with Wolbachia bacteria, uninfected females produce unviable offspring, a phenomenon called cytoplasmic incompatibility (CI). Current theory predicts that ‘sterilization’ of uninfected females by infected males confers a fitness advantage to Wolbachia in infected females. When the infection is above a threshold frequency in a panmictic population, CI reduces the fitness of uninfected females below that of infected females and, consequently, the proportion of infected hosts increases. CI is a mechanism that benefits the bacteria but, apparently, not the host. The host could benefit from avoiding incompatible mates. Parasite load and disease resistance are known to be involved in mate choice. Can Wolbachia also be implicated in reproductive behaviour? We used the two‐spotted spider mite – Wolbachia symbiosis to address this question. Our results suggest that uninfected females preferably mate to uninfected males while infected females aggregate their offspring, thereby promoting sib mating. Our data agrees with other results that hosts of Wolbachia do not necessarily behave as innocent bystanders – host mechanisms that avoid CI can evolve.     

Intraguild interactions and aphid predators: biological efficiency of Harmonia axyridis and Episyrphus balteatus

Introductions of the harlequin ladybird Harmonia axyridis into Belgium for aphid biological control have been followed by declines in native aphid natural enemies. We first examined, in laboratory and field conditions, the impact of larval mobility of either H. axyridis or Episyrphus balteatus, the most abundant native hoverfly in central Europe, on aphid suppression. The hoverfly larvae consumed more aphids (Megoura viciae) in a short term, whereas the ladybird ones were more efficient in a long term. We second investigated the intraguild interactions between H. axyridis and E. balteatus larvae and adults. In larva pairings between the two species in laboratory microcosms containing aphid (M. viciae) infested broad bean (Vicia faba) plants, H. axyridis had an intraguild predation (IGP) advantage over the hoverfly. When conspecific larvae were paired together on aphid‐infested plants, no cannibalism between them was detected. The presence of either H. axyridis or E. balteatus larvae on aphid‐infested plants negatively influenced the ovipositional behaviour of H. axyridis and E. balteatus females; lower numbers of laid eggs were recorded compared to control treatment. Moreover, eggs laid by E. balteatus females were also dropped as victims of predation mainly by H. axyridis larvae. Our results suggest that while the exotic ladybird was more efficient in aphid biological control, larvae and eggs of the native hoverfly species face increased IGP by H. axyridis, which would contribute, as a consequence, to the decline in E. balteatus population following invasion.     

Effects of predation risk on mating behavior of the Kanzawa spider mite

In the Kanzawa spider mite, Tetranychus kanzawai, adult males locate pre-reproductive quiescent females and engage in precopulatory mate guarding. We found that re-reproductive quiescent females preferred to be near veins, rather than other leaf parts, and moreover, adult males spent more time along the vein than on other parts. Consequently, T. kanzawai males found more quiescent females along veins than those on other parts. However, the predatory mite Neoseiulus womersleyi also found more quiescent T. kanzawai females along veins than those on other parts. Moreover, N. womersleyi found more guarding males than solitary males of T. kanzawai. Thus, we experimentally examined the effects of predation risk on the mating behavior of T. kanzawai. The presence of N. womersleyi reduced T. kanzawai female preference for vein vicinity as a quiescent site. Although the predation risk of guarding T. kanzawai males was lower than that of solitary males after detection by predators, the presence of N. womersleyi also reduced the proportion of guarding T. kanzawai males. These results suggest that the possible benefits of preferring vein vicinity as quiescent sites by T. kanzawai females is outweighed by predation risk in the presence of predators, and that the risk of detection by predators would be more important for T. kanzawai males than the risk of being preyed upon.     

Intraguild predation among plant pests: western flower thrips larvae feed on whitefly crawlers

Omnivores obtain resources from more than one trophic level, and choose their food based on quantity and quality of these resources. For example, omnivores may switch to feeding on plants when prey are scarce. Larvae of the western flower thrips Frankiniella occidentalis Pergande (Thysanoptera: Thripidae) are an example of omnivores that become predatory when the quality of their host plant is low. Western flower thrips larvae usually feed on leaf tissue and on plant pollen, but may also attack eggs of predatory mites, their natural enemies, and eggs of the two-spotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae), one of their competitors. Here, we present evidence that western flower thrips larvae prey on Trialeurodes vaporariorum Westwood (Hemiptera: Aleyrodidae), another competitor for plant tissue. We tested this on two host plant species, cucumber (Cucumis sativa L.), considered a host plant of high quality for western flower thrips, and sweet pepper (Capsicum annuum L.), a relatively poor quality host. We found that western flower thrips killed and fed especially on whitefly crawlers and that the incidence of feeding did not depend on host-plant species. The developmental rate and oviposition rate of western flower thrips was higher on a diet of cucumber leaves with whitefly crawlers than on cucumber leaves without whitefly crawlers, suggesting that thrips do not just kill whiteflies to reduce competition, but utilize whitefly crawlers as food.     

Intraguild predation and cannibalism among Dicyphini: Dicyphus cerastii vs. two commercialized species

Dicyphine mirids are one of the most important groups of predators on tomato. In the Mediterranean region, several species in the genera Dicyphus, Macrolophus, and Nesidiocoris (Hemiptera: Miridae, Bryocorinae, Dicyphini) colonize protected horticultural crops. In Portugal, Nesidiocoris tenuis (Reuter) is increasingly abundant in the mirid species complex of tomato crops and appears to be displacing the native Dicyphus cerastii Wagner. In order to know whether intraguild predation (IGP) can explain the decreasing abundance of D. cerastii, we evaluated predatory interactions between adult females and first instars of D. cerastii vs. N. tenuis but also D. cerastii vs. Macrolophus pygmaeus (Rambur), as this species is also naturally present in horticultural crops in Portugal. Cannibalistic interactions were also tested for the same three species. All experiments were performed under laboratory conditions, in Petri dish arenas, in the presence or absence of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) eggs as alternative prey. Predation on both heterospecific and conspecific nymphs occurred only in the absence of alternative food. Intraguild predation was mutual and symmetrical between D. cerastii and M. pygmaeus. However, IGP was asymmetrical between D. cerastii and N. tenuis, favouring the first. Cannibalism was not significantly different among these mirid species. Our results show that D. cerastii has a greater capacity to feed on intraguild prey than N. tenuis. Therefore, IGP on small nymphs does not explain the abundance shift between D. cerastii and N. tenuis.     

Lima bean�Clady beetle interactions: spider mite mediates sublethal effects of its host plant on growth and development of its predator

Cultivated plants can have negative effects on natural enemies that attack spider mites. In this study, we tested the hypothesis that spider mites mediate effects of a lima bean, Phaseolus lunatus L., cultivar on the life history of a lady beetle Stethorus punctillum Weise. We provisioned laboratory arenas with two-spotted spider mites, Tetranychus urticae Koch, from planters containing Henderson Bush Bean or Fordhook 242 lima bean plants and monitored the growth, development, larval survival, fecundity, and adult life span of predators. We determined the protein content and the linamarin (a cyanogenic glycoside) content in foliage, spider mites, and predators. Predators took longer to develop and were smaller sized when consuming mites from the Henderson foliage. There was no significant mite-mediated effect of cultivar on predator fecundity or life span. Although soluble protein was greater in foliage of the Henderson than the Fordhook cultivar, mites contained less protein when reared on the Henderson, and predators contained less protein when fed with mites from the Henderson. Linamarin content was greater in Henderson than Fordhook foliage, and greater in spider mites and predators in the Henderson treatment. Linamarin in Henderson foliage may reduce the ability of spider mites to utilize plant protein. As a result, prey quality is reduced and predators that feed on these prey (from the Henderson treatment) grow at a slower rate and are smaller sized than their cohorts (from the Fordhook treatment). In conclusion, T. urticae mediates the effects of the Henderson cultivar on S. punctillum development but not fecundity or life span.     

Intraguild interference and biocontrol effects of generalist predators in a winter wheat field

Arable land typically harbours communities of polyphagous invertebrate natural enemies, among them numerous soil-surface dwelling predators such as ground beetles (Carabidae) and spiders (Lycosidae, Linyphiidae). Numbers of these predators were experimentally manipulated in a winter wheat field in order to study the predation impact of a generalist predator assemblage on herbivorous insects, the possible interferences among the predators concerned, and subsequent effects on wheat plant parameters. Removing ground beetles doubled numbers of Lycosidae indicative of intraguild interference between these two predator groups. Aphid densities were highest in carabid removal plots implying a substantial predation impact of ground beetles on the pest population. The predation impact of ground beetles was strongest earlier and disappeared later in the season. In mid-season, at intermediate aphid densities, the combined impact of carabid beetles and spiders appeared to be responsible for the reduction in aphid abundance. This result was probably due to a biomass effect rather than to a synergistic effect of the predator community. Thysanoptera decreased when spiders were removed (perhaps because spiders were preying on a predator of thrips), while Cicadellidae and Delphacidae showed no effect at all. The rise of aphid numbers in carabid removal plots corresponded to an increase in protein content of the wheat grains, while other plant parameters such as plant numbers and grain mass were not affected. In conclusion, this study provided field evidence for intraguild interference among generalist ground predators in arable land. Despite this interference the polyphagous predator community was able to depress numbers of aphids in winter wheat, a result cascading down to plant quality parameters.     

东亚小花蝽对西方花蓟马和二斑叶螨的捕食选择性

多食性天敌对猎物的捕食选择性及猎物密度对天敌捕食的干扰作用直接影响到天敌对不同猎物的控制作用.在实验室条件下研究了东亚小花蝽对西方花蓟马和/或二斑叶螨不同虫态的捕食选择性,以及两猎物中一种猎物的密度变化对小花蝽取食另一种猎物的影响.结果如下:东亚小花蝽5龄若虫和成虫对西方花蓟马2龄若虫的捕食选择性均强于对其成虫,对二斑叶螨的选择性为雌成螨>若螨>幼螨.实验中西方花蓟马2龄若虫是东亚小花蝽最喜好的虫态.二斑叶螨雌成螨密度固定为60头/19.63cm2,西方花蓟马若虫密度从10增加到60时显著地减少了东亚小花蝽对二斑叶螨的取食.反之,固定西方花蓟马同样密度,增加二斑叶螨密度却没有显著改变小花蝽对西方花蓟马的取食.此结果进一步表明,西方花蓟马是东亚小花蝽更喜好的猎物.     

Intraguild predation among larval plethodontid salamanders: a field experiment in artificial stream pools

Intraguild predation can be important in determining community structure and dynamics. Artificial stream pools were used to test for the impacts of intraguild predation among three species of larval plethodontid salamanders. Intraguild predators (large Gyrinophilus porphyriticus and Pseudotriton ruber) significantly decreased the survival of small Pseudotriton ruber. There was a trend toward reduced growth of Pseudotriton and Eurycea cirrigera in the presence of intraguild predators. The presence of large Gyrinophilus significantly reduced the growth rate of large Pseudotriton, both in the absence and presence of intraguild prey. The presence of intraguild prey did not significantly increase the growth rates of the intraguild predators. Intraguild predation is likely to be an important force shaping the evolution and ecology of these salamanders.     

Intraguild predation and sublethal interactions between two zoophytophagous mirids,Macrolophus pygmaeus and Nesidiocoris tenuis

The omnivorous predators Macrolophus pygmaeus and Nesidiocoris tenuis (Hemiptera: Miridae) are important biological control agents of pests on tomato crops. In this study, potential intraguild predation (IGP) interactions between the two species were investigated on tomato. We examined: (a) the within plant distribution of both species in the field, (b) the within plant distribution of each predatory species when co-occurred at high densities on tomato caged plants, (c) their behavioral interactions when enclosed in experimental arenas and (d) the development young and old nymphs of M. pygmaeus when enclosed together with N. tenuis adults. Results revealed that the two predators showed a different distribution pattern on the plants, with N. tenuis exploiting mostly the upper part, whereas M. pygmaeus were mostly observed on the 5th to the 7th leaf from the top. However, when the predators co-occurred, N. tenuis or M. pygmaeus individuals were recorded with increased numbers on the lower or the higher part of the plant, respectively. In the presence of N. tenuis adult young nymphs of M. pygmaeus completed their development to the adult stage, when alternative prey (lepidopteran eggs) was present on the plant, however failed to reach adulthood in the absence of alternative prey. A high percentage of the dead nymphs found with their body fluids totally sucked indicating predation by N. tenuis. However, large 4th instar nymphs of M. pygmaeus were much less vulnerable to N. tenuis than younger. The behavior of N. tenuis was affected by the presence of M. pygmaeus, but at a rate similar to that when two individuals of N. tenuis were enclosed together. Contacts between the predators were recorded in a similar frequency in mono- and heterospecific treatments, whereas aggressive behavior was not observed. This study shows that intraguild interactions between M. pygmaeus and N. tenuis occur but are not intensive. The potential implications of the outcomes for biological control are discussed.     

Comparative toxic and sublethal effects of fluvalinate on two-spotted spider mite and European red mite

Four fluvalinate formulations differed in their residual toxicity to female two-spotted spider mite (TSM), Tetranychus urticae adults; the emulsifiable concentrate (EC) was the most toxic. In contrast, there was little difference in toxicity between the formulations with the European red mite (ERM) Panonychus ulmi with the exception of the EC formulation which was the least toxic. Fluvalinate 2F caused minimal (<10%) TSM and ERM egg mortality. Fluvalinate 2F was more toxic and caused greater larval dispersal for the TSM compared to the ERM at the field concentration and below. The toxicity of fluvalinate 2F to TSM and ERM protonymphs, deutonymphs and adults was low, approximately <20% at field concentration. Dispersal was the main response to fluvalinate and this was positively correlated with increasing concentration. The combined mortality and dispersal LC₅₀ was five times lower for ERM protonymphs and adults, but 11 times higher for ERM deutonymphs compared to equivalent TSM life stages. Fluvalinate 2F reduced TSM development from the protonymph and deutonymph stages to a greater extent compared to the ERM. The mortality response to fluvalinate 2F was unaffected by host type (peach or apple) for the TSM whereas ERM mortality was higher on apple compared to peach. TSM dispersal was higher from apple compared to peach whereas ERM dispersal was similar on both host types. Oviposition by both mite species was lower on apple than peach leaves. A 1 h exposure to fluvalinate 2F reduced ERM oviposition for 12 days.     

Intraguild interactions of aphidophagous predators in fields: effect of Coccinella septempunctata and Episyrphus balteatus occurrence on aphid infested plants

Intraguild relations between beneficial insects have become a major research topic in biological pest control. In order to understand the intraguild competitions between aphidophagous populations in natural conditions, a field experiment was carried out in the experimental farm of the Gembloux Agricultural University. As biological control of pests involve a community of diverse natural enemies, this experiment firstly aimed to assess the aphidophagous predator diversity and abundance in green pea (Pisum sativum) field and secondly to investigate the impact of the large natural occurrence of C. septempunctata on the aphidophagous beneficial dispersion and efficiency as aphid biological control agents in pea field. Visual observations were weekly performed throughout the 2006 growing season. The pea aphids were attacked by several predatory groups, mainly ladybird beetles and hoverflies. Higher densities of ladybirds and hoverflies were recorded in the beginning of July, associated with an aphid occurrence peak. Using net cage system in the field, the particular intraguild relations between added C. septempunctata or E. balteatus and the natural beneficial arrivals and dispersion were observed. The E. batteatus (eggs and larvae) presence inhibited other aphidophagous predators presence on the aphid infested plants. Lower abundance of E. balteatus was observed on aphid infested plants already colonised by C. septempunctata. To explore more accurately the oviposition and predation behaviours of ladybirds and hoverflies and to determine the chemical factors that could influence these behaviours, current researches are performed in laboratory and will be discussed to promote efficient biological control of aphids by natural enemies.     

Cannibalism and interspecific predation in the phytoseiid mites Phytoseiulus persimilis and Neoseiulus californicus: predation rates and effects on reproduction and juvenile development

We examined intra- and interspecific predation of adult females and immature stages of the generalist Neoseiulus californicus and the specialist Phytoseiulus persimilis. Adult females and immatures of both predators exhibited higher predation rates on larvae than on eggs and protonymphs. N. californicus fed more inter- than intraspecifically. Predation on P. persimilis by N. californicus was more severe than vice versa. P. persimilis had higher predation rates on conspecifics than heterospecifics and was more prone to cannibalism than N. californicus. When provided with phytoseiid prey, P. persimilis suffered higher mortality than N. californicus. When held without food, adult females and protonymphs of N. californicus survived longer than the corresponding stages of P. persimilis. N. californicus females were able to sustain oviposition when preying upon P. persimilis, whereas cannibalizing females did not lay eggs. Females of P. persimilis were not able to sustain oviposition, irrespective of con- or heterospecific prey. Immatures of both predators were able to reach adulthood when provided with either con- or heterospecifics. Juvenile development of N. californicus was shorter with heterospecific vs. conspecific larvae; mortality of P. persimilis immatures was less when feeding on conspecific vs. heterospecific larvae. Different behavioral pattern in intra- and interspecific predation are discussed in regard to their feeding types (generalist vs. specialist).     

Inhibition of spider mite ATPases by plictran and three organochlorine acaricides

The ATPase enzyme system from two-spotted spider mites, $\text{Tetranychus}$$\text{urticae}$ (Koch) was sensitive, in vitro, to four acaricides. Tricyclohexylhydroxytin (Plictran^R) was an outstanding inhibitor of oligomycin-sensitive (mitochondrial) Mg²⁺ATPase from fish brain and spider mite homogenates. The I₅₀ values were 6.6×10^?11M and 6.2×10^?10M, respectively. Less effective were chlorbenside, chlorfenethol and ovotran. Plictran at a higher concentration (2×10^?7M) was also more effective on Na⁺-K⁺ATPase both in mites and fish brain homogenates as compared to chlorfenethol, chlorbenside and ovotran. Plictran inhibited oligomycin-insensitive Mg²⁺ATPase at concentrations of 10^?8M but stimulated at high concentrations (5×10^?6M and higher).