HYPERPARASITISM: Multitrophic Ecology and Behavior

Sullivan, Daniel J.; Völkl, Wolfgang

doi:10.1146/annurev.ento.44.1.291

Cited by 205 publications

(211 citation statements)

References 105 publications

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“…This is in addition to the advantages mentioned previously of protection against predators and parasites (Way 1963;Collins & Scott 1982;Buckley 1987aBuckley , 1990Vinson & Scarborough 1991). In compensation, ants also prey upon a range of hyperparasitoids (Sullivan & Völk 1999). Some parasites are able to lure the ants by chemical mimicry of their attended aphids (Liepert & Dettner 1993).…”

Section: Delabiementioning

confidence: 90%

“…Small size, sedentarism, ubiquity and gregarious habits, all contribute to facilitate finding ants, which use them as a stable source of nutrients. On the other hand, the same can be argued to make these insects easy and plentiful hosts for a range of hymenopterous parasites (Carver et al 1991, Sullivan & Völk 1999.…”

Section: Who Are the Partners Of The Trophobiosis And Why Does It Makmentioning

confidence: 99%

“…When this occurs, the fallen honeydew is simply licked by ants (Dejean et al 1996). A range of parasitic wasps of several families specialize in attacking isolated or aggregated Sternorrhyncha or Auchenorrhyncha at different stages: Aphelinidae, Braconidae Aphidiinae, Dryinidae, Encyrtidae, Eupelmidae and Mymaridae (Nixon 1951, Nechols & Seibert 1985, Rozario et al 1992, González-Hernández et al 1999, Sullivan & Völk 1999, Stadler & Dixon 1999, Moya-Raygoza & Nault 2000. Beetles of the family Coccinellidae and Syrphidae flies are among their main predators (Way 1963, Collins & Scott 1982, while spiders have been reported as predators in more recent papers (Cushman & Whitham 1989, Buckley 1990, Cushman & Addicott 1991, Moya-Raygoza & Nault 2000.…”

Section: Diversity and Evolution Of Mutualisms Betweenmentioning

confidence: 99%

See 2 more Smart Citations

Trophobiosis Between Formicidae and Hemiptera (Sternorrhyncha and Auchenorrhyncha): an Overview

Delabie¹

2001

Neotrop. Entomol.

239

246

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Trofobiose Entre Formicidae e Hemiptera (Sternorrhyncha e Auchenorrhyncha):Uma Visão Geral RESUMO -Fêz-se uma revisão sobre a relação conhecida como trofobiose e que ocorre de forma convergente entre formigas e diferentes grupos de Hemiptera Sternorrhyncha e Auchenorrhyncha (até então conhecidos como 'Homoptera'). As principais características dos 'Homoptera' e dos Formicidae que favorecem as interações trofobióticas, tais como a excreção de honeydew por insetos sugadores, atendimento por formigas e necessidades fisiológicas dos dois grupos de insetos, são discutidas. Aspectos da sua evolução convergente são apresentados. O sistema mais arcaico não é exatamente trofobiótico, as forrageadoras coletam o honeydew despejado ao acaso na folhagem por indivíduos ou grupos de 'Homoptera' não associados. As relações trofobióticas mais comuns são facultativas, no entanto, esta forma de mutualismo é extremamente diversificada e é responsável por numerosas adaptações fisiológicas, morfológicas ou comportamentais entre os 'Homoptera', em particular Sternorrhyncha. As trofobioses mais diferenciadas são verdadeiras simbioses onde as adaptações mais extremas são observadas do lado dos 'Homoptera'. Ao mesmo tempo, as formigas mostram adaptações comportamentais que resultam de um longo período de coevolução. Considerando-se os insetos sugadores como principais pragas dos cultivos em nível mundial, as implicações das relações trofobióticas são discutidas no contexto das comunidades de insetos em geral, focalizando os problemas que geram em Manejo Integrado de Pragas (MIP), em particular. PALAVRAS-CHAVE:Relações insetos/insetos, relações plantas/insetos, mutualismo, coevolução.ABSTRACT -In this paper, the mutualistic relationship known as trophobiosis, which occurs convergently between ants and several groups of Hemiptera Sternorrhyncha and Auchenorrhyncha (formerly 'Homoptera') is reviewed. The main characteristics of 'Homoptera' and Formicidae which favor trophobiotic interactions, such as honeydew excretion by sapsucking insects, ant attendance and physiological needs of both insects groups, are discussed. Aspects of the convergent evolution are presented. The most archaic system is not trophobiotic per se, foragers collect the honeydew casually expelled on the foliage by individuals or groups of non-associated 'Homoptera'. The commonest trophobiotic relationships are facultative; therefore, this form of mutualism is extremely diversified and is responsible for a range of physiological, morphological and behavioral adaptations by the 'Homoptera', mainly Sternorrhyncha. The more differentiated trophobioses are true symbioses where the most extreme changes can be observed on the 'Homoptera' side. Meanwhile, the ants show mainly behavioral adaptations resulting from a long coevolutive process. Considering the situation of sap-sucking insects as main crop pests worldwide, implications of trophobiotic relationships are discussed in the context of insect communities, in general, and on the problems that imply to Integrated Pest Manage...

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Section: Delabiementioning

confidence: 90%

Section: Who Are the Partners Of The Trophobiosis And Why Does It Makmentioning

confidence: 99%

Section: Diversity and Evolution Of Mutualisms Betweenmentioning

confidence: 99%

See 1 more Smart Citation

Trophobiosis Between Formicidae and Hemiptera (Sternorrhyncha and Auchenorrhyncha): an Overview

Delabie¹

2001

Neotrop. Entomol.

239

246

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“…The activity of secondary parasitoids can limit the success of primary parasitoids and may disrupt the effectiveness of essential biological control (Rosenheim 1998). In aphid communities, secondary parasitoids are ubiquitous, diverse and may have a strong impact on interactions among plants, herbivores and primary parasitoids (Mü ller et al 1999;Sullivan & Vö lkl 1999). Nevertheless, studies on multi-trophic interactions in insect communities often neglect the presence of this fourth trophic level (Brodeur 2000; but see Harvey et al 2003;Soler et al 2005).…”

Section: Introductionmentioning

confidence: 99%

Fungal endosymbionts of plants reduce lifespan of an aphid secondary parasitoid and influence host selection

2008

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Complex biotic interactions shape ecological communities of plants, herbivores and their natural enemies. In studies of multi-trophic interactions, the presence of small, invisible micro-organisms associated with plants and those of a fourth above-ground trophic level have often been neglected. Incorporating these neglected factors improves our understanding of the processes within a multi-trophic network. Here, we ask whether the presence of a fungal endosymbiont, which alters plant quality by producing herbivoretoxic substances, trickles up the food chain and affects the performance and host-selection behaviour of aphid secondary parasitoids. We simultaneously offered hosts from endophyte-free and endophyteinfected environments to secondary parasitoids. Older and more experienced parasitoid females discriminated against hosts from the endophyte-infected environment. Developing in lower quality hosts from the endophyte-infected environment reduced the lifespan of secondary parasitoids. This indicates that aphid secondary parasitoids can perceive the disadvantage for their developing offspring in parasitoids from the endophyte environment and can learn to discriminate against them. In the field, this discrimination ability may shift the success of primary parasitoids to endophyte-infected plants, which co-occur with endophyte-free plants. Ultimately, the control of aphids depends on complex interactions between primary and secondary parasitoids and their relative sensitivity to endophytic fungi.

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“…Hyperparasitism is considered to be one of the major causes of mortality in aphid primary parasitoids (Chua 1977, Rosenheim 1998, Sullivan and Völkl 1999, Gómez-Marco et al 2015. To our knowledge, the highest hyperparasitism rate of aphids in oilseed rape cultures was reported to be around 50 % during the late growing season (Varennes 2016), and generally appears lower than this the rest of the time on this crop (e.g.…”

Section: Discussion Amplification Success and Detection Of Trophic Lementioning

confidence: 99%

Disentangling higher trophic level interactions in the cabbage aphid food web using high-throughput DNA sequencing

Lefort¹,

Wratten²,

Cusumano³

et al. 2017

Metabarcoding and Metagenomics

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The lack of understanding of complex food-web interactions has been a major gap in the history of biological control. In particular, a better understanding of the functioning of pest food-webs and how they vary between native and invaded geographical ranges is of prime interest for biological control research and associated integrated pest management. Technical limitations associated with the deciphering of complex food-webs can now be largely overcome by the use of high throughput DNA sequencing techniques such as Illumina MiSeq. We tested the efficiency of this next generation sequencing technology in a metabarcoding approach, to study aphid food-webs using the cabbage aphid as model. We compared the variations in structure and composition of aphid food-webs in the species' native range (United Kingdom, UK) and in an invaded range (New Zealand, NZ). We showed that Illumina MiSeq is a well suited technology to study complex aphid food-webs from aphid mummies. We found an unexpectedly high top down pressure in the NZ cabbage aphid food-web, which coupled to a large ratio of consumer species / prey ‡, § § species and a lack of potential inter-specific competition between primary parasitoids, could cause the NZ food-web to be more vulnerable than the UK one. This study also reports for the first time the occurrence of a new hyperparasitoid species in NZ, as well as new associations between hyperparasitoids parasitoids and the cabbage aphid in this country. We conclude that the complexity of aphid food-webs in agricultural systems could often be underestimated, particularly at higher trophic levels; and that the use of high throughput DNA sequencing tools, could largely help to overcome this impediment.

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HYPERPARASITISM: Multitrophic Ecology and Behavior

Cited by 205 publications

References 105 publications

Trophobiosis Between Formicidae and Hemiptera (Sternorrhyncha and Auchenorrhyncha): an Overview

Trophobiosis Between Formicidae and Hemiptera (Sternorrhyncha and Auchenorrhyncha): an Overview

Fungal endosymbionts of plants reduce lifespan of an aphid secondary parasitoid and influence host selection

Disentangling higher trophic level interactions in the cabbage aphid food web using high-throughput DNA sequencing

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