Insect Parasitoids
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Insect Parasitoids Parasitoid—An animal that feeds in or on another living animal for a relavely long 4me, consuming all or most of its 4ssues and eventually killing it. Insect parasitoids account for 7% of described species. Most parasitoids are found in 3 orders: Hymenoptera (76%) 1 evolu4onary lineage Diptera (22%) 21 evolu4onary lineages Coleoptera (2%) 14 evolu4onary lineages Parasitoids of Ants Family Species Order (Tribe) Richness Natural History Strepsiptera Myrmecolacidae ~100 Males are parasitoids of adult worker ants; females are parasitoids of mantids and orthopterans Hymenoptera Braconidae 35 Parasitoids of adult worker ants (Neoneurinae) Chalicididae 6 Parasitoids of worker larvae-pupae (Smicromorphinae) Diapriidae >25 Parasitoids of worker larvae-pupae Eucharitidae ~500 Parasitoids of worker larvae-pupae Ichneumonidae 16 Parasitoids of worker larvae-pupae (Paxylommatinae) Diptera Phoridae ~900 Parasitoids of adult worker ants Tachinidae 1 Endoparasitoid of founding queens of Lasius Parasitoids of Ants Family Species Order (Tribe) Richness Natural History Strepsiptera Myrmecolacidae ~100 Males are parasitoids of adult worker ants; females are parasitoids of mantids and orthopterans Hymenoptera Braconidae 35 Parasitoids of adult worker ants (Neoneurinae) Chalicididae 6 Parasitoids of worker larvae-pupae (Smicromorphinae) Diapriidae >10 Parasitoids of worker larvae-pupae Eucharitidae ~500 Parasitoids of worker larvae-pupae Ichneumonidae 16 Parasitoids of worker larvae-pupae (Paxylommatinae) Diptera Phoridae ~900 Parasitoids of adult worker ants Tachinidae 1 Endoparasitoid of founding queens of Lasius Salient Features of the Phoridae Member of the Aschiza Muscomorpha Small flies with very diverse habits 244 genera recognized, ~4000 species described 111 genera associated with social insects 60 genera associated with ants Parasitoid lifestyle evolved numerous 4mes Lifestyles of Phorid Flies Associated with Ants Nest symbionts – all life stages found in ant nests as scavengers, predators of host ants or other guests, or on food regurgitated directly to them by host ants. Body highly modified including the reduc4on of wings, appendages and abdominal sclerites. ~40 genera, >80% of the species associated with New World army ants (Ecitoninae). Aerial parasitoids – adults are free living, larvae are obligate parasitoids of sterile worker caste(s) or reproduc4ve females. Body unmodified except for scleri4zed ovipositor. ~20 genera, 6 of 24 subfamilies of ants aacked. Lifecycles of Aerial Parasitoids The Ant-Decapitators Female aracted Larva develops to healthy host In head capsule Female uses ovipositor to lay a single egg in host New adult emerges Larva pupariates Larva eventually from head capsule In head capsule decapitates host Photos by S. D. Porter Lifecycles of Aerial Parasitoids The Scavengers Larvae develop in Female lays mul4ple Female aracted body cavity to distressed host eggs in host Larvae pupariate Larvae crawl away Larvae emerge away from host from host from host Photos by D. H. Feener Comparison of Lifestyle Attributes of the Phorid Parasitoids of Ants Characteristic Decapitators Scavengers Host vitality Healthy, mobile Moribund, immobile Host location cue Trail pheromone? Alarm pheromone? Oviposition Difficult Easy Mate on host? Some species Some species Host feeding No Yes Clutch size Single egg/host Multiple eggs/host Time to hatching 48 hrs 6 hrs Larval development Long (~14-30 days) Short (~3-5 days) Larva-host interactions Yes No Larva-larva interactions No Yes Phorid Parasitoids of Ants Are Typically Species Specific Parasitoid Hosts Cremersia Ecitoninae Parasitoid Host Neodohrniphora Ani A. feeneri P. dentata Apocephalus Poneromorphs Ecitoninae A. sp. 1 P. morrisi Myrmicinae A. brunneiventris P. hyatti Dolichoderinae P. perpilosa Formicinae A. orthocladus P. diversipilosa P. hyatti Other Apocephalus- P. tetra series species P. vallicola A. pugilis P. bicarinata Parasitoid Hosts A. sp. 26 P. titanis A. attophilus-group Atta & Acromyrmex A. titanis P. rhea A. feeneri-group Pheidole A. uncinus P. obtusospinosa A. grandipalpis-group Ecitoninae 8 species Unknown A. miricauda-group Poneromorphs A. pergandei-group Camponotus …And OEen Caste Specific Apocephalus feeneri-group species Apocephalus colombicus aacks only aacks only the major workers of their leaf carriers of its host A8a colombica Pheidole hosts 1.1 1.0 Pl Pt 0.9 Pb 0.8 Pcr Pw 0.7 Pcu Worker Head Size (mm) 0.6 0.3 0.4 0.5 0.6 Parasitoid Body Size (mm) Neodohrniphora curvinervis aacks Pseudacteon species associated with only large unladen workers of its host Solenopsis fire ants specialize on workers Aa cephalotes of different sizes Photos: P. Bertner, D. H. Feener Several Parasitoid Species May Use Different Parts of the Same Caste Drawings by Jesse Cantley. From: Brown, B.V. (1999) Sociobiology 33: 95-103 …And Form Parallel Ecological Guilds in Different Hosts Drawings by Jesse Cantley. From: Brown, B.V. (1999) Sociobiology 33: 95-103 Why Are Phorid Parasitoids So Specialized? Ecological Constraint Females use ant pheromones as Males use hosts host locaon cues Encounter as the primary mang site host range Establish Maintain Ants are hard hosts Host-larvae to oviposit in interac4ons X Host-Parasitoid Coevolu4on Host Locaon Cues Ecological Constraint Cues used in host locaon Encounter host range Establish Maintain Host-Parasitoid Coevolu4on Chemical CommunicaPon in Ants Alarm pheromone A chemical substance produced and release by an individual to warn or alert nestmates of impending danger. Trail pheromone Anatomical location of the 4 major exocrine A chemical substance produced glands of ants. M = mandibular gland; D = and release by an individual to Dufour’s gland; Po = poison gland or sac; Py = pygidial gland. Modified from Hölldobler & recruit and direct nestmates to a Wilson (1990). food source. 300 Exocrine glands typical contain a mixture of N N few to many chemical compounds. 200 6 N N 5 Gas chromatogram of volale chemicals from N N Response N N 3 100 1 the mandibular gland of a single worker of N N 2 N N Odontomachus ruginodis collected from N N tridecane 8 4 7 Punta Cana (Dominican Republic). 0 11.0 13.0 15.0 17.0 18.0 19.0 Time (min) Ant Pheromones as Host LocaPon Cues • Apocephalus paraponerae is aracted to two mandibular gland components of Paraponera clavata host (Feener et al. 1996). • Pseudacteon brevicauda is aracted to Photo: A.L. Wild alarm pheromone in mandibular gland of Photo: L. Morrison Myrmica rubra host (WiVe et al. 2010). Photo: D. H. Feener • Pseudacteon formicarum is aracted to formic acid in venom glands of Lasius niger host (Maschwitz et al. 2008). Photo: A. Weissflog • Pseudacteon tricuspis is aracted to pyrazine alarm pheromone in mandibular gland and several alkaloids in the poison gland of Solenopsis invicta host (Chen et al. 2009, Sharma et al. 2011). Ant Species Currently Under Study Ant species Mandibular glands Phorid behavior Ectatomma tuberculatum ? Attracted to head Ectatomma ruidum ? Odontomachus bauri Pyrazines Attracted to head Odontomachus clarus Pyrazines? Odontomachus erythrocephalus ? Attracted to head Odontomachus hastatus Pyrazines? Attracted to head Odontomachus opaciventris ? Indiscriminate Odontomachus ruginodis Pyrazines Pachycondyla apicalis Benzaldehyde? Pachycondyla harpex ? Attracted to head Pachycondyla impressa ? ? Pachycondyla stigma ? Pachycondyla verenae ? Pachycondyla villosa Ketones, alcohols Attracted to head? Paraponera clavata Ketones, alcohols Attracted to head Use of Ant Pheromones Enforces Specificity • Ants adver4se their iden4ty and locaon through the use of specialized alarm and trail pheromones. • These specialized signals are detectable and reliable cues to the iden4ty and precise locaon of suitable hosts. Use of such specialized cues should reduce search 4me between patches of hosts. • Because ants live in colonies, detec4on of appropriate host locaon cues oken means the availability of numerous hosts. This should reduce search 4me between both oviposion events and mang events. Oviposion Behavior & Host Defense Ecological Constraint Encounter host range Establish Maintain Oviposion behavior & host defense Host-Parasitoid Coevolu4on Specialized Oviposion in Injured Hosts Specialized Oviposion in Injured Hosts Specialized Oviposion in AcPve Hosts Ants Are Hard Hosts to Oviposit In • Hard exoskeleton forces phorid parasitoids to oviposit in very specialized locaons. Photo: P. Bertner • Ants have specialized defense postures and evasive behavior that make oviposion more difficult. Photo: A. Weissflog • Some ant species use nestmates to defend against parasitoid aack. Parasitoids must evade these Photo: D. H. Feener defenses. Hitchhikers of Photos: D. H. Feener Aa colombica defend leaf-carriers against Defense posture of ApocephalusSolenopsisPhoto: L. Morrison colombicus geminata Ant Hosts as MaPng Sites Ecological Constraint Males use hosts Encounter as the primary mang site host range Establish Maintain Host-Parasitoid Coevolu4on Ant Hosts as MaPng Sites MaPng on Hosts Enforces Specificity • Males are aracted to host ant species and oken arrive before females and in larger numbers. • Males use the same host locaon cues as females, leading to posive assortave mang. • Use of hosts as the primary mang site makes a phorid parasitoid more dependent on its host. This may serve as a populaon isolang mechanism that enforces host specificity. Working Hypothesis for CoevoluPon between Ants and Phorid Parasitoids Ant Chemical Parasitoid Phylogeny Communicaon Phylogeny Signals Summary Ecological Constraint Both ant decapitators and ant Host specificity in the ant scavengers show strong host- scavengers is determined specificity, u4lizing one species primarily by processes related or a few closely related species Encounter to host encounter and site of as hosts. oviposion. Host specificity in the Phorid parasitoids ant decapitators is host of ants is a determined by a range wonderfully rich complex mixture of system to explore host encounter, host Establish Maintain general ques4ons in defense and host- the evolu4on and larvae interac4ons, ecology of host- the balance of which parasitoid must s4ll be worked interac4ons. out. Host-Parasitoid Coevolu4on .