Predicting parasitoid attack of potential Brazilian peppertree biological control agents Greg Wheeler

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Predicting parasitoid attack of potential Brazilian peppertree biological control agents Greg Wheeler Invasive Plant Research Lab, USDA/ARS, Ft Lauderdale, FL, USA

Classical biological control of Two key risks: weeds Direct risks: damage of non-target species. Quarantine/overseas testing Indirect risks: agent provides food subsidies to native natural enemies leading to apparent competition and other consumer interactions

Brazilian pepper, Schinus terebinthifolia (Anacardiaceae) Classic tree invader damaging native habitats (Richardson & Rejmanek 2011) Introduced for horticulture ~150 yrs bp Bird dispersed Invasive in several regions of the world, North America, Australia, South Africa In Fla & HI one of our most invasive spp

Classical biological control of Two key risks: weeds Direct risks: damage of non-target species. Quarantine/overseas testing Indirect risks: agent provides food subsidies to native natural enemies leading to apparent competition and other consumer interactions

Search for biological control agents Brazil Surveys of South America, 2005 to March 2018 20 + trips to Brazil, Argentina, Paraguay; > 900 sites Paraguay Argentina Uruguay

Schinus biological control Aggregation of adult thrips Pseudophilothrips ichini Thrips Petitioned TAG Aug 2014 (approved!) Thrips damage Thrips adult

Recommended talk: Friday 12:00 12:25 Dr. Dale Halbritter Expected Impact and Mass Production of the Thrips Biological Control Agent of Brazilian Peppertree Change in leaf number 50 40 30 20 10 0-10 No thrips Thrips ns Leaf number a b a b -20 Low Medium High Fertilizer level

P. ichini thrips testing Test plant list: Anacardiaceae - small family in US with 11 genera and 48 species Total no-choice tested: 45 families 99 genera 130 taxa, including 5 Pistachio; 4 Mango var. Tested for F 1 adults

Results of thrips choice test

P. ichini thrips results - multiple generation tests

Classical biological control of Two key risks: weeds Direct risks: damage of non-target species. Quarantine/overseas testing Indirect risks: agent provides food subsidies to native natural enemies leading to apparent competition and other consumer interactions

Can we reduce in-direct effects? Biocontrol focuses on simple herbivoreplant relationships but ignores more complex community relationships These complex community relationships should be better understood if we are to predict these interactions prior to release Pearson and Callaway 2003. TREE

Multi-trophic Food web Simple predatory prey model Native herbivores

Multi-trophic Food web Three trophic levels Native herbivores Native parasitoids

Multi-trophic Food web Biocontrol introduction Native herbivores Native parasitoids? Introduced biocontrol

Multi-trophic Food web Alternate hosts Native herbivores Native parasitoids?? Introduced biocontrol X Alternate hosts

Multi-trophic Food web Many native herbivores Native parasitoids Native herbivore Native herbivore

Multi-trophic Food web Which biocontrol is most susceptible to NE attack? Native herbivores Native parasitoids?? Potential Biocontrol agents

Predicting parasitoid accumulation in biological control Goeden & Louda 1976 Reviewed impact of natural enemies (NE) on agents. Conclude effect of NE unpredictable-inevitable Hill & Hulley 1995 Recorded parasitoids from 40% of agents but not a strong effect Paynter et al 2010 reported significant effect; suggested we: Select agents with species-poor parasitoid faunas in native range Avoiding agents with ecological analogues in the invaded range

Herbivores in Brazil - native range Total number of spp 124 + Caterpillars (Lepidoptera) 65 spp Geometridae ~24 spp Paectes spp. ~4 spp Episimus spp. ~ 10 spp Thrips 3 spp Beetles (Coleoptera) 27 spp Bugs (Hemiptera) 10 spp

Herbivores in Brazil - native range Total number of spp 124 + Caterpillars (Lepidoptera) 65 spp Geometridae ~25 spp Paectes spp. ~4 spp Episimus spp. ~ 10 spp Thrips 3 spp

Collections of Schinus herbivores - native range Rearing for parasitoids in Q 2011-2017 4 regions Trees sampled visually/shaking branches 20-30 sites/region Paraguay Argentina Uruguay

Herbivores of S. terebinthifolia in invaded range - Florida Florida distribution 15 sites Collections visual & shake branches Herbivores: o Geometridae o Paectes spp. o Episimus spp. o Thrips

Paectes spp. (Euteliidae) in native & invaded range DNA reveals many species Brazilian spp.: P. longiformis, P. similis, P. sinuosa, and more Florida spp.: Paectes asper P. fructescens & P. nana

Paectes spp. Parasitoids in Native & Invaded range Brazilian parasitoids Braconidae Chalcidoidea Florida parasitoids Cotesia spp.

Episimus (Tortricidae) in native & invaded range

Episimus spp. in native & invaded range Brazilian: Episimus unguiculus Florida native: Episimus transferranus

Episimus spp. parasitoids in native & invaded range Florida Brazil Braconidae Diolcogaster sp. Tachinidae Chalcididae Braconidae Hymenochaonia delicata

Geometridae from Brazilian - native range surveys 25+ spp Hymenomima memor Prochoerodes onustaria

Geometridae Parasitoids from Brazilian - native range Ichneumonidae Braconidae Tachinidae Torymidae

Geometridae from Florida - invaded range surveys - 2 spp Florida species: Florida native species: Pleuroprucha asthenaria Oxydia vesulia

Thrips Native range, Pseudophilothrips ichini P. ichini damage adults Feed and distort flushing leaf tips Brazil Pseudophilothrips ichini (Thysanoptera: Phlaeothripidae) Wide range Bahia to SC, Brazil; sea level to 1300 m High degree of host specificity Native range

Thrips: Native range Pseudophilothrips ichini Parasitoids, only 1 sp. in native range: Thripastichus gentilei (Eulophidae) Paoli 1931

Thrips: Surrogates Invaded range Two spp thrips on Schinus in Florida Retithrips syriacus, black vine thrips Retithrips syriacus Selenothrips rubrocinctus, red banded thrips Selenothrips rubrocinctus

Parasitoids of Schinus herbivores in Brazil - Native range South American parasitism rates 2011-2015: Similar across defoliator guilds Mostly less than 20% Thrips < 5%

Parasitoids of Schinus herbivores in Florida- invaded range Florida parasitism rates 2014-2015: No Geo or thrips parasitism Paectes/Episimus Mostly less than 20%

Conclusions: Episimus and Paectes defoliators are parasitized at same rates in native range Predict ~15% parasitism if released in Florida Geometridae had 10% parasitism in South America but rare in Florida Thrips have low parasitism in both South and North America Predict < 5% parasitism if released in Florida

Conclusions: Release of thrips as biological controls pose the lowest risk of indirect effects - little parasitism expected. Thrips also pose the lowest risk of direct effects due to a narrow host range

Multi-trophic Food web Which biocontrol is most susceptible to NE attack? Native herbivores Native parasitoids?? Potential Biocontrol agents

Multi-trophic Food web Which biocontrol is most susceptible to NE attack? Native herbivores Native parasitoids?? Potential Biocontrol agents

Acknowledgements greg.wheeler@ars.usda.gov unding: Florida Fish Wildlife Commission SFWMD USDA/ARS Southwest Florida Water Management District ork: Kirsten Dyer, USDA/ARS/IPRL Chawner, Rendon, Hernandez, Silverson, Fung, Jones, SCA/AmeriCorps D. Williams, TCU D. Davis, Smithsonian J Brown, M. Pogue, M. Gates, R. Kula, et al. USDA/ARS/SEL C. O Brien, Green Valley, AZ L. Mound, CSIRO Canberra Australia J.F. Landry, Ag Canada, Ottawa, Canada M. Vitorino, Univ Blumenau, Brazil R. Barreto, Univ Fed Vicosa, Brazil