Phytophagous on flower heads of Neotropical Compositae

Thomas Lewinsohn with Paulo Inácio Prado USP Mário Almeida Neto UFG Adriana Almeida UFRN Leonardo Ré Jorge Unicamp ______Laboratório Interações Insetos-Plantas Depto. Biologia , Inst. Biologia Unicamp – University of Campinas herbivores+: the multicellular majority Terry Erwin, 1982: “... as many as 30 million insects”

Terry Erwin who’s who among the herbivorous insects

beetles , butterflies , midges sawflies bugs, aphids grasshoppers thrips walking sticks data sources: taxonomic studies

based on adults - what do larvae do? no host records unreliable host identification data sources: biocontrol surveys

Carduus nutans with Rhynocyllus conicus (Curculionidae) data sources: community diversity studies

• samples (plots, individual trees) and • mass samples (net sweep, suction samples, fogging, light traps)

Murdoch, Evans & Peterson 1972 adult insects on plants: herbivores or tourists? Insects and Compositae as ecological study systems A model system for herbivore evolution Solidago – Eurosta – parasitoids/predators A model system for population dynamics ragwort, Senecio jacobaea - cinnabar , Tyria jacobaeae

Longitarsus

Chromatomyia

Melanagromyza metacommunity dynamics a field experiment From biocontrol surveys to ecological insights Biocontrol prospecting in

Baccharis Daniel Gandolfo Gutierrezia Chromolaena odorata > Campuloclinium macrocephalum basic study design a suitable plant-herbivore system

endophagous insects in flower heads flower heads have a rich and diversified associated entomofauna

tephritid larvae and pupae in Porophyllum ruderale, Unicamp Study sites: mountains

Fortaleza dos Aparados, R.G. Sul

Conselheiro Mata, Minas Gerais Study sites: cerrado

Martinho Prado, São Paulo sampled populations

Erigeron maximus

Lychnophora salicifolia procedures surveyed regions and sites

Espinhaço

Cerrados SP Mantiqueira Rio SP

Serras Sul Plant species distribution - localities

200 180 160 139

140 120 100 80 60 number of species of species number 40 20 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15

localities per plant species sampled plant taxa

tribe species samples tribe genus species samples Astereae Aster 1 1 Acritopappus 2 9 Baccharidastrum 3 8 Adenostemma 2 13 Baccharis 37 175 Ageratum 2 141 Conyza 6 32 Austroeupatorium 6 76 Erigeron 1 21 Ayapana 1 11 Haplopappus 1 8 Barrosoa 3 27 Heterothalamus 2 3 Campovassouria 1 23 Noticastrum 3 9 Campuloclinium 6 42 Solidago 1 7 Chromolaena 32 371 Astereae Total 57 266 Disynaphia 2 4 Grazielia 6 76 Barnadesiinae Dasyphyllum 5 12 Gyptis 3 3 Hatschbachiella 1 5 Cardueae Arctium 1 1 Heterocondylus 4 40 Carduus 1 1 Koanophyllon 4 13 Cirsium 1 11 Mikania 41 178 Cardueae Total 3 13 Neocabreria 1 3 Ophryosporus 1 1 Praxelis 3 32 Pseudobrickellia 1 7 Raulinoreitzia 2 4 Stevia 6 8 Stomathantes 1 1 9 62 Trichogonia 5 72 Trichogoniopsis 1 2 Vittetia 1 2 Eupatorieae Total 152 1232 sampled plant taxa tribe genus species samples tribe genus species samples Gnaphalieae Achyrocline 2 27 Mutisieae Actinoseris 10 23 Chevreulia 2 2 Chaptalia 6 14 Gnaphalium 7 7 Gochnatia 14 59 Helichrysum 1 1 Holocheilus 1 2 Lucilia 1 1 Jungia 1 8 Stenophalium 2 2 Mutisia 1 1 Gnaphalieae Total 15 40 Pamphalea 1 1 2 10 Helenieae Porophyllum 4 23 Trixis 6 40 Wunderlichia 2 11 Heliantheae Aspilia 23 63 Mutisieae Total 46 173 Bidens 5 27 Calea 16 26 Plucheeae Pluchea 3 8 Dimerostemma 1 1 Pterocaulon 5 12 Isostigma 1 2 Stenachaenium 1 5 Verbesina 4 10 Plucheeae Total 9 25 Viguiera 8 28 Heliantheae Total 59 159 Senecioneae Emilia 2 6 Erechtites 5 21 Lactuceae Hypochaeris 3 5 Hoehnephytum 1 4 Sonchus 1 1 Pentacalia 1 7 Lactuceae Total 4 6 Senecio 21 92 Senecioneae Total 35 139 Moquinieae 1 5 sampled plant taxa tribe genus species samples tribe species samples Vernonieae Anteremanthus 1 2 Anthemideae 1 1 Centratherum 1 25 Chresta 2 8 Astereae 57 266 Chrysolaena 6 42 Barnadesiinae 5 12 Cyrtocymura 1 27 Cardueae 3 13 Echinocoryne 2 14 Elephantopus 4 12 Cichorioideae 1 1 Eremanthus 12 56 Eupatorieae 152 1232 Lepidaploa 11 84 Lessingianthus 35 166 Gnaphalieae 15 40 Lychnophora 17 59 Helenieae 4 23 Lychnophoriopsis 1 1 Heliantheae 59 159 Minasia 8 24 Orthopappus 2 15 Lactuceae 4 6 Piptocarpha 1 19 Moquinieae 1 5 Piptolepis 4 9 Mutisieae 46 173 Proteopsis 2 22 Stenocephalum 2 12 Plucheeae 9 25 Stilpnopappus 1 1 Senecioneae 35 139 Vernonanthura 25 165 Vernonia 2 2 Vernonieae 143 768 Vernonieae Total 143 768 Total 535 2863

Grand Total 535 2863 faunistics The main herbivore families on Compositae

proportions of reared proportions of specimens species (excl. Cecidomyiidae) Agromyzidae Tortricidae Pyralidae Cecidomyiidae Curculionidae; &c Diptera: Tephritidae

4700 described species fruit pests: medfly - Ceratitis, Anastrepha, Rhagoletis; Dacus, Bactrocera Compositae main host family Diptera: Tephritidae tribe genera Acrotaeniini Caenoriata Tetreuaresta Tomoplagia Dithrycini Cecidochares Eutretini Dictyotrypeta Paracantha Myopitini Neomyopites Acinia Dioxyna Dyseuaresta Euarestoides Oxyna Plaumannimyia Trupanea Trypanaresta Xanthaciura Diptera: Tephritidae Tomoplagia Diptera: Agromyzidae

3000+ described species leafminer, stemborer pests Compositae important host family flower head feaders mostly in Melanagromyza; Lyriomyza, other genera minor Diptera: Cecidomyiidae

6000+ described species gall midges (also saprophages, predators etc.) Compositae major host family flowerhead feeders non-gallers or inconspicuous galls most in very large genera: Asphondylia, Neolasioptera, Dasineura, Clinodiplosis Diptera: Cecidomyiidae the Cecidomyiidae seem to be the family [of Diptera] with the least developed taxonomic knowledge in the neotropics (Amorim 2009) : Tortricidae

9400+ described species flowerhead feeders: tribe Cochylini, > 900 species, mostly associated with Compositae Lepidoptera: Pterophoridae plume moths c. 1200 described species flowerhead, stem and root feedeers; sometimes complex cycles Compositae one of major host families One taxonomist in the world Lepidoptera: Pyralidae

6200+ described species key pest species for stored flour, grain main flowerhead feeders in Phycitinae, two genus groups: • Phycitodes / Homoeosoma / Rotruda Phycitodes mucidella • Unadilla new species, new genera, new host records now what? “metaendemic species” insect-plant interactions: from two perspectives interaction matrices and questions entomocentric vs. phytocentric approaches herbivore specialization Taxonomic host span - different families (Lep: Pterophoridae) generalists, specialists, both?

Adaina bipunctatus Adaina microdactyla South America to Florida , widespread (Central and the Caribbean Asia?) in , our records span strictly monophagous on 54 host species in 7* different tribes of L. Compositae Adaina bipunctatus

Eupatorieae 55% of host species 89% of adults Adaina microdactyla

Eupatorieae: 1 native species – only host 2 introduced species, not used Host ranges of panamerican tephritids

genus Region A C E I H M S V Acinia Neotrop X Nearctic X Dioxyna Neotrop X Nearctic X X Dyseuaresta Neotrop X Nearctic X Paracantha Neotrop X Nearctic X X Tomoplagia Neotrop X X X Nearctic X X X Trupanea Neotrop X X X X X Nearctic X X X X X X Trypanaresta Neotrop X X Nearctic X Xanthaciura Neotrop X X Nearctic X X Neotrop X X Nearctic X X

insect-plant biogeography large-scale contrasts

Espinhaço

Cerrados SP Mantiqueira Rio SP

Serras Sul Plant species per region

240 17 130 4%

Southeast South Insect species per region

61 41 18 34%

Southeast South Insect species per region

Diptera Lepidoptera (2 families, 92 spp) (3 families, 28 spp)

51 30 11 10 11 7

Southeast South

Southeast South Similarity of vs. herbivores

South

Southeast

plants

South

Southeast insects beta-diversity of plants: dissimilarity matrix

localities within same region localities in different regions

CNESS (m=10) plants: number os samples insects: frequency in samples Do major changes in floras entail equivalent changes in insect faunas?

No. • Most differences in regional floras are at the species level, and in the relative diversity of higher taxa. • Most major plant genera are represented in local communities. • Among regions, most insects switch host species within a genus or subtribe. • No important host shift was found among regions. • Generalists are conservative! We found no large host switches even between continents Do endemic plants bear endemic insects?

No. ! endemic plant species belonging to widespread genera share phytophages with widely-distributed congeneric plants.

Yes. ! endemic genera or subtribes have sets of endemic phytophages. insect-plant interaction structure and dynamics Quantitative plant-herbivore webs Mantiqueira: Campos do Jordão

5 20 23 35 37 2 4 8 11 14 15 16 17 18 19 21 22 24 27 28 29 30 32 33 34 36

1 2 3 5 7 8 9 12 13 14 15 17 21 22 23 25 27 30 32 33 34 36 38 26 31

112 plant samples, 121 host records Effects of degradation on interactive assemblages plants and insect herbivores in a cerrado gradient

Mário Almeida Neto, 2006 – PhD plants and insect herbivores in a cerrado gradient … just out tangled trees: can we match phylogenies? matching tephritids and their symbionts matching tephritids with symbiotic bacteria Tephritid phylogenies

Han, 2006; see also 2009 Tephritid phylogenies

Han, 2006; see also 2009 Thanks first... Benoît and Pirani, supporters, coorganizers Thanks Participants Umberto Kubota, Adalberto Lopes, Carlos Fonseca, Bruno Buys, Antonio Carlos Macedo, Flavia Batista, Marcelo Lopes, Marina Braun, &c Identification, discussions, insights Hermógenes Leitão Filho, João Semir, Harold Robinson, John Pruski, Nelson Matzenbacher, Nick Hind, &c Allen Norrbom, Angelo Pires Prado, Victor Becker, Cees Gielis, Alma Solis, Keith Brown, José Candido Mello Carvalho, &c Financial support FAPESP CNPq CAPES NERC (UK) NSF/NCEAS (USA) Hermógenes, Mogi-Guaçu cerrado, February 1977 addendum A picky Mutisiae feeder

Actinoseris aff. radiata 2 Gochnatia paniculata 3 Actinoseris angustifolia 5 Gochnatia polymorpha 1 Actinoseris arenaria 3 Gochnatia pulchra 17 Actinoseris polymorpha 5 Gochnatia sp.01 2 Actinoseris radiata 2 Gochnatia sp.02 1 Actinoseris revoluta 1 Gochnatia sp.03 1 Actinoseris sp.01 1 Gochnatia sp.04 1 Actinoseris sp.02 1 Holocheilus illustris 2 Actinoseris sp.03 2 Jungia floribunda 8 Actinoseris stenophylla 1 Mutisia campanulata 1 Chaptalia aff. integerrima 3 Mutisieae sp.03 3 Chaptalia exscapa 1 Mutisieae sp.04 1 Chaptalia integerrima 4 Pamphalea smithii 1 Chaptalia martii 2 Trichocline catharinensis 8 Chaptalia nutans 3 Trichocline macrocephala 2 Chaptalia sinuata 1 Trixis eryngioides 3 Gochnatia aff. pulchra 1 Trixis lessingii 1 Gochnatia amplexifolia 8 Trixis ophiorhiza 2 Gochnatia barrosii 4 Trixis praestans 2 Gochnatia discoidea 9 Trixis vauthieri 21 Gochnatia floribunda 6 Trixis verbasciformis 11 Gochnatia hatschbachii 4 Wunderlichia mirabilis 10 Gochnatia orbiculata 1 Wunderlichia senaeii 1 ! A picky Mutisiae feeder?

Actinoseris aff. radiata 2 Gochnatia paniculata 3 Actinoseris angustifolia 5 Gochnatia polymorpha 1 Actinoseris arenaria 3 Gochnatia pulchra 17 Actinoseris polymorpha 5 Gochnatia sp.01 2 Actinoseris radiata 2 Gochnatia sp.02 1 Actinoseris revoluta 1 Gochnatia sp.03 1 Actinoseris sp.01 1 Gochnatia sp.04 1 Actinoseris sp.02 1 Holocheilus illustris 2 Actinoseris sp.03 2 Jungia floribunda 8 Actinoseris stenophylla 1 Mutisia campanulata 1 Chaptalia aff. integerrima 3 Mutisieae sp.03 3 Chaptalia exscapa 1 Mutisieae sp.04 1 Chaptalia integerrima 4 Pamphalea smithii 1 Chaptalia martii 2 Trichocline catharinensis 8 Chaptalia nutans 3 Trichocline macrocephala 2 Chaptalia sinuata 1 Trixis eryngioides 3 Gochnatia aff. pulchra 1 Trixis lessingii 1 Gochnatia amplexifolia 8 Trixis ophiorhiza 2 Gochnatia barrosii 4 Trixis praestans 2 Gochnatia discoidea 9 Trixis vauthieri 21 Gochnatia floribunda 6 Trixis verbasciformis 11 Gochnatia hatschbachii 4 Wunderlichia mirabilis mirabilis 10 10 Gochnatia orbiculata 1 Wunderlichia senaeii 1 ! ! A picky feeder

Wunderlichia mirabilis, Bruno Buys, Serra do Cabral, 1995

Lewinsohnia magna Prado & Norrbom, 2006 2nd South American Compositae Meeting, 2016

What do insects think of the new Compositae taxonomies?

Lewinsohnia magna Prado & Norrbom, 2006