Phytophagous insects 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 Animal, Inst. Biologia Unicamp – University of Campinas

herbivores+plants: the multicellular majority

Terry Erwin, 1982: “... as many as 30 million insects”

Terry Erwin

who’s who among the herbivorous insects

beetles moths, butterflies

flies, midges sawflies

bugs, aphids grasshoppers

thrips walking sticks

data sources: taxonomic studies

taxonomy 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

•  Plant samples (plots, individual trees) and

•  insect 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

Longitarsus

Chromatomyia

Melanagromyza

A model system for population dynamics ragwort, Senecio jacobaea - cinnabar moth, Tyria jacobaeae

metacommunity dynamics a field experiment

From biocontrol surveys to ecological insights

Biocontrol prospecting in South America

Daniel Gandolfo Baccharis Gutierrezia Chromolaena odorata > Campuloclinium macrocephalum

basic study design

a suitable plant-herbivore system

tephritid larvae and pupae in Porophyllum ruderale, Unicamp

endophagous insects in flower heads

flower heads have a rich and diversified associated entomofauna

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

Serras Sul

Cerrados SP

Espinhaço

Mantiqueira Rio

SP

Plant species distribution - localities

139

0

20

40

60

80

100

120

140

160

180

200

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15

localities per plant species

num

ber

of s

peci

es

sampled plant taxa tribe genus species samplesAstereae Aster 1 1

Baccharidastrum 3 8Baccharis 37 175Conyza 6 32Erigeron 1 21Haplopappus 1 8Heterothalamus 2 3Noticastrum 3 9Solidago 1 7

Astereae Total 57 266

Barnadesiinae Dasyphyllum 5 12

Cardueae Arctium 1 1Carduus 1 1Cirsium 1 11

Cardueae Total 3 13

tribe genus species samplesEupatorieae Acritopappus 2 9

Adenostemma 2 13Ageratum 2 141Austroeupatorium 6 76Ayapana 1 11Barrosoa 3 27Campovassouria 1 23Campuloclinium 6 42Chromolaena 32 371Disynaphia 2 4Grazielia 6 76Gyptis 3 3Hatschbachiella 1 5Heterocondylus 4 40Koanophyllon 4 13Mikania 41 178Neocabreria 1 3Ophryosporus 1 1Praxelis 3 32Pseudobrickellia 1 7Raulinoreitzia 2 4Stevia 6 8Stomathantes 1 1Symphyopappus 9 62Trichogonia 5 72Trichogoniopsis 1 2Vittetia 1 2

Eupatorieae Total 152 1232

sampled plant taxa tribe genus species samplesGnaphalieae Achyrocline 2 27

Chevreulia 2 2Gnaphalium 7 7Helichrysum 1 1Lucilia 1 1Stenophalium 2 2

Gnaphalieae Total 15 40

Helenieae Porophyllum 4 23

Heliantheae Aspilia 23 63Bidens 5 27Calea 16 26Dimerostemma 1 1Isostigma 1 2Verbesina 4 10Viguiera 8 28

Heliantheae Total 59 159

Lactuceae Hypochaeris 3 5Sonchus 1 1

Lactuceae Total 4 6

Moquinieae Moquinia 1 5

tribe genus species samplesMutisieae Actinoseris 10 23

Chaptalia 6 14Gochnatia 14 59Holocheilus 1 2Jungia 1 8Mutisia 1 1Pamphalea 1 1Trichocline 2 10Trixis 6 40Wunderlichia 2 11

Mutisieae Total 46 173

Plucheeae Pluchea 3 8Pterocaulon 5 12Stenachaenium 1 5

Plucheeae Total 9 25

Senecioneae Emilia 2 6Erechtites 5 21Hoehnephytum 1 4Pentacalia 1 7Senecio 21 92

Senecioneae Total 35 139

sampled plant taxa tribe genus species samplesVernonieae Anteremanthus 1 2

Centratherum 1 25Chresta 2 8Chrysolaena 6 42Cyrtocymura 1 27Echinocoryne 2 14Elephantopus 4 12Eremanthus 12 56Lepidaploa 11 84Lessingianthus 35 166Lychnophora 17 59Lychnophoriopsis 1 1Minasia 8 24Orthopappus 2 15Piptocarpha 1 19Piptolepis 4 9Proteopsis 2 22Stenocephalum 2 12Stilpnopappus 1 1Vernonanthura 25 165Vernonia 2 2

Vernonieae Total 143 768

Grand Total 535 2863

tribe species samplesAnthemideae 1 1Astereae 57 266Barnadesiinae 5 12Cardueae 3 13Cichorioideae 1 1Eupatorieae 152 1232Gnaphalieae 15 40Helenieae 4 23Heliantheae 59 159Lactuceae 4 6Moquinieae 1 5Mutisieae 46 173Plucheeae 9 25Senecioneae 35 139Vernonieae 143 768Total 535 2863

faunistics

proportions of reared specimens

proportions of species

(excl. Cecidomyiidae)

The main herbivore families on Compositae

Tephritidae Agromyzidae Tortricidae Pterophoridae Pyralidae Cecidomyiidae Curculionidae; &c

Diptera: Tephritidae

4700 described species fruit fly pests: medfly -

Ceratitis, Anastrepha, Rhagoletis; Dacus, Bactrocera

Compositae main host family

Diptera: Tephritidae tribe generaAcrotaeniini Caenoriata

TetreuarestaTomoplagia

Dithrycini CecidocharesEutretini Dictyotrypeta

ParacanthaMyopitini NeomyopitesTephritini Acinia

DioxynaDyseuarestaEuarestoidesOxynaPlaumannimyiaTrupaneaTrypanarestaXanthaciura

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)

Lepidoptera: 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

• Unadilla Phycitodes mucidella

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

Adaina (Lep: Pterophoridae) generalists, specialists, both?

Adaina bipunctatus South America to Florida

and the Caribbean in Brazil, our records span

54 host species in 7* different tribes of Compositae

Adaina microdactyla Europe, widespread (Central

Asia?) strictly monophagous on

Eupatorium cannabinum L.

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

Urophora Neotrop X X

Nearctic X X

insect-plant biogeography

large-scale contrasts

Serras Sul

Cerrados SP

Espinhaço

Mantiqueira Rio

SP

240 17 4% 130

Southeast South

Plant species per region

61 41 34%

18

Southeast South

Insect species per region

Diptera (2 families, 92 spp)

Lepidoptera (3 families, 28 spp)

Insect species per region

Southeast South

Southeast South

51 11 30 11 10 7

Similarity of Asteraceae vs. herbivores

South

Southeast

plants

insects

South

Southeast

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

112 plant samples, 121 host records

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

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

Mário Almeida Neto, 2006 – PhD

Effects of degradation on interactive assemblages plants and insect herbivores in a cerrado gradient

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 10 Gochnatia orbiculata 1 Wunderlichia senaeii 1 !

Wunderlichia mirabilis 10 !

A picky feeder

Lewinsohnia magna Prado & Norrbom, 2006

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?