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?