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Host Fungi and Feeding Habits of Ciidae (Coleoptera) in aSubtropical Rainforest in Southern Brazil, with an Overview of Host Fungi of Neotropical CiidsAuthor(s) :Letcia V. Graf-Peters, Cristiano Lopes-Andrade, Rosa Mara B. daSilveira, Luciano de A. Moura, Mateus A. Reck and Flvia Nogueira de SSource: Florida Entomologist, 94(3):553-566. 2011.

Published By: Florida Entomological SocietyDOI: 10.1653/024.094.0320URL: http://www.bioone.org/doi/full/10.1653/024.094.0320

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Graf-Peters et al.: Feeding Habits of Neotropical Ciidae 553

HOST FUNGI AND FEEDING HABITS OF CIIDAE (COLEOPTERA) IN ASUBTROPICAL RAINFOREST IN SOUTHERN BRAZIL, WITH AN OVERVIEW

OF HOST FUNGI OF NEOTROPICAL CIIDS

LETCIA V. GRAF-PETERS1, CRISTIANOLOPES-ANDRADE2,*, ROSAM ARAB. D A SILVEIRA3, LUCIANODE A. MOURA4,M ATEUS A. RECK 3 ANDFLVIANOGUEIRADE S 51Programa de Ps Graduao em Ecologia, Departamento de Ecologia, Universidade Federal do Rio Grande do Sul

(UFRGS), Porto Alegre, RS, Brasil

2Laboratrio de Sistemtica e Biologia de Coleoptera, Departamento de Biologia Animal, Universidade Federal de Viosa (UFV), Viosa, MG, Brasil

3Laboratrio de Micologia, Departamento de Botnica, Universidade Federal do Rio Grande do Sul (UFRGS),Porto Alegre, RS, Brasil

4Programa de Ps-Graduao em Biologia Animal, Departamento de Zoologia, Universidade Federal do Rio Grandedo Sul (UFRGS), Porto Alegre, RS, Brasil

5Universidade de Braslia (UnB), Campus Planaltina (FUP), Braslia, DF, Brasil

*Corresponding author; E-mail: [email protected]

ABSTRACT

Ciids or minute tree-fungus beetles (Coleoptera: Ciidae) are amongst the most abundantand speciose fungivorous beetles. They spend most of their lives in or around polypore ba-sidiomes, which are used as a food resource and shelter by larvae and adults. The study of Neotropical ciids is incipient and there is no comprehensive work on their host fungi. Thepresent work provides a descriptive analysis of the Ciidae fauna, its feeding habits and poly-pore hosts at a subtropical rainforest in So Francisco de Paula, southern Brazil. A discus-sion on the current knowledge of host fungi of Neotropical Ciidae is also provided. Polyporebasidiomes were collected in eld trips carried out monthly from Aug 2006 to Mar 2007 andkept in the laboratory for up to 3 mo, while adult beetles were continuously captured fromthem. Basidiomes of 376 individual fungi were collected, comprising a total of 40 species. Among these, 152 individual fungi of 33 species had ciid beetles. Twenty-one species of ciidswere recognized among 233 emergent adults. Only 1 ciid species was considered monopha-gous, 6 were considered oligophagous, and 6 polyphagous. Eight ciid species had less than 5occurrences, and thus could not be included in any category. There is empirical evidence,from data provided or compiled herein, indicating that some morphologically similar Ciidaespecies, usually comprising a species group, frequently use the same or closely related spe-cies of fungi as the host. This is the rst faunistic study on Ciidae and their host fungi in theNeotropical region.

Key Words: fungivory, mycetobionts, Tenebrionoidea, polypores, Basidiomycota

RESUMEN

Los ciidos, conocidos como escarabajos diminutos de hongos de rboles (Coleoptera: Cii-dae), se encuentran entre los escarabajos fungvoros ms abundantes y con un gran n-mero de especies. Pasan la mayor parte de su vida en o alrededor de un basidioma declase poliporo, que es utilizado como fuente de alimento y refugio por larvas y adultos.El estudio de los ciidos neotropicales es incipiente y no hay un trabajo exhaustivo sobrelos hongos hospederos. El presente trabajo presenta un anlisis descriptivo de la faunade Ciidae, sus hbitos alimenticios y los hospederos poliporos en una selva subtropicalen So Francisco de Paula, en el sur de Brasil. Tambin, se provee una discusin sobreel conocimiento actual sobre los hongos hospederos de las especies de los Ciidae neotro-picales. Los basidiomas poliporos fueron recolectados mensualmente en salidas decampo realizadas desde agosto del 2006 hasta marzo del 2007 y mantenidos en el labo-ratorio durante un mximo de tres meses, mientras que los escarabajos adultos fueroncapturados de forma continua. Se recolectaron basidiomas de 376 hongos individuales,comprendiendo un total de 40 especies. Entre estos, habian escarabajos presentes en 152de los hongos individuales que representan 33 especies de hongos. Veintin especies deciidos fueron reconocidas, con 233 datos de ocurrencia. Slo una especie de ciido se con-


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554 Florida Entomologist 94(3) September 2011

sider monfaga, seis se consideraron oligfagas y seis polfagas. Hubo menos de cincoapariciones en ocho de las especies de ciidos y por lo tanto no fue posible incluirlas enninguna categora. Hay evidencia emprica, a partir de los datos obtenidos o compilados,indicando que algunas espcies de Ciidae que son morfolgicamente similares y queusualmente son del mismo grupo de especies, con frecuencia usan la misma especie dehongo o especies de hongos estrechamente relacionados como hospedero. Este es el pri-mer estudio faunstico de Ciidae y sus hongos hospederos en la regin Neotropical.

Insects, particularly dipterans and coleopter-ans, are the animals that most frequently utilizeresources from fungi (Hanski 1989; Komonen2003; Amat-Garca et al. 2004). The consumptionof mycelium, basidiomes, or spores of fungi iscalled either fungivory or mycophagy, and may beone of the oldest feeding habits of beetles (Gillott1982; Lawrence 1989). The specialization in using

1 or few parts of fungi has led to special adapta-tions of the mouthparts, ovipositor, feeding hab-its, and life cycle of fungivorous organisms(Lawrence 1989).

Fungi are not homogeneous resources, and nu-trients may be concentrated 10 times more in thebasidiomes than in the substrate on which theygrow (Hsu et al. 2002). Besides being rich in pro-teins and carbohydrates (Gooday 1995; Hsu et al.2002), basidiomes have large amounts of biologi-cally important elements, such as phosphorousand nitrogen (Watkinson et al. 2006), which, for ex-ample, may accelerate the development of the lar-vae of beetles (Martin 1979). However, basidiomesmay also contain high concentrations of toxins,such as phenols, pyrones, and heterocyclic nitro-gen complexes. Therefore, there is great selectivepressure for beetles to develop mechanisms toavoid intoxication against these substances whileusing them as food or habitat (Martin 1979).

Feeding on basidiomes may be facultative orobligatory for fungivorous beetles (Robertson etal. 2004; Grimaldi & Engel 2005). Insects that de-pend on fungi as food and shelter in all their de-velopmental stages are called mycetobionts(Hammond & Lawrence 1989). Among insects,minute tree-fungus beetles in the family Ciidaeare included among the most abundant and spe-ciose mycetobionts, and currently comprisearound 650 described species grouped in 42 gen-era (Lopes-Andrade 2008b; Lawrence & Lopes- Andrade 2010). They are usually gregarious, andsometimes thousands of individuals may live in-side a single basidiome (Lawrence & Britton1991). As true mycetobionts, ciids spend most of their lives in or around a basidiome, leaving itonly for dispersal. Both adults and larvae buildgalleries inside the basidiome, and pupation also

occurs there (Lawrence 1973; Costa et al. 1988). As females usually oviposit continuously for along period, overlapping generations are usuallyobserved (Lawrence 1973).

In the Neotropical region (sensu Morrone2002), the study of Ciidae is incipient. There are

about 150 described species in 13 genera reportedin the region, and dozens of undescribed formsknown from museum and institutional collections(Lawrence & Lopes-Andrade 2008; Lopes-An-drade 2008b). The present work provides a de-scriptive analysis of the Ciidae and their feedinghabits and their polypore hosts at a subtropicalrainforest in So Francisco de Paula, southern

Brazil. A compilation and brief discussion on thecurrent knowledge of host fungi of Neotropical Ci-idae is also provided. This is the rst faunisticstudy of Ciidae and their host fungi in the Neotro-pical region.

M ATERIALS ANDMETHODS

Study Area

This study was carried out at the National For-est of So Francisco de Paula (FLONA/SFP,2923-2927S, 5023-5027W), located in themunicipality of So Francisco de Paula, in thestate of Rio Grande do Sul, southern Brazil.FLONA/SFP has remnants of subtropical rainfor-est (Diverio et al. 2001), which occupies 40% of itsarea, in addition to plantation areas of Araucariaangustifolia (Bertol.) Kuntze, Pinus spp., and Eu-calyptus spp. (Dobrovolski et al. 2006). The wholearea covers 1,606 ha and reaches a maximum al-titude of 923 m (Diverio et al. 2001). The climateis temperate, without a dry season, and with a hotsummer (Cfa in the Koeppen-Geiger climateclassication, sensu Peel et al. 2007). All mo arerainy, with an average annual precipitation of 2,252 mm (Backes et al. 2005).

Field Collection

Field trips were carried out monthly from Aug2006 to Mar 2007. During arbitrary walks alongtracks in forest areas of FLONA/SFP, polyporebasidiomes, which usually develop on dead treetrunks, were collected with a knife. Sampling of the same individual fungi in subsequent eldtrips was avoided by following different tracksduring each eld trip. Young basidiomes, which

usually do not have ciids, were not collected. Anindividual fungus was dened as the basidiome(s)occurring on a single trunk, because it is not pos-sible to know where an individual fungus beginsand ends in the eld. Therefore, the number of ba-sidiomes sampled from different individual fungi


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varied. Sampling effort was quite constant, withan average of 40 individual fungi collected pereld trip. After removing the basidiomes from thetrunks, they were separately packed in papertowels and plastic bags to prevent escape of beetlelarvae and adults.Laboratory Work

Samples were sorted for beetles within 3 daysafter of eld collection to avoid fungal rotting andbeetle death. After the rst beetle sorting, the ba-sidiome(s) of each individual fungus was kept in-dividually to allow newly emerged beetles tobreed. Basidiomes were stored in plastic contain-ers covered with a ne mesh cloth to keep beetlesinside (Komonen 2001). Moist tissue paper wasput inside the containers to prevent fungi fromdrying out, and the containers were partiallyclosed (Jonsell et al. 2001; Schigle 2008).

As it was difcult to observe beetles outsidethe woody fungi, their containers were wrappedin aluminum foil and a glass vial was attached toeach 1 to attract beetles to light (Jonsell et al.2001). However, not all beetle species were at-tracted to light, so all fungi were dissected 3 molater to observe whether or not there were livebeetles inside them. Before being dissected, allfungi were submitted to humidity monitoring andextraction of adult beetles twice a week. For indi-

vidual fungi hosting a large number of adult bee-tles, at least 50 beetles were collected to guaran-tee capture of all species. According to Schigle(2008), direct collecting on the fungus and rearingadult beetles from their basidiomes remain reli-able and sensible methods of the eld research.Due to the methodology used here, all host fungirecords were treated as breeding records.

All fungi that had associated Ciidae were iden-tied following the pertinent works on their tax-onomy (Ryvarden & Johansen 1980; Gilbertson &Ryvarden 1986, 1987; Ryvarden 1991; Silveira &Guerrero 1991; Ryvarden & Iturriaga 2003; Ry-varden 2004). A key to the pileate polypores foundin FLONA/SFP was provided by Silveira et al.(2008) based on the fungi collected for the presentstudy, including all species except for Mycobonia

ava (Sw.) Fr. (Polyporales: Boreostereaceae). Voucher specimens of the fungi were deposited atthe ICN herbarium (Instituto de Biocincias -UFRGS). Adult ciids were identied by compari-son to named specimens and literature data(Lawrence 1967, 1971; Lopes-Andrade et al. 2002;Lopes-Andrade & Lawrence 2005; Lopes-An-drade 2008b). Voucher specimens of the adult ci-

ids were deposited at the collection of the Museude Cincias Naturais, Fundao Zoobotnica doRio Grande do Sul (MCNZ, Porto Alegre, RS, Bra-zil), and at the Lopes-Andrade Collection housedin the Universidade Federal de Viosa (LAPC, Viosa, MG, Brazil).

Classication of Feeding Habits

The classication of insects as specialists andgeneralists is based on the number of hosts uti-lized by each species. However, such classication

is a matter of convention, because species of a ma- jor taxonomic group may show a continuum in thenumber of host species (Thompson 1998; Begon etal. 2006). In the case of fungivorous insects, thereare divergent opinions on how many records arenecessary for a given fungus species to be consid-ered as a host (Lawrence 1973; Orledge & Rey-nolds 2005). Consequently, studies on feedinghabits of fungivorous insects are based on differ-ent concepts of feeding specicity, and there is nosingle or most correct classication (Jonsell et al.1999; Jonsell & Nordlander 2004). Here, we con-sidered monophagous species as strict specialists(who feed in only 1 host species). When a ciid spe-cies exclusively or preferably used 1 fungus fam-ily as its host (according to Kirk et al. 2001), itwas dened as oligophagous, otherwise as polyph-agous (Gess & Gess 2004; Schoonhoven et al.2005; Blthgen & Metzner 2007). Therefore, wecalled oligophagous species the specialists with atleast 90% of occurrence in the same fungus fam-ily. When the percentage of occurrences in a sin-gle fungus family was less than 90%, the ciid spe-cies was considered polyphagous (generalist).Here, an occurrence refers to the collection of 1 to

several specimens of a ciid species in a single in-dividual fungus. Classication of feeding habitswas applied only to ciid species with at least 5records of occurrence.

RESULTS

Basidiomes of 376 individual fungi were col-lected, comprising a total of 40 species. Amongthese, 152 individual fungi of 33 species (see Figs.1-8 for a few examples) had ciid beetles. The ciidhost fungi belonged to 7 families, 6 in the orderPolyporales and 1 in Hymenochaetales (Table 1).Basidiomes of the following 7 fungi species weredevoid of Ciidae: Abundisporus subexibilis(Berk. & M. A. Curtis) Parmasto, Antrodiella lie-bmanii (Fr.) Ryvarden, Antrodiella reexa Ry-varden & Nez, Inonotus fulvomelleus Murrill,

Junghuhnia sp. (probably J. minuta I. Lindblad &Ryvarden), Laetiporus sulphureus (Bull.) Murrill,and Polyporus ciliatus Fr. These non-host speciesare not listed in Tables 1 and 3. The occurrence of ciids in Mycobonia Pat., Amauroderma Murrill,

Flaviporus Murrill, and Junghuhnia Corda arethe rst records of ciids feeding on fungi of thesegenera.

Twenty-one species of ciids (Table 2) were rec-ognized, with 233 occurrence data. In severalcases there was more than 1 ciid species in an in-dividual fungus. Ten ciid species were identiedto species level, 9 were determined to genus level


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only, and 2 species belong to 2 undescribed genera(Table 2). The following 4 ciid species (Figs. 9-12)are new country records for Brazil:Ceracis sim-

plicicornis (Pic), Cis melliei Coquerel, Xylogra- phus corpulentus Melli, and X. gibbus Melli.These 4 species were previously known only fromtheir original descriptions. Three species-groupsof Cis Latreille (named fagi , melliei and vitulus byLawrence 1971), each with 1 species fromFLONA/SFP (see Table 2), are new countryrecords of the groups from Brazil.

The sampled ciid species had variable hostranges (Table 3). Scolytocis fritzplaumanniLopes-Andrade was the only monophagous spe-cies, with all 19 occurrences inGanoderma aus-trale (Fr.) Pat. Six ciid species were considered oli-gophagous (Table 3). Among these oligophagousspecies, Ceracis limai Lopes-Andrade, Madureira& Zacaro and Gen.1 sp. were exclusively ormostly frequently associated with Hymenocha-etaceae. The remaining oligophagous specieswere exclusively or mostly frequently associated

with Polyporaceae. Six ciids were consideredpolyphagous (Table 3). Eight ciid species had lessthan 5 occurrences, and thus could not be in-cluded in any category (Table 3).

Among the 8 ciid species without an attrib-uted feeding habit, 3 showed a tendency to oli-gophagy:Cis sp.3 (comptus group) and Cis dia-dematus Melli, each with 3 occurrences only inPolyporaceae species; and Cis kawanabeiLopes-Andrade, with 4 occurrences in Rigi-doporus spp. (Meripilaceae). Three non-catego-rized ciid species showed a tendency to polyph-agy: Cis sp. 5 ( fagi group) with 3 occurrences,each in a fungus of a different host family;Cismelliei with 3 occurrences in hosts of 2 families;and Ceracis sp.3 with 2 occurrences, each in ahost from different families. No tendency couldbe traced for X. gibbus because it was capturedonly once. The last non-categorized ciid species,Gen.2 sp., occurred in only 1 host fungus,Peren-niporia martii (Berk.) Ryvarden (with 4 occur-rences).

Figs. 1-12. Some host fungi (1-8) and Ciidae (9-12) collected in a subtropical rainforest in So Francisco de Paula(Rio Grande do Sul, southern Brazil): 1,Ganoderma australe ; 2, Rigidoporus concrescens ; 3, Fomitella supina ; 4, enzites betulina ; 5, Perenniporia martii ; 6,Trametes membranacea ; 7,Trichaptum sector ; 8, Flaviporus subhydro-hilus ; 9, male of Ceracis simplicicornis , lateral view; 10, male of Cis melliei , dorsal view; 11, male of Xylographus

corpulentus , lateral view; 12, male of Xylographus gibbus , lateral view.


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T A B L E 1 . H O S T F U N G I O F C I I D A E C O L L E C T E D A T A S U B T R O P I C A L R A I N F O R E S T I N S O F R A N C I S C O D E P A U L A ( R I O G R A N D E D O S U L , S

O U T H E R N B R A Z I L ) .

O r d e r

F a m

i l y

F u n g u s s p e c

i e s

H y m e n o c

h a e t a

l e s

H y m e n o c

h a e t a c e a e

C y c l o m y c e s t a b a c i n u s

( M o n

t . ) P a t .

I n o n o t u s s p .

P h e l l i n u s a p i a h y n u s

( S p e g .

) R a j c h e n

b . a n

d J . E

. W r i g

h t

P h e l l i n u s f a s t u o s u s

( L v

. ) S . A h m a d

P h e l l i n u s g i l v u s

( S c h w e i n .

) P a t .

P h e l l i n u s g r e n a d e n s i s ( M u r r i

l l ) R y v a r

d e n

P h e l l i n u s w a h l b e r g i i ( F r

. ) D

. A . R

e i d

P h e l l i n u s s p . 1



P o l y p o r a

l e s

B o r e o s t e r e a c e a e

M y c o b o n i a a v a

( S w . )

F r .

G a n o d e r m a t a c e a e

A m a u r o d e r m a c o l t r i c i o i d e s

T . W

. H e n

k e l , A i m e a n

d R y v a r

d e n

G a n o d e r m a a u s t r a l e ( F r .

) P a t .

G r a m m o t

h e l e a c e a e

B j e r k a n d e r a a d u s t a

( W i l l d . ) P

. K a r s t .

M e r

i p i l a c e a e

R i g i d o p o r u s c o n c r e s c e n s

( M o n

t . ) R a j c h e n

b .

R i g i d o p o r u s m i c r o p o r u s

( S o w e r

b y ) I m a z e k

i

R i g i d o p o r u s u l m a r i u s

( S o w e r

b y ) I m a z e k

i

R i g i d o p o r u s s p . 1


P o l y p o r a c e a e

C o r i o l o p s i s r i g i d a ( B e r

k . a n

d M o n

t . ) M u r r i

l l

D a t r o n i a m o l l i s ( S o m m e r

f . ) D o n

k

F o m i t e l l a s u p i n a (

S w . )

M u r r i

l l

L e n z i t e s b e t u l i n a (

L . ) F r .

P e r e n n i p o r i a m a r t i i ( B e r

k . ) R y v a r

d e n

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P o l y p o r u s d i c t y o p u s

M o n

t .

P y c n o p o r u s s a n g u i n e u s

( L . )

M u r r i

l l

T r a m e t e s c u b e n s i s

( S w . )

K r e

i s e l

T r a m e t e s m e m b r a n a c e a

( S w . )

K r e

i s e l

T r a m e t e s v i l l o s a ( S w . )

K r e

i s e l

T r i c h a p t u m s e c t o r

( E h r e n

b . ) K r e

i s e l

S t e c c h e r

i n a c e a e

F l a v i p o r u s s u b h y d r o p h i l u s

( S p e g .

) R a j c h e n

b . a n

d J . E

. W r i g h

t

J u n g h u h n i a u n d i g e r a

( B e r

k . a n

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. A . C

u r t i s )

R y v a r d e n


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DISCUSSION

Ciidae of FLONA/SFP

The Ciidae found at FLONA/SFP are charac-teristic of a Neotropical fauna, and the species,species-groups, and most genera are, for in-stance, quite distinct from those of the Andeanregion (see Lopes-Andrade 2010 for a brief dis-cussion on the composition of the Andean Ci-idae fauna). Among the new records from Bra-zil, C. simplicicornis belongs to the furcifer spe-cies-group, together with the common Neotropi-cal speciesCeracis cornifer (Melli) andCeracis

furcifer Melli. It was previously known onlyfrom the type locality in Buenos Aires, Argen-tina (Pic 1916).Cis melliei belongs to the mel-liei species-group, which comprises alsoCiscrinitus Lawrence, Cis rotundulus Lawrence,Cis ursulinus Casey, Cis hirsutus Casey, andCis hirtellus Jacquelin-Duval, the latter 2 beingpossible synonyms (Lawrence 1971). All species

of the melliei species-group are rarely collected,and few specimens are available in collectionsfor most of them. Xylographus corpulentus and

X. gibbus were formerly known only from Peruand Colombia, respectively. However, both havebeen collected in several localities in southeast-

ern, northeastern, and northern Brazil, but thespecimens from So Francisco de Paula are therst collected in southern Brazil (C.L.A., un-published data). Each of these 2 species of Xy-lographus Melli may indeed constitute a spe-cies-complex, rather than a single species.

Ceracis bicornis Melli, Cis testaceimembris(Pic), andCis kawanabei Lopes-Andrade are spe-cies frequently collected in Brazil (C.L.A., unpub-lished data). The former belongs to thecucullatusspecies-group, and the latter 2 belong to the tau-rus species-group together with Cis sp.1. How-ever, all these species are widespread and poly-morphic, and each may constitute a species-com-plex, instead of a single species.

Cis diadematus was previously known onlyfrom its original description, from Bahia, Brazil(Melli 1849). In fact, it does not fit the genericlimits of Cis and will be transferred to a new ge-nus in a work already in preparation (C.L.A., un-published data). Cis sp.3 possibly belongs to thecomptus species-group, which comprises species

of broad geographic distribution in the Neotropics(Lopes-Andrade et al. 2003; de Almeida & Lopes Andrade 2004) and several Nearctic and Palearc-tic species (Lawrence 1971; Krlik 2002).Cis sp.4belongs to the tricornis species-group, which ismostly Neotropical (Lawrence 1971).

T ABLE 2. SPECIES OF CIIDAE COLLECTED IN BASIDIOMES OFH YMENOCHAETALES ANDPOLYPORALES IN A SUBTROPICALRAINFOREST INS OFRANCISCO DEP AULA(RIO GRANDE DOSUL, SOUTHERNBRAZIL). THE SUPERSCRIPT ABE-FORE A NAME INDICATES THAT IT IS THE FIRST RECORD OF THE SPECIES OR SPECIES-GROUP FROMBRAZIL.

Tribe Ciidae species Species-group

CiiniCeracis bicornis (Melli) cucullatusCeracis limai Lopes-Andrade et al. singularisaCeracis simplicicornis (Pic) furciferCeracis sp.1 (aff.multipunctatus )Ceracis sp.2 (aff. powelli )Ceracis sp.3 furcatus?Cis diadematus MelliCis kawanabei Lopes-Andrade taurusaCis melliei Coquerel amellieiCis testaceimembris (Pic) taurusCis sp.1 taurusCis sp.2 (aff. fasciatus ) avitulusCis sp.3 comptusCis sp.4 tricornisCis sp.5 a fagiGen.1 sp.Gen.2 sp.Strigocis sp.

Orophiinia Xylographus corpulentus Mellia Xylographus gibbus Melli

XylographelliniScolytocis fritzplaumanni Lopes-Andrade fritzplaumanni


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T A B L E 3 . C I I D A E

A N D T H E I R R E S P E C T I V E H O S T F U N G I O F T H E O R D E R S H Y M E N O C H A E T A L E S A N D P O L Y P O R A L E S I N A S U B T R O P I C A L R A I N F O R E S T I N S O F R A N C I S C O D E P A U L A

( R I O G R A N D E D O S U L , S

O U T H E R N B R A Z I L ) S H O W I N G T H E N U M B E R O F O C C U R R E N C E S ( N ) F O R E A C H C I I D S P E C I E S , T H E N U M B E R O F I N D I V I D U A L F U N G I B E A R I N G C I I D S

( N I N D . F

U N G I ) A N D T H E N U M B E R O F C I I D S P E C I E S ( N C I I D A E S P P . ) F O R E A C H F U N G U S S P E C I E S . C L A S S I F I C A T I O N O F F E E D I N G H A B I T W A S N O T P O S S I B L E F O R T H E

L E S S F

R E Q U E N T B E E T L E S P E C I E S ( S E E T E X T ) .

C e r a c i s b i c o r n i s

C e r a c i s l i m a i

C e r a c i s s i m p l i c i c o r n i s

C e r a c i s s p . 1



C i s d i a d e m a t u s

C i s k a w a n a b e i

C i s m e l l i e i

C i s t e s t a c e i m e m b r i s

C i s s p . 1

C i s s p . 2

C i s s p . 3

C i s s p . 4

C i s s p . 5

G e n . 1 s p .

G e n . 2 s p .

S t r i g o c i s s p .

X y l o g r a p h u s c o r p u l e n t u s

X y l o g r a p h u s g i b b u s

S c o l y t o c i s f r i t z p l a u m a n n i

P o l y p h a g o u s

O l i g o p h a g o u s











M o n o p h a g o u s

N i n d . f u n g i

N C i i d a e s p p .

H y m e n o c

h a e t a

l e s

C y c . t a b a c i n u s

1

1

4

3

6

4

I n o n o t u s s p .

1

1

1

3

3

P . a p i a h y n u s

4

2

6

2

P . f a s t u o s u s

1

1

1

P . g i l v u s

9

1

4

1

1

1 2

5

P . g r e n a d e n s i s

3

1

1

5

3

P . w a h l b e r g i i

6

6

1

P h e l l i n u s s p .

1

1

1

1


2

1

1

1

2


3

1

1

2

2

P o l y p o r a

l e s

M . a v a

1

1

2

2

A . c o l t r i c i o i d e s

5

1

6

2

G . a u s t r a l e

2 0

1 4

2

4

1 9

5 9

5

B . a d u s t a

1

1

1

R . c o n c r e s c e n s

1

1

1

R . m

i c r o p o r u s

1

2

1

4

3


9/15


R . u

l m a r i u s

2

1

5

3

1 1

4


1

1

1


1

1

1

C o r . r i g i d a

6

1

1

8

3

D . m o l l i s

1

1

1

F . s u p i n a

4

1

2

2

1

1 0

5

L . b e t u l i n a

1

1

1

3

3

P e r . m a r t i i

1

1

4

2

3

P e r e n n i p o r i a s p .

2

2

1

P o l . d i c t y o p u s

1

1

1

P y c . s a n g u i n e u s

9

1

1

1

3

1 5

5

T . c u b e n s i s

1

1

1

T . m e m b r a n a c e a

1

1

1

1

8

1 6

3

3 1

7

T . v i l l o s a

1

1

1

1

1

3

8

6

T r i . s e c t o r

1

1

5

7

3

F l . s u b h y d r o p h i l u s

1

1

1

J . u n d i g e r a

1

1

2

2

N o

c c u r r e n c e s

1 4

1 5

1 0

3 1

1 0

2

3

4

3

1 6

3 6

1 0

3

2 0

3

8

4

1 1

1 0

1

1 9

T A B L E 3 . ( C O N T I N U E D ) C I I D A E A N D T H E I R R E S P E C T I V E H O S T F U N G I O F T H E O R D E R S H Y M E N O C H A E T A L E S A N D P O L Y P O R A L E S I N A S U B T R O P I C A L R A I N F O R E S T I N S O F R A N -

C I S C O

D E P A U L A ( R I O G R A N D E D O S U L , S O U T H E R N B R A Z I L ) S H O W I N G T H E N

U M B E R O F O C C U R R E N C E S ( N ) F O R E A C H C I I D S P E C I E S , T H E N U M B E R O

F I N D I V I D U A L

F U N G I B E A R I N G C I I D S ( N I N D . F

U N G I ) A N D

T H E N U M B E R O F C I I D S P E C I E S ( N C I I D A E S P P . ) F O R E A C H F U N G U S S P E C

I E S . C L A S S I F I C A T I O N O F F E E D I N G H A B I T W A S N O T

P O S S I B L E F O R T H E L E S S F R E Q U E N T B E E T L E S P E C I E S ( S E E T E X T ) .

C e r a c i s b i c o r n i s

C e r a c i s l i m a i

C e r a c i s s i m p l i c i c o r n i s




C i s d i a d e m a t u s

C i s k a w a n a b e i

C i s m e l l i e i

C i s t e s t a c e i m e m b r i s

C i s s p . 1

C i s s p . 2

C i s s p . 3

C i s s p . 4

C i s s p . 5

G e n . 1 s p .

G e n . 2 s p .

S t r i g o c i s s p .

X y l o g r a p h u s c o r p u l e n t u s

X y l o g r a p h u s g i b b u s

S c o l y t o c i s f r i t z p l a u m a n n i













M o n o p h a g o u s

N i n d . f u n g i

N C i i d a e s p p .


10/15


Ceracis sp.1 is morphologically similar toCeracis multipunctatus (Melli), a northern Neo-tropical species that also occurs in Alabama andFlorida (USA). Ceracis sp.2 is morphologicallysimilar to Ceracis powelli Lawrence, a speciesfrom southern Arizona (USA) and northern Mex-ico (Lawrence 1967).Ceracis limai is not fre-quently collected, and specimens found inFLONA/SFP are the first known from southernBrazil. Ceracis sp.3 is a small species without sec-ondary sexual characters in males, and of un-known morphological affinities in the Neotropicalregion. It somewhat resembles females of speciesof the furcatus species-group, such as Ceracisvariabilis Melli.

Scolytocis fritzplaumanni was described dur-ing the elaboration of this work, based partiallyon the specimens collected at FLONA/SFP(Lopes-Andrade 2008b). The species seems to berestricted to southern Brazil and is 1 of 3 speciesof Xylographellini found in the country (Lopes- Andrade 2008b).

The genus assignment of the Strigocis sp. fromFLONA/SFP is a matter of discussion. The speci-mens have a sutural ange diverging near theelytral apex and the apex of each protibia bears arow of spines, a combination of features regardedas diagnostic for Strigocis Dury (Lawrence 1971;Lopes-Andrade 2011). The species named Gen.1sp. and Gen.2 sp. belong to 2 undescribed Neotro-

pical genera, each with a small number of speciespreviously collected in northern and southeasternBrazil (C.L.A., unpublished data). It will certainlytake several years to adequately describe the spe-cies of FLONA/SFP. The high proportion of unde-scribed forms, in relation to the described species,had been expected, because Neotropical species of the family have not been studied well until re-cently.

Host Fungi and Feeding Habits

Among the fungi recorded as ciid hosts for therst time, Amauroderma is a pantropical genus(Ryvarden 1991) and Mycobonia is distributedonly in the Neotropical region (Corner 1984). Jun-

ghuhnia and Flaviporus may also be found intemperate regions (Ginns 1980; Gilbertson & Ry-varden 1986), but currently there is no availableinformation on their use as hosts by ciids. Therecords of 5 ciid species in Pycnoporus sanguineus(L.) Murrill, a common species throughout theNeotropical region, is worth mentioning. Thisfungus belongs to the trametoid group and, as theother species of the genus, their basidiomes have

a high concentration of cinnabarins, a group of toxic substances with antibiotic action (Smnia etal. 1998; Oliveira et al. 2007). The high toxicity of these fungi would be expected to function as abarrier for their consumption by insects, andtherefore it would be expected that few beetle spe-

cies could use them as a food resource; which issupported by documented reports. So far, onlyspecies of theCeracis furcifer species-group havebeen collected in Pycnoporus P. Karst. fungi(Lawrence 1973; Gumier-Costa et al. 2003). How-ever, some insects are known to be resistant to thechemicals of their hosts (see Schoonhoven et al.2005 for plant examples). The use of Pyc. san-

guineus by 5 ciid species (see Table 3) suggeststhat insect resistance may also be possibleagainst antibiotic constituents in fungi. Both Ga-noderma australe (Fr.) Pat. and Pyc. sanguineushosted the same number of ciid species atFLONA/SFP, although 59 occurrences of ciidswere recorded from the former species, 1 of thecommonest bracket fungi in the study area, andonly 15 occurrences were recorded from Pyc. san-

guineus . Among the oligophagous species, only 2,C. li-

mai and Gen.1 sp., were found mostly or exclu-sively in Hymenochaetaceae. The other oligopha-gous species were mostly associated with Polypo-raceae. It is interesting to note that none of theoligophagous ciids were mostly associated withthe other 5 Polyporales families, which meansthat fungi of these families were most frequentlyexplored by polyphagous and monophagous spe-cies. Gen.2 sp. had all of its 4 occurrences in Pe-renniporia martii and future records may conrmthat the species is monophagous.

Considering the patchy distribution of thehosts of Ciidae, the existence of strong selectionagainst specialization, particularly monophagy,can be expected to be operating. Such a feedinghabit would only be sustainable if the host were areliably present species amenable to be used ef-ciently as a resource. The only monophagous spe-cies found in FLONA/SFP wasS. fritzplaumanni ,and it occurred in the most frequent and peren-nial fungus, G. australe . The specialization inclosely related hosts (oligophagy), rather than ina single host species, would be the most advanta-geous strategy, because these hosts would bemore efciently located, and variations in popula-tion dynamics of a single fungus species wouldnot affect the availability of resources to such ciidspecies. Several studies suggest that oligopha-gous insects tend to use closely related hosts asresources (Jonsell & Nordlander 2004;Schoonhoven et al. 2005; Bangert et al. 2006;Blthgen & Metzner 2007). This pattern may beapplied to oligophagous ciids, as in the case of C.limai , which occurred only in species of PhellinusQul, except for 1 occurrence in R. ulmarius . Insuch cases, the oligophagous species should have

the capability of detecting volatiles common toclosely related host fungi, and a physiologicalmechanism to allow breeding in these hosts. How-ever, the factors determining host use by ciids arenot clearly elucidated (Guevara et al. 2000). It hasalready been suggested that host fungi have vola-


11/15


tile compounds that attract insects (Jonsson et al.1997; Jonsell et al. 2003; Orledge & Reynolds2005), and it has already been shown that ciidspecies have distinct responses to several fungalvolatiles (Thakeow et al. 2008). Graf (2008) alsoshowed that the consistency of the basidiome isimportant for host selection.

The available surveys or compilations on thehost fungi of Ciidae are for the Nearctic and Pale-arctic faunas (e.g. Paviour-Smith 1960; Lawrence1973; Reibnitz 1999). In these works, most of theciid species were shown to be polyphagous, sev-eral were oligophagous, and a few species weretruly monophagous. Lawrence (1973) suggestedthat the degree of host specicity would begreater in tropical forests than in temperate andsubtropical regions, but he did not suggest possi-ble explanations for this pattern. Future studiesshould concentrate on tropical and subtropicalclimate areas in order to evaluate the degree of specialization of Ciidae and its correlation to lati-tude and/or climate.

Host Fungi of Neotropical Ciidae

The oldest information available was providedby Melli (1849) who cited Pyc. sanguineus as thehost for C. furcifer in Izabal, Guatemala, and byCoquerel (1849) who cited Rigidoporus lineatus(Pers.) Ryvarden (Meripilaceae) as the host forCis melliei at Fort-de-France, Martinique. Inter-estingly, Cis melliei was found in FLONA/SFPand had 3 occurrences, each from a different hostfungus, 2 Hymenochaetaceae and 1 Steccheri-naceae (Table 3). Future records from both loca-tions may show that the species is polyphagous,or that there are regional differences in host-usefor this species.

Lawrence (1971) listed the host fungi for Ne-arctic populations of several Neotropical-NearcticCis species, as follows:Cis castlei (Dury) mainlyin Bjerkandera adusta (Willd.) P. Karst. andTrichaptum biforme (Fr.) Ryvarden; Cis cayensisLawrence mainly in Inonotus porrectus Murrill(doubtful identication, see Lawrence 1971),

Phellinus robiniae (Murrill) A. Ames, and Hexagonia hydnoides (Sw.) M. Fidalgo;Cis creber-rimus Melli in several hosts, which indicatespolyphagous feeding habits; Cis crinitusLawrence, with few records but occurring mainlyin H. hydnoides , Coriolopsis caperata (Berk.)Murrill, and Lopharia papyrina (Mont.) Boidin;Cis hirsutus Casey mainly in H. hydnoides , Fomes

fasciatus (Sw.) Cooke, andGanoderma zonatumMurrill; Cis subfuscus Gorham in Trametes hir-

suta (Wulfen) Pilt, Panellus stipticus (Bull.) P.Karst., Lenzites elegans (Spreng.) Pat., and Pyc. sanguineus . Cis delicatulus (Jacquelin-Duval), of the tricornis species-group, was originally foundin Trametes membranaceae (Sw.) Kreisel (Jacque-lin-Duval 1857) and has 1 record inTrametes vil-

losa (Sw.) Kreisel (Navarrete-Heredia & Burgos-Solorio 2000). Interestingly, the Cis sp.4 fromFLONA/SFP, which also belongs to thetricornisspecies-group, had 80% of its occurrences in theformer fungus and 1 occurrence in the latter. Jac-quelin-Duval (1857) also cited thatCis hirtellusJacquelin-Duval was collected in boletus ungula-tus , which possibly corresponds to Fomitopsis

pinicola (Sw.) P. Karst. Cis uzai de Almeida &Lopes-Andrade was originally found in Pyc. san-

guineus (de Almeida & Lopes-Andrade 2004),where occasionally species of thecomptus species-group, such as Cis subfuscus , are found. Notably,the only species of the comptus species-groupfound in FLONA/SFP,Cis sp.3, had 1 record in

Pyc. sanguineus and the other 2 occurrences wereon different species of the same fungus family.Cischinensis Lawrence, an Asian species introducedin Brazil (Lopes-Andrade 2008a), was observedbreeding in Schizophyllum commune Fr. andother unidentied fungi together with En-nearthron victori Lopes-Andrade & Zacaro. Fi-nally, it is worth mentioning that although theseprevious host records for Cis species seem to benumerous, the data is scanty considering that Cisis the most speciose genus of the Neotropical re-gion, with about 70 described species.

Falsocis brasiliensis Lopes-Andrade was col-lected only in Hymenochaete luteobadia (Fr.)Hhn. & Litsch., wrongly identified as Phellinus

sp. by Lopes-Andrade (2007) but belonging to thesame fungus family, Hymenochaetaceae. Porcu-lus grossus Lawrence was most frequently foundin Rigidoporus Murrill basidiomes ( R. concre-

scens (Mont.) Rajchenb., R. lignosus (Klotzsch)Imazeki, and unidentified Rigidoporus spp.); theother 2 host records for the species,Trametes cor-rugata (Pers.) Bres. and Ganoderma sp., werepossibly incidental (Lawrence 1987; Navarrete-Heredia & Burgos-Solorio 2000). Porculus gros-

sus is a common species in the Neotropical region,and several host fungi suitable for it were col-lected in the present survey. However, this beetlewas not found in FLONA/SFP. Few species occu-pied Rigidoporus basidiomes in FLONA/SFP, 5 of them were polyphagous (C. bicornis , C. limai ,Ceracis sp.1, Ceracis sp.2, and Cis sp.1), whereasCis kawanabei was the only beetle that occurredexclusively in Rigidoporus .

Species of Phellinocis Lopes-Andrade &Lawrence are usually found in Phellinus (Lopes- Andrade & Lawrence 2005). Phellinocis erwiniLopes-Andrade & Lawrence was collected mainlyin basidiomes of Phellinus gilvus (Schwein.) Pat.in Panama, whereas Phellinocis thayerae Lopes-

Andrade & Lawrence was most frequently foundin Phellinus nilgheriensis (Mont.) G. Cunn. in thesame country. However, both ciid species werealso less frequently collected in unidentied

Phellinus spp., and Phellinocis thayerae had 2records in P. gilvus and a single record in Phyl-


12/15


loporia pectinata (Klotzsch) Ryvarden. There areno published data on the host fungi of Phellinocisromualdoi Lopes-Andrade & Lawrence, but thespecies is usually collected in basidiomes of uni-dentied Hymenochaetaceae in southeastern,northeastern, and northern Brazil (C.L.A., un-published data). It is worth mentioning that no

Phellinocis were found in FLONA/SFP, althoughseveral suitable host fungi for them were col-lected. The genus has 2 described species from thenorthern Neotropical region, and only 1 species,

Phellinocis romualdoi , from the southern Neotro-pics. The southernmost record of Phellinocis ro-mualdoi is from Lavras, Minas Gerais (2114S)(Lopes-Andrade & Lawrence 2005), about 1,000km north of FLONA/SFP.

Data on host fungi of the New WorldCeracisMelli are based mainly on records for Nearcticpopulations of Neotropical-Nearctic species(Lawrence 1967), as follows (in part):Ceracis cur-tus (Melli) in Fomes fasciatus and H. hydnoides ;Ceracis nigropunctatus Lawrence mainly in H.hydnoides and Trametes hirsuta ; Ceracis pullulusmainly in P. gilvus , H. hydnoides , and G. zona-tum ; Ceracis punctulatus Casey in P. gilvus andless frequently in several other fungi; and Ceracisquadricornis Gorham mainly in Coriolopsis occi-dentalis (Klotzsch) Murrill,Trametes spp. and H.hydnoides . Ceracis similis Horn was collected inGanoderma lobatum (Schwein.) G.F. Atk. in Mex-

ico (Navarrete-Heredia 1987). Ceracis casta-neipennis Melli was found inTrichaptum sector(Ehrenb.) Kreisel in Cuba, and the enigmaticCeracis taurulus Jacquelin-Duval was taken inTrametes membranaceae (Jacquelin-Duval 1857).The Nearctic Ceracis monocerus Lawrence, amember of the furcifer species-group, is usuallycollected in Pyc. sanguineus (Lawrence 1967), aswell as morphologically similar Neotropical spe-cies of the same species-group, such asC. corniferand C. furcifer (Lawrence 1973; Gumier-Costa etal. 2003). Ceracis simplicicornis in FLONA/SFPhad 90% of its occurrences in Pyc. sanguineus ,conrming the general pattern of host-use by thespecies in the group. Ceracis multipunctatus(Melli) was mostly found inG. zonatum and Fo-mitella supina (Sw.) Murrill (Lawrence 1967). Amorphologically similar species from FLONA/ SFP, Ceracis sp.1, was observed mostly inG. aus-trale (64.5%). Specimens included in the type se-ries of C. limai ( singularis species-group) werecollected in unidentied Phellinus and Gano-derma in southern Brazil (Lopes-Andrade et al.2002). However, the species is most frequentlycollected in basidiomes of Phellinus spp. (C.L.A.,

unpublished data), in a similar pattern as foundin FLONA/SFP (more than 93% of the occur-rences in Phellinus spp.). The closely relatedCeracis singularis (Dury), from North America, isalso found in Phellinus spp., mainly in P. gilvus(Lawrence 1967). It is worth mentioning that no

other species of Ceracis from FLONA/SFP wasfound in Phellinus .

The Neotropical species of Scolytocis Blair (Xy-lographellini) are most frequently found inGano-derma spp., Rigidoporus spp., and Phellinus spp.basidiomes (Lopes-Andrade 2008b). However, afew records provide identication of hosts to spe-cies level, as follows:Scolytocis kiskeyensis Lopes- Andrade in Fomes fasciatus (but also in an uni-dentied Ganoderma ); Scolytocis lawrenceiLopes-Andrade in R. lineatus , R. microporus (Fr.),and Earliella scabrosa (Pers.) Gilb. & Ryvarden(and in Rigidoporus sp.); and Scolytocis panamen-

sis Lopes-Andrade in Fomes pseudosenex (Mur-rill) Sacc. & Trotter (and in Phellinus sp.). Theidentied host fungus of Scolytocis fritzplau-manni , G. australe , observed in So Francisco dePaula and cited by Lopes-Andrade (2008b) corre-sponds exactly to the host records provided for thespecies in the present work. Lopes-Andrade(2008b) also cited an unidentied Ganodermafrom Guaratuba as host for the species, whichcould possibly beG. australe in a very advanceddecaying stage.

CONCLUSION

The present work shows that most of the datapreviously available on host fungi of NeotropicalCiidae were scattered, provided by different au-

thors during more than a century and a half. Thedata provided here on the host fungi of the Ciidaeof FLONA/SFP are based on the rst comprehen-sive survey of host fungi of a Neotropical Ciidaefauna, and a rst step in elucidating the patternsof host-use and host-specialization of NeotropicalCiidae.

Furthermore, there is empirical evidence, fromthe present work and data compiled herein, indi-cating that some morphologically similar ciids,usually comprising a species-group, frequentlyuse the same fungus species or closely relatedspecies as host. Evolutionary and ecological pro-cesses certainly determine host-use by ciids. Fur-ther studies should analyze the co-occurrence of ciid species in a host to evaluate the possibility of competitive exclusion and to explain regional pat-terns of host-use by ciids. Also, future workshould focus on the phylogenetic analyses of ciidsto make possible a comparison to phylogenetic hy-potheses of their host fungi.

ACKNOWLEDGMENTS

This project was partially nanced by Coordenaode Aperfeioamento de Pessoal de Nvel Superior(CAPES) and by the Graduate Program in Ecology of the Federal University of Rio Grande do Sul (grant toL.V.G.P.). C.L.A. was supported by Fundao de Amparo Pesquisa do Estado de Minas Gerais (FAPEMIG: PPP21/2008, CRA - APQ-00049-09; PPM 03/2010, CRA -PPM-00017-10), Conselho Nacional de Desenvolvi-


13/15


mento Cientco e Tecnolgico (CNPq: post-doctoral fel-lowship n 151800/2007-3, from Nov 2007 to Oct 2008;PROTAX 52/2010 n 562229/2010-8), and the GraduateProgram in Entomology of the Federal University of Viosa. L.A.M. was nanced by CNPq (post-doctoral fel-lowship, process n 150639/2009-0). The recognition of Gen.2 sp. as not belonging to Xylographus and the iden-tication of the true Xylographus species were possibleonly after a careful comparison and study of the speci-mens by Vivian E. Sandoval-Gmez, who also kindlycorrected the abstract in Spanish. We thank Tatiana B.Gibertoni for the identication of Hymenochaete luteo-badia , host fungus of Falsocis brasiliensis .

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