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2013 Floral associations of cyclocephaline scarab Matthew Robert Moore Wichita State University

Mary Liz Jameson Wichita State University, [email protected]

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Moore, Matthew Robert and Jameson, Mary Liz, "Floral associations of cyclocephaline scarab beetles" (2013). Papers in Entomology. 151. http://digitalcommons.unl.edu/entomologypapers/151

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Journal of Science: Vol. 13 | Article 100 Moore and Jameson

Floral associations of cyclocephaline scarab beetles

Matthew Robert Moorea* and Mary Liz Jamesonb

Wichita State University, Department of Biological Sciences, 1845 Fairmount, Wichita, KS, USA 67260-0026

Abstract The scarab tribe Cyclocephalini (Coleoptera: : ) is the second larg- est tribe of rhinoceros beetles, with nearly 500 described species. This diverse group is most closely associated with early diverging angiosperm groups (the family Nymphaeaceae, magnoliid clade, and monocots), where they feed, mate, and receive the benefit of thermal rewards from the host . Cyclocephaline floral association data have never been synthesized, and a comprehen- sive review of this ecological interaction was necessary to promote research by updating nomenclature, identifying inconsistencies in the data, and reporting previously unpublished data. Based on the most specific data, at least 97 cyclocephaline beetle species have been reported from the of 58 plant genera representing 17 families and 15 orders. Thirteen new cy- clocephaline floral associations are reported herein. Six cyclocephaline and 25 plant synonyms were reported in the literature and on beetle voucher specimen labels, and these were updated to reflect current nomenclature. The valid names of three unavailable plant host names were identi- fied. We review the cyclocephaline floral associations with respect to inferred relationships of angiosperm orders. Ten genera of cyclocephaline beetles have been recorded from flowers of ear- ly diverging angiosperm groups. In contrast, only one , , has been recorded from dicot flowers. Cyclocephaline visitation of dicot flowers is limited to the New World, and it is unknown whether this is evolutionary meaningful or the result of sampling bias and incomplete data. The most important areas for future research include: 1) elucidating the factors that attract cyclocephalines to flowers including floral scent chemistry and thermogenesis, 2) determining whether cyclocephaline dicot visitation is truly limited to the New World, and 3) inferring evolu- tionary relationships within the Cyclocephalini to rigorously test vicarance hypotheses, host plant shifts, and mutualisms with angiosperms.

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Journal of Insect Science: Vol. 13 | Article 100 Moore and Jameson Keywords: Cantharophily, Scarabaeidae, Dynastinae, , , , Nymphaceae Correspondence: a [email protected], b [email protected], *Corresponding author. Editor: Daniela Takiya and Inon Scharf were editor of this paper. Received: 8 July 2012 Accepted: 13 November 2012 Published 1 October 2013 Copyright: This is an open access paper. We use the Creative Commons Attribution 3.0 license that permits unrestricted use, provided that the paper is properly attributed. ISSN: 1536-2442 | Vol. 13, Number 100 Cite this paper as: Moore MR, Jameson ML. 2013. Floral associations of cyclocephaline scarab beetles. Journal of Insect Science 13:100. Available online: http://www.insectscience.org/13.100

clocephaline visitation of dicot flowers is Introduction poorly known and little studied.

The Cyclocephalini (Coleoptera: Scarabae- Cyclocephaline floral associations have been idae: Dynastinae) is the second largest reported in journals, books, and monographs rhinoceros beetle tribe, currently containing since the late 18th century. However, the prev- 15 genera and nearly 500 described beetle alence, geographic scope, and biological species (Jameson et al. 2002; Ratcliffe 2003; importance of these records are difficult to Smith 2006). Cyclocephalines have a pan- gauge because publications summarizing cy- tropical distribution, though the majority of clocephaline floral visitation are somewhat the group’s generic and species diversity is dated and report floral visitation only for spe- concentrated in the New World (Ratcliffe cific plant families, geographic areas, or 2003; Ratcliffe and Cave 2006). Most genera vegetation types (Henderson 1986; Gibernau are sexually dimorphic, with males having 2003; Gottsberger and Silberbauer- enlarged protarsal claws and females having Gottsberger 2006; Gibernau 2011). The frag- expanded elytral epipleura (Moore 2012). Cy- mentary nature of these data and the citation clocephalines are important economically and of unpublished observations have hampered ecologically as root pests (larvae) and pollina- the ability to identify floral association trends tors (adults) (Ratcliffe 2003; Ratcliffe and within cyclocephaline genera and species. Paulsen 2008). Adult cyclocephaline beetles can be found within the of ear- The phylogeny of the Cyclocephalini was in- ly diverging angiosperm groups (the family vestigated for the first time by Clark (2011), Nymphaeaceae, magnoliid clade, and mono- and the generic-level relationships within the cots; Figure 1) and have been shown to tribe remain an area of active research by M. contribute to pollination in the Annonaceae, R. Moore. Tribal circumscription of the Cy- Araceae, Arecaceae, , Magnoli- clocephalini is subject to change based on aceae, and Nymphaeaceae (Cramer et al. ongoing phylogenetic analyses. This research 1975; Beach 1982; Beach 1984; Young 1986; will provide an evolutionary framework for Young 1988b; Gottsberger 1989; Dieringer et interpreting patterns of floral visitation. Com- al. 1999; Hirthe and Porembski 2003; Maia et pilation and synthesis of a checklist of floral al. 2012). Studies of these interactions indi- associations is needed in order to understand cate that some early diverging angiosperm the ecology of the Cyclocephalini within a groups offer rewards to cyclocephalines in the phylogenetic context. form of mating sites, food, and metabolic boosts associated with floral thermogenicity in This checklist synthesizes data (plant and bee- return for pollination services (Gottsberger tle species, geographic locality, and original 1986; Young 1986; Seymour et al. 2009). Cy- citation) for the floral associations of adult

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Journal of Insect Science: Vol. 13 | Article 100 Moore and Jameson cyclocephaline beetles. Invalid nomenclature unverified plant names were reported accord- in the surveyed literature is identified and cor- ing to the original citation for the floral rected; conflicting data, sources of error, and association, and the name was noted as unre- uncertainty in the data are identified; and un- solved. Occasionally, host plant and beetle published floral association data from species were not assigned an author in the ref- examined voucher specimens are added. The erence for an association. This caused aim of this work is to promote future research problems due to the prevalence of synonyms of these ecological interactions by providing a and homonyms in the plant and insect litera- comprehensive data set of the taxonomic and ture. Resulting ambiguities were rectified to geographic scope of floral visitation for cy- the extent possible and explained in the re- clocephaline beetles. marks column (Appendix 1).

Materials and Methods Borrowed specimens of cyclocephaline spe- cies allowed for direct evaluation of species- Literature was surveyed from 1758 (Linnaeus) level identifications that were reported by to 2012. Keyword searches for all cyclocepha- several authors. Particularly, this included line genera (sensu Ratcliffe and Cave 2006; specimens of Cyclocephala sexpunctata Clark 2011) were conducted in the following Laporte (1840) and C. brevis Höhne (1847) databases: BioOne® (www.bioone.org), collected by George Schatz, Helen Young (La BIOSIS Previews® Selva Biological Station, Costa Rica), Alberto (http://apps.webofknowledge.com/), JSTOR Seres, and Nelson Ramirez (Henri Pittier Na- (www.jstor.org), and Biodiversity Heritage tional Park, Venezuela), with floral Library (www.biodiversitylibrary.org). Every association data that were subsequently pub- host plant reference from Pike et al. (1976) lished or unpublished. Identifications of these was checked for floral association data. specimens (or specimen vouchers) were criti- cally examined (Moore 2011). Exemplar All reported cyclocephaline species names material borrowed from the University of Ne- from the literature were verified by referenc- braska State Museum (authoritatively ing the original species description and identified by B. C. Ratcliffe) and monograph- monographic treatments of the Dynastinae ic treatments (Ratcliffe 2003; Ratcliffe and (Endrödi 1985; Ratcliffe 2003; Ratcliffe and Cave 2006) served as the basis for evaluating Cave 2006). Synonyms or misspelled cy- species identifications as well as detailed im- clocephaline species names in the literature ages of some type specimens. The operating were updated to reflect current nomenclature. assumption was that the collectors and authors All reported host plant names were verified were consistent with their species-level de- using the peer-reviewed botanical taxonomic terminations. Identifications deemed incorrect databases Tropicos (www.tropicos.org) and based on current were updated and (www.plantlist.org). Synonyms noted accordingly. Unpublished host plant or misspelled plant names were updated to data were also found with cyclocephaline reflect current nomenclature based on The specimens in collections. These specimens Plant List (2010). In some cases, scientific were collected by M. R. Moore and deposited names in the literature could not be identified at Wichita State University, Wichita, Kansas, as valid or invalid (e.g., unavailable manu- USA, or loaned from the following institu- script names or conflicting synonyms). Some tions:

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Journal of Insect Science: Vol. 13 | Article 100 Moore and Jameson Concrete and anecdotal evidence of floral as- INBC: Instituto Nacional de Biodiversidad, sociations were also included in the checklist. Santo Domingo de Herédia, Costa Rica The nature of the published association occa- (Angel Solís) sionally needed clarification or elaboration MLUH: Zentralmagazin Naturwissenschaft- (e.g., cyclocephalines reported near flowers licher Sammlungen, Martin Luther Universität but not on them or museum specimens cov- Halle-Wittenberg, Halle, Saxony-Anhalt, ered in resin and pollen). These clarifications Germany (Karla Schneider) were provided in the remarks column of Ap- MNHN: Muséum national d'Histoire naturelle, pendix 1. A large amount of unpublished and Paris, France (Olivier Montreuil) inaccessible data exists with regard to cy- SEMC: Snow Entomological Museum, Uni- clocephaline floral visitation. These records versity of Kansas, Lawrence, KS (Zach Falin provide ambiguous data for plant species, cy- and Jennifer Thomas) clocephaline species, locality, and associated UNSM: University of Nebraska State Muse- voucher information. For example, Schatz um, Lincoln, NE (Brett Ratcliffe and Matt (1990, Table 7.3) recorded known and pre- Paulsen) dicted (without distinguishing the two) plant USNM: U.S. National Museum, Washington, taxa pollinated by dynastines in the Neotrop- D.C. (currently housed at the University of ics. Schatz (1990, Table 7.4) recorded Nebraska State Museum for off-site enhance- cyclocephaline plant visitation at La Selva ment) (Floyd Shockley and Dave Furth) Biological Station, but a large amount of data UVGC: Universidad del Valle de Guatemala, could not be extracted because of the non- Guatemala City, Guatemala (Jack Schuster specific nature of the record (i.e., the data and Enio Cano) were reported at the tribal-level rather than at WICH: Wichita State University, Wichita, KS the species-level). These inaccessible data are (Mary Liz Jameson) important because they report certain associa- ZMHB: Museum für Naturkunde der Hum- tions that are not recorded elsewhere in the boldt Universität zu Berlin, Berlin, Germany literature. Repetitive data from these types of (Johannes Frisch and Joachim Willers) records were omitted from the checklist. Only unique generic or species-level plant associa-

Table 1. Previously unpublished cyclocephaline beetle floral association data.

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Journal of Insect Science: Vol. 13 | Article 100 Moore and Jameson

tions were reported for the beetle tribe from Table 2. Generic-level summary of floral association records for these data sets. These non-specific records are the Cyclocephalini (group names in parentheses are based on APG III (2009)) [? indicates a potentially dubius record, see Appendix 1]. reported at the end the checklist with the in- tention that they be reevaluated with the

addition of more data.

Results

Based on species-specific records from the literature and voucher label data, at least 97

cyclocephaline species from nine or 10 genera (depending on the identity of the cyclocepha-

line reported by Gibbs et al. (1977)) were recorded in association with the flowers of at

least 161 species representing 58 genera, 17 families, and 15 orders (Appendix 1). Exam-

ined voucher specimens occasionally had unique, unpublished, floral association data.

Thirteen new plant associations are provided in Table 1. Examined voucher specimens that

did not have unique data are noted in Appen- dix 1. The most specific data are summarized

at the generic-level for the plant association (plant classification according to the Angio-

sperm Phylogeny Group III (2009)) in Table 2 and are provided in full detail (lowest-level

taxonomy, geographic data, and references) in Appendix 1. Cyclocephaline beetle genera and

their associations with angiosperm plant line- ages were mapped onto the APG III

angiosperm phylogeny (Figure 1).

Five of the 15 cyclocephaline genera were not reported as floral visitors in any of the sur-

veyed literature: Acrobolbia Ohaus (1912), Erichson (1847), Harposcelis

Burmeister (1847), Stenocrates Burmeister (1847), and Surutu Martínez (1955). Prelimi-

nary phylogenetic analysis of the Cyclocephalini indicated that the Neotropical

genus Parapucaya Prell (1934) (Dynastinae: Pentodontini) and the Indonesian archipelago

genus Neohyphus Heller (1896) (Dynastinae: Oryctoderini) fall within a potential newly

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Journal of Insect Science: Vol. 13 | Article 100 Moore and Jameson

Table 2. Continued. (1847) is sister to all remaining genera of the Cyclocephalini + Neohyphyus + Parapucaya.

Erioscelis was included in this checklist be- cause of its documented visitation of several

genera in the Araceae (also visited by other cyclocephalines) and its historical inclusion in

the Cyclocephalini.

Floral associations that are less specific or ambiguous (non-specific records) were also

reported (Appendix 1). For example, Lista- barth (1996) reported dynastine scarabs, with

no further species identification, on three spe- cies of Bactris palms (). These data

include records for Scarabaeidae, Dynastinae, and beetles on flowers that fit the general pat-

tern of cyclocephaline floral visitation (nocturnal visitation of bowl-shaped, thermo-

genic inflorescences). Non-specific records were included in the checklist with the hope

that they may be reevaluated with additional data.

Gathering and interpreting floral association

data were complicated by the prevalancy of synonyms, invalid names, and unavailable

names in the literature. Based on The Interna- tional Code of Zoological Nomenclature

(ICZN 1999), an unavailable name is a name that is excluded from use due to the require-

ments of the code. For example, the unavailable name Cyclocephala inpunctata

was reported in the surveyed literature (Gotts- berger 1986, 1988). C. inpunctata has never

been described in the literature. This name is unavailable and was likely reported in error.

Based on published locality data for the floral association, images of the beetle (Gottsberger

1988; Figure 4a, 5 a–d), and subsequently defined Cyclocephalini (Clark 2011). These published records, we consider this species to

genera were included in the systematic litera- be Cyclocephala quatuordecimpunctata Man- ture searches but yielded no floral association nerheim (1829) (personal communication with

records. The results of Clark (2011) hypothe- B. C. Ratcliffe, April 2011). Synonyms of six sized that the genus Erioscelis Burmeister cyclocephaline genus or species names were

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Journal of Insect Science: Vol. 13 | Article 100 Moore and Jameson reported in the surveyed literature; these inva- spatial data (Moore 2011). The taxonomy of lid names were updated based on current the species C. sexpunctata and C. brevis re- nomenclature (Appendix 2). Synonyms of 25 mains unresolved (a possible species plant genus or species names were reported in complex), and their floral associations were the surveyed literature and on voucher speci- reported in detail (Moore 2011). Some vouch- men label data; these invalid names were er specimens for reported floral associations updated based on current nomenclature (Ap- of C. sexpunctata and C. brevis remain to be pendix 3). examined, and some data will require reinter- pretation after the examination of type Seven unresolved or unavailable plant names specimens. were reported from label data and in the sur- veyed literature (Appendix 4). According to Discussion The Plant List (2010), unresolved names are those for which “it is not yet possible to assign Examination of cyclocephaline floral associa- a status of either ‘accepted’ or ‘synonym.’” tions with respect to inferred relationships of Two of these names, atlanticum angiosperm orders revealed that 10 of the 15 and longivaginata, were una- genera of cyclocephaline beetles have been vailable manuscript names (place-holder recorded from flowers of early diverging an- names for species that were later described) of giosperm groups (the family Nymphaeaceae, Thomas Croat and Michael Grayum (Missouri magnoliid clade, and monocots; Figure 1). In Botanical Garden, St. Louis, Missouri, USA). contrast, only one genus, Cyclocephala, has These species were identified as Philodendron been recorded from dicot flowers (Figure 1). ligulatum Schott and Dieffenbachia tonduzii Experimental and observational studies have Croat and Grayum, respectively (personal demonstrated that cyclocephalines can act as communication with T. Croat and M. Grayum, pollinators in Nymphaeales, , Ar- April 2011). Xanthosoma macrorrhizas is an ecales, , and (Figure 1; unavailable name that was reported by Valerio Table 2) (Cramer et al. 1975; Beach 1982; (1984). This species may be the cultivated, Beach 1984; Young 1986; Young 1988b; naturalized, non-native species Alocasia Gottsberger 1989; Dieringer et al. 1999; macrorrhizos (L.) G. Don (personal commu- Hirthe and Porembski 2003; Maia et al. 2012). nication with T. Croat, April 2011). In these early diverging plant groups, a wide set of floral traits and floral pollination syn- Certain cyclocephaline species were common- dromes indicate a correlation with ly reported as floral visitors. For example, cyclocephaline beetles (large pollen grains Cyclocephala sexpunctata had over 20 floral with sticky exudates, sturdy and funnel- visitation records in the surveyed literature shaped inflorescences or large disc-shaped (Appendix 1). C. sexpunctata is externally flowers, timing of anthesis, and thermogene- nearly identical to C. brevis (sensu Ratcliffe sis) (Thien et al. 2009; Gibernau et al. 2010). 2003; Ratcliffe and Cave 2006). Research on These angiosperm orders offer rewards to cy- these two species showed that they represent clocephalines in the form of mating sites, four, or potentially five, morphospecies food, and heat resources associated with floral (Moore 2011). This conclusion was based on thermogenicity (Young 1986; Seymour et al. male genitalic characters, the form of the fe- 2009). male epipleuron, and extensive range and

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Journal of Insect Science: Vol. 13 | Article 100 Moore and Jameson Some cyclocephaline/ associations are (Schlumpberger et al. 2009). Cyclocephala mutualistic (Cramer et al. 1975; Beach 1982; metrica Steinheil (1874) was observed feeding Beach 1984; Young 1986; Young 1988b; on in flower heads of Verbesina enceli- Gottsberger 1989; Dieringer et al. 1999; oides (Cav.) Benth. and Hook. f. ex A. Gray Hirthe and Porembski 2003; Maia et al. 2012). (Asterales) in (Hayward 1946). Ervik and Knudsen (2003) provide a compel- predation in phytophagous scarabs is ling argument that scarab pollination of the rare, the only other known example being Nymphaeaceae (Nymphales) is a mutualistic some members of the subtribe Anisopliina relationship that dates to the early Cretaceous. (Scarabaeidae: Rutelinae: Anomalini) that Whether this represents an example of coevo- feed on grass seeds (Poaceae) (Jameson et al. lution is unclear, and only one study has 2007). addressed this hypothesis (Schiestl and Dötterl 2012). Schiestl and Dötterl (2012) argued that In contrast to apparent destructive associations volatile organic compound produc- with dicots, only one detailed account pro- tion/detection systems arose in the vides evidence of a cyclocephaline beetle Scarabaeoidea during the Jurassic, whereas pollinating a eudicot. Prance (1976) observed floral volatile organic compounds arose in the male and female Cyclocephala verticalis Cretaceous/Paleocene. This was taken as evi- Burmeister (1847) occupying the inflores- dence that early diverging angiosperm cences of Lecythis, Corythophora, and plant/scarab associations evolved due to a Eschweilera () in Amazonas, . preexisting sensory bias in scarabs rather than C. verticalis was strong enough to lift the as a result of coevolution (Schiestl and Dötterl closed androphore flap of (Eri- 2012). However, coevolution could not be cales) inflorescences and displayed selective ruled out for the mutualism between cy- feeding of floral parts, eating only staminode clocephaline scarabs and aroid flowers tissue at the apex of the androphore and leav- (Schiestl and Dötterl 2012). ing fertile stamens untouched (Prance 1976). Based on these observations, C. verticalis was Floral visitation of the core eudicot clade considered a likely pollinator of some Lecy- (Figure 1) by cyclocephalines is poorly de- thidaceae genera, though this hypothesis was scribed and, in certain cases, differs not tested (Prance 1976). significantly from a pollination mutualism. Such cases involve feeding and mating within Gottsberger (1986) considered cyclocephaline flowers in which cyclocephalines have no ap- floral visitation of the dicot families Apocy- parent pollinating function and may destroy naceae (Gentianales), Calophyllaceae the reproductive capability of the plant. For (Malpighiales), and Sapotaceae (Ericales) to example, in the Brazilian dicot mon- be opportunistic. In the absence of early di- ocantha Haw. (), Cyclocephala verging angiosperm host flowers, Gottsberger have been observed mating within the flowers (1986) hypothesized that cyclocephalines and feeding on stamens (Lenzi and Inácio would visit strongly scented flowers of other Orth 2011). Observations made on Echinopsis groups. Cyclocephalines have been shown to ancistrophora Speg. subsp. ancistrophora aggregate based on floral scent compounds (Caryophyllales) flowers indicate that Cy- alone (Gottsberger et al. 2012). Cyclocepha- clocephala visitors display destructive feeding line species (and populations) likely are behavior and do not contribute to reproduction biased towards a wide range of floral scent

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Journal of Insect Science: Vol. 13 | Article 100 Moore and Jameson compounds. Eudicot species with geograph- multiple host plant genera within a family (ol- ically variable floral scent profiles may evolve igophagous), and 27 species have been scents that incidentally stimulate cyclocepha- recorded from multiple host plant families line aggregation by randomly sampling the (polyphagous) (Appendix 1). Single inflores- sensory bias range of scarabs present in that cences often contain multiple cyclocephaline area (e.g., Schlumpberger and Raguso 2008; species, and an extreme example is Dieffen- Schlumpberger et al. 2009). This scenario, if bachia nitidipetiolata Croat and Grayum accurate, would lend support to the hypothesis (Alismatales), which was visited by at least of Schiestl and Dötterl (2012) that preexisting nine Cyclocephala species at La Selva Biolog- sensory biases in cyclocephalines have an im- ical Station, Costa Rica (Young 1990; see portant role in determining the host flower Croat 2004 for plant identification). These profile of a given cyclocephaline species. multi-species aggregations might be explained if floral scents are serving as sex pheromones Based on the assembled data (Appendix 1), for multiple cyclocephaline species (Schatz cyclocephaline visitation of is limited 1990). This hypothesis may be supported by to the New World. It is unknown whether this the observations of Gottsberger et al. (2012) shift represents an evolutionary event that oc- that Cyclocephala literata Burmeister will ag- curred in New World cyclocephalines. gregate due to floral scent compounds alone. Observations of cyclocephalines on dicot flowers (Figure 1) have largely been made by The consequences of polyphagous and oli- chance and have not been the subject of rigor- gophagous cyclocephalines for pollination ous experimentation or sampling protocols. efficiency have been experimentally ad- Thus, it is quite possible that Old World cy- dressed, indicating that cyclocephaline floral clocephalines (Ruteloryctes, Peltonotus, and visitors are differentially important as pollina- potentially Neohyphus) visit both early diverg- tors due to an interaction between their ing angiosperm groups and dicot groups, but relative abundance and specific behavior dicot associations have not been recorded. (Young 1986, 1988a, b, 1990). It is less clear However, it is certain that the known diversity how cyclocephalines species, which often ma- of host flowers lineages is much higher for te inside inflorescences, maintain sexual New World cyclocephalines (15 orders, 17 isolation in close proximity to multiple con- families, and 58 genera) compared to Old generics. A single infloresence may host large World cyclocephalines (two orders, two fami- crowds of beetles, often more then 30 individ- lies, and three genera) (Appendix 1). This uals (Maia et al. 2012). Sexual isolation may correlation may indicate that the radiation of be maintained due to interspecific mating the cyclocephalines in the New World was morphology (Moore 2012). Sexually dimor- accompanied by a subsequent increase in the phic cyclocephaline species have enlarged diversity of their floral associations. protarsal claws (males), and the elytral epipleuron variably expanded into a shelf or Cyclocephaline species are generally oli- flange (females). Morphological differences gophagous or polyphagous. For among epipleural expansions are useful for cyclocephaline species with multiple host rec- species-level identification in the Cyclocepha- ords, only seven species have been recorded lini (Ratcliffe 2003). Females have sclerotized from a single host plant genus (monopha- patches, sometimes with setae, on the ventral gous), 23 species have been reported from portion of epipleural expansions (Moore

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Journal of Insect Science: Vol. 13 | Article 100 Moore and Jameson 2012). It is hypothesized that the interaction diversification on New World dicots. Re- between the male protarsal claw, the female search on cryptic species of host and epipleural expansions, and the ventral portion beetles is fundamental to understanding this of the female elytra serves as a pre-copulatory system. This includes the role of floral volatile sexual isolation mechanism. Further sexual compounds in attracting cyclocephaline bee- isolation between species is accomplished by tles and patterns of pollination, herbivory, and species-specific differences in male genitalic interspecific competition within floral hosts. structure (Moore 2012). The male protarsal claw and the female epipleuron may also be Acknowledgements involved in intraspecific mate competition. For example, male Cyclocephala gravis Bates We thank Brett Ratcliffe (University of Ne- were observed clinging tightly to the epipleu- braska State Museum) and Ron Cave ral structures of a female (guarding behavior), (University of Florida) for providing travel thus limiting the mating access of other C. funding, specimens for this research, and val- gravis males (Moore 2012). Cyclocephaline uable advice on preparing this manuscript. We beetles exhibit some similarity to hopliine are grateful to Michael Grayum, Thomas Cro- scarabs (Scarabaeidae: Rutelinae: Hopliini), at (both Missouri Botanical Garden), and which are generalist flower visitors in South Boris Schlumpberger (University of Munich) Africa (Ahrens et al. 2011). Sexual dimor- for their botanical expertise. Curators and col- phism has evolved independently several lections managers in the Methods section are times within the Hopliini (Ahrens et al. 2011). gratefully acknowledged. This work was sup- Evolution of sexual dimorphism in hopliines ported, in part by NSF DBI 0743783 to S. could be tied to the group’s biology, as they Scott, E. Moriyama, L.-K. Soh, and M. L. feed and compete for mates within inflores- Jameson; NSF DEB 0716899 to B. C. cences (Midgeley 1992; Ahrens et al. 2011). Ratcliffe and R. D. Cave; and Wichita State Sexual dimorphism in cyclocephalines and University. hopliines may be analogous, driven by selec- tion pressures related to oligophagous and References polyphagous flower feeding, mating behavior, and host visitation. Aguirre A, Guevara R, Dirzo R. 2011. Effects of forest fragmentation on assemblages of Cyclocephaline beetles and floral associations pollinators and floral visitors to male- and provide an ideal system for investigating female-phase inflorescences of Astrocaryum ecology (pollination, competition) and evolu- mexicanum (Arecaceae) in a Mexican rain tion (sexual selection, mutualisms). A well- forest. Journal of Tropical Ecology 27: 25–33. founded phylogenetic framework for the Cy- clocephalini is needed to advance this work. Ahrens D, Scott M, Vogler AP. 2011. The While ecological associations between beetles phylogeny of monkey beetles based on and early diverging angiosperm groups is fair- mitochondrial and ribosomal RNA genes ly well-established, additional research is (Coleoptera: Scarabaeidae: Hopliini). necessary to understand the ecological and Molecular Phylogenetics and Evolution 60: historical associations of cyclocephaline bee- 408–415. tles and dicots. Specifically, research is needed to address the apparent cyclocephaline

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Figure 1. Cyclocephaline beetle genera and their associations with angiosperm plant lineages (plant phylogeny from APGIII 2009). Icons de- note beetle genera that are associated with angiosperm plant lineages. Numbers in the icons indicate the number of species for each beetle genus. If the number of beetle species is unresolved due to conflict in the literature, this is indicated with ~ symbol (the number may be X ± 1 species). If the beetle genus has not been satisfactorily associated with the plant lineage, it is denoted with a ? symbol. For each angiosperm plant lineage, the number of families and genera that the beetles are associated with is denoted with #f (number of families) and #g (number of genera). See Appendix 1 for data. High quality figures are available online.

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Journal of Insect Science: Vol. 13 | Article 100 Moore and Jameson Appendix 1. Checklist of floral associations for the Cyclocephalini (Scarabaeidae: Dynastinae).

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Appendix 1. Continued.

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Appendix 1. Continued.

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Appendix 1. Continued.

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Appendix 1. Continued.

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Appendix 1. Continued.

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Appendix 1. Continued.

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Appendix 1. Continued.

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Appendix 1. Continued.

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Appendix 1. Continued.

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Appendix 1. Continued.

Appendix 2. Cyclocephaline synonyms reported in the floral association literature.

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Appendix 3. Plant synonyms reported in floral association literature and on voucher specimen label data.

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Appendix 4. Unavailable and unresolved plant names from the floral association literature and voucher specimen label data.

*ined: a name only that appears in an unpublished manuscript and is thus invalid.

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