Parasite distributions fundamentally depend on the distributions of their hosts but may be more restricted than their hosts. Host-parasite symbioses tend to be spatially aggregated, and widely distributed host-parasite relationships are rare. Here, we combine field observations with published collection data to document the current known distribution of the nematode, Myrmeconema neotropicum, which infects the Neotropical canopy ant Cephalotes atratus. We report 6 new records from different Brazilian ecosystems, bringing the total number of independent observations of this interaction to 11. The broad distribution of these data points suggests that M. neotropicum infects C. atratus throughout its geographic range, although possible disturbance effects and specific habitat associations of the interaction remain unknown.Keywords: Host, Hymenoptera, Ants, Myrmeconema neotropicum, Rang

Dattilo, Wesley

Falcao, Jessica C. F.

Izzo, Thiago J.

Poinar, George, Jr.

Yanoviak, Stephen P.

Undetermined

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J. Parasitol., 99(1), 2013, pp. 155–157 American Society of Parasitologists 2013The Geographic Distribution of Parasite-Induced Fruit Mimicry in Cephalotes atratus(Formicidae: Myrmicinae)Wesley Dáttilo, Jéssica C. F. Falcão, Stephen P. Yanoviak*, George Poinar, Jr.†, and Thiago J. Izzo, Department of Ecology and Botany,Universidade Federal de Mato Grosso, Cuiabá, Mato Grosso 78068–900, Brazil; *Department of Biology, University of Louisville, Louisville, Kentucky 40292;†Department of Zoology, Oregon State University, Corvallis, Oregon 97331. e-mail: yanoviak@gmail.comABSTRACT: Parasite distributions fundamentally depend on thedistributions of their hosts but may be more restricted than their hosts.Host–parasite symbioses tend to be spatially aggregated, and widelydistributed host–parasite relationships are rare. Here, we combine fieldobservations with published collection data to document the currentknown distribution of the nematode, Myrmeconema neotropicum, whichinfects the Neotropical canopy ant Cephalotes atratus. We report 6 newrecords from different Brazilian ecosystems, bringing the total number ofindependent observations of this interaction to 11. The broad distributionof these data points suggests that M. neotropicum infects C. atratusthroughout its geographic range, although possible disturbance effects andspecific habitat associations of the interaction remain unknown.In relatively heterogeneous environments, host–parasite symbioses tendto be spatially aggregated on biogeographic scales (Gregory, 1990; Poulin1998), possibly reflecting differential effects of abiotic and geographicfactors on the lifestyles of hosts and parasites (Poulin, 1995; Morand andKrasnov, 2010). In contrast, parasite distributions are expected to matchthe distribution of their hosts in relatively homogeneous environments(Poulin, 1998). Thus, partly as a consequence of increasing environmentalheterogeneity at larger spatial scales, the distribution of host–parasiteinteractions, the degree of host specificity, and other ecological parametersshould vary across the landscape (Krasnov et al., 2005).Recently, a case of morphological and behavioral change in theNeotropical canopy ant Cephalotes atratus (L.) (Formicidae: Myrmici-nae), parasitized by the tetradonematid nematode Myrmeconema neo-tropicum Poinar and Yanoviak (Nematoda: Tetradonematidae), wasreported in tropical forests of Peru and Panama (Poinar and Yanoviak,2008; Yanoviak et al., 2008). Ants infected with the nematode exhibitseveral behavioral and morphological differences from uninfectedindividuals, the most conspicuous being the change of the gaster colorof infected workers from black to red. This color change causes gasters toresemble ripe fruits of various forest plants, including species ofHyeronima, Psychotria, and Trema, that are consumed by birds(Yanoviak, 2010; S. Yanoviak, unpubl. obs.). The working hypothesisfor this apparent mimicry complex is that it fools frugivorous oromnivorous birds into eating infected gasters, thereby transmitting theparasite to other ant colonies via their feces (Yanoviak et al., 2008). Sinceits discovery, this parasitic relationship has generated many questionsregarding its origins, effects, and mechanisms (Hughes et al., 2008; Shik etal. 2011; Verble et al., 2012). Here, we compile historical collection recordsand field data to summarize the current known distribution of theinteraction.Cephalotes atratus ranges from Panama south to Argentina and iswidely distributed in different ecosystems (from primary forest to urbansettings) and among different elevations; however, records of C. atratusparasitized by M. neotropicum are limited to a few sites in Brazil,Colombia, Peru, and Panama (de Andrade and Baroni Urbani, 1999;Yanoviak et al., 2008). Poinar and Yanoviak (2008) proposed that theinteraction between C. atratus and M. neotropicum occurs throughout thedistribution of C. atratus. However, detecting infected workers in the fieldcan be difficult because the infection frequency among colonies, and thenumber of workers with red gasters within infected colonies, tend to below (ca. 5%; Yanoviak et al., 2008). Consequently, this interaction caneasily be overlooked.Here, we present 6 new records of C. atratus workers parasitized by M.neotropicum in Brazilian ecosystems and evaluate the potential distribu-tion of this interaction. Data were obtained from 3 sources: (1) directobservation of red-gastered C. atratus workers during field expeditionsconducted during 2005 and 2010 in different Brazilian ecosystems (seeYanoviak et al., 2008), (2) references to ‘‘red gaster’’ in publishedcollection records for C. atratus (de Andrade and Baroni Urbani, 1999),and (3) examination of red-gastered specimens in the myrmecologicalcollection of the Museu de Zoologia of Universidade de São Paulo, Brazil(MZSP) (Fig. 1; Table I).Host–parasite interactions are complex, and various factors can affecttheir coevolutionary dynamics (Poulin, 1995; Duffy and Sivars-Becker,2007). The geographic distributions of specialized host–parasite interac-tions tend to be more restricted than those of generalist parasites (Price,1990; Poulin, 1998). Generalists tolerate a wider range of physical andenvironmental barriers and are thus capable of parasitizing a wider rangeof taxa (Tella et al., 1999; Tripet et al., 2002; Krasnov et al., 2005). Indeed,there are few cases where highly specialized parasite–host interactions arewidely distributed (Krasnov et al., 2005). All information that we havegathered to date indicates that the interaction between M. neotropicumand C. atratus is very specialized, consistently results in the distinctive redgaster, and occurs throughout the geographic range of C. atratus asproposed by Poinar and Yanoviak (2008). However, other parasites andpathogens occasionally cause localized reddening of the C. atratusFIGURE 1. Records of Cephalotes atratus (Formicidae: Myrmicinae)parasitized byMyrmeconema neotropicum (Nematoda: Tetradonematidae)in Central and South America. Cephalotes atratus ranges from centralPanama to northern Argentina and Uruguay.DOI: 10.1645/GE-3181.1155exoskeleton (Verble et al., 2012). Such cases are exceedingly rare and notrepeated among workers in a colony and, thus, are unlikely to be confusedwith M. neotropicum infection (S. Yanoviak, unpubl. obs.). Also, 2 otherCephalotes species apparently are infected by Myrmeconema with similareffects on gaster color (de Andrade and Baroni Urbani, 1999; Verble et al.,2012), but the species identity of the parasite remains unknown in bothcases.Cephalotes atratus is a relatively common and conspicuous ant thatinhabits trees in forests as well as in highly disturbed settings (e.g., Weber,1957; Corn, 1976; Yanoviak et al., 2005). Although we show that M.neotropicum infects C. atratus at sites representing different elevations andforest types, the effects of disturbance on this interaction remain unknownand would be an appropriate extension of this work. Specifically, whereasC. atratus often inhabits disturbed sites, the appropriate paratenic vectorsof the parasite (presumably birds) may not. Clearly, direct determinationof the paratenic host is an essential next step.We thank Cesare Baroni Urbani, Rodrigo Feitosa, and Fabrı́cioBaccaro for their comments on earlier versions of this manuscript and forproviding helpful information related to this study. We also thank OfficeNational des Forêts Brazil for logistical support in the Cotriguaçu city.WD and JCFF received Master’s fellowships from CAPES and CNPq,respectively. This is publication no. 20 in the NEBAM technical series.LITERATURE CITEDCORN, M. L. 1976. The ecology and behavior of Cephalotes atratus, aNeotropical ant (Hymenoptera: Formicidae). Ph.D. Thesis. HarvardUniversity, Cambridge, Massachusetts, 200 p.DE ANDRADE, M. L., AND C. BARONI URBANI. 1999. Diversity andadaptation in the ant genus Cephalotes, past and present. StuttgarterBeiträge zur Naturkunde, Serie B (Geologie und Paläontologie),Stuttgart Museum of Natural History, Stuttgart, Germany, 889 p.DUFFY, M. A., AND L. SIVARS-BECKER. 2007. Rapid evolution andecological host-parasite dynamics. Ecology Letters 10: 44–53.GREGORY, R. D. 1990. Parasites and host geographic range as illustratedby waterfowl. Functional Ecology 4: 645–665.HUGHES, D. P., D. J. C. KRONAUER, AND J. J. BOOMSMA. 2008. Extendedphenotype: Nematodes turn ants into bird-dispersed fruits. CurrentBiology 18: 294–295.KRASNOV, B. R., R. POULIN, G. I. SHENBROT, D. MOUILLOT, AND I. S.KHOKHLOVA. 2005. Host specificity and geographic range inhaematophagous ectoparasites. Oikos 108: 449–456.MORAND, S., AND B. KRASNOV. 2010. The biogeography of host-parasiteinteractions. Oxford University Press, Oxford, U.K., 288 p.POINAR JR., G., AND S. P. YANOVIAK. 2008. Myrmeconema neotropicum n.g., n. sp., a new tetradonematid nematode parasitizing SouthAmerican populations of Cephalotes atratus (Hymenoptera: For-micidae), with the discovery of an apparent parasite-induced hostmorph. Systematic Parasitology 69: 145–153.POULIN, R. 1995. Phylogeny, ecology, and the richness of parasitecommunities in vertebrates. Ecological Monographs 65: 283–302.———. 1998. Evolutionary ecology of parasites: From individuals tocommunities. Chapman and Hall, London, U.K, 212 p.PRICE, P. W. 1990. Host populations as resources defining parasitecommunity organization. In Parasite communities: Patterns andprocesses, G. Esch, A. Bush, and J. Aho (eds.). Chapman and Hall,London, U.K., p. 21–40.SHIK, J. Z., M. KASPARI, AND S. P. YANOVIAK. 2011. Preliminaryassessment of metabolic costs of the nematode Myrmeconemaneotropicum on its host, the tropical ant Cephalotes atratus. Journalof Parasitology 97: 958–959.TABLE I. Records of the neotropical canopy ant Cephalotes atratus (Formicidae: Myrmicinae) parasitized by Myrmeconema neotropicum (Nematoda:Tetradonematidae). Records 1 and 2 are from examination of museum specimens and 3–6 are from field data; all others are from published information.Record Country Locality DateCoordinates* andelevation Ecosystem Citation1† Brazil ca. Araguacema, Tocantins 2005 08.8748S, 49.3728W,214 mSavanna This study2† Brazil Caraça range, Minas Gerais unkn. 20.0838S, 43.4668W,1,546 mMontane meadow This study3‡ Brazil ca. Juruena River, Cotriguaçu, MatoGrosso2010 09.8668S, 58.2068W,206 mTropical rainforest This study4 Brazil ca. Marimbondo Waterfall, Chapada dosGuimarães, Mato Grosso2010 15.3348S, 55.6348W,454 mSavanna (gallery forest) This study5 Brazil ca. road AM-240, Presidente Figueiredo,Amazonas2008 02.0428S, 59.8348W,88 mTropical rainforest This study6 Brazil ca. Mutum Waterfall, PresidenteFigueiredo, Amazonas2008 01.9848S, 59.9068W,181 mTropical rainforest This study7 Brazil ca. Rio Uaupés, Taracua, Amazonas 1964 00.0508N, 68.5178W,98 mTropical rainforest de Andrade andBaroni Urbani(1999)8† Brazil Rio Grande Reservoir, Piraı́, Rio deJaneiro1966 22.9168S, 43.4668W,810 mTropical rainforest de Andrade andBaroni Urbani(1999)9† Colombia ca. Bellavista city and Tiquie River,Dept. of Vaupésunkn. 00.1508N, 70.0178W,182 mTropical rainforest de Andrade andBaroni Urbani(1999)10 Panama Barro Colorado Island, GigantePeninsula, and Camino de Cruces,Canal Zone2005–6,201209.1558N, 79.8478W,113 mTropical rainforest Yanoviak et al. (2008)and Yanoviakunpub. obs.11 Peru Los Amigos (CICRA) field station 100km W of Puerto Maldonado2007 12.5778S, 70.0708W,343 mTropical rainforest Yanoviak et al. (2008)* Coordinates and elevation are approximate for records with unknown collection dates (unkn.) or collection dates prior to 2005.† Deposited in the Museu de Zoologia da Universidade de São Paulo, Brazil (MZSP).‡ Deposited in the Setor de Entomologia da Coleção Zoológica da Universidade Federal de Mato Grosso, Brazil (CEMT).156 THE JOURNAL OF PARASITOLOGY, VOL. 99, NO. 1, FEBRUARY 2013TELLA, J. L., G. BLANCO, M. G. FORERO, A. GAJÓN, J. A. DONÁZAR, AND F.HIRALDO. 1999. Habitat, world geographic range, and embryonicdevelopment of hosts explain the prevalence of avian hematozoa atsmall spatial and phylogenetic scales. Proceedings of the NationalAcademy of Sciences USA 6: 1785–1789.TRIPET, F., P. CHRISTE, AND A. P. MØLLER. 2002. The importance of hostspatial distribution for parasite specialization and speciation: Acomparative study of bird fleas (Siphonaptera: Ceratophyllidae).Journal of Animal Ecology 71: 735–748.VERBLE, R. M., A. D. MEYER, M. G. KLEVE, AND S. P. YANOVIAK. 2012.Exoskeletal thinning in Cephalotes atratus ants (Hymenoptera:Formicidae) parasitized by Myrmeconema neotropicum (Nematoda:Tetradonematidae). Journal of Parasitology 98: 226–228.WEBER, N. A. 1957. The nest of an anomalous colony of the arboreal antCephalotes atratus. Psyche 64: 60–69.YANOVIAK, S. P. 2010. ‘Berry’ ants: An eye-popping symbiosis from therainforest canopy. In Ant ecology, L. Lach, C. L. Parr, and K.Abbott (eds.). Oxford University Press, Oxford, U.K., p. 98–99.———, R. DUDLEY, AND M. KASPARI. 2005. Directed aerial descent incanopy ants. Nature 433: 624–626.———, M. KASPARI, R. DUDLEY, AND G. POINAR, JR. 2008. Parasite-induced fruit mimicry in a tropical canopy ant. American Naturalist171: 536–544.RESEARCH NOTES 157

The Geographic Distribution of Parasite-Induced Fruit Mimicry in Cephalotes atratus (Formicidae: Myrmicinae)

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The Geographic Distribution of Parasite-Induced Fruit Mimicry in Cephalotes atratus (Formicidae: Myrmicinae)

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