Tales of urban conservation: Eumaeus butterfliesand their threatened cycad hostplants

Lorena Ramírez-Restrepo1& Sandy Koi2 & Ian MacGregor-Fors1

# Springer Science+Business Media New York 2016

Abstract Urbanization has caused the local extinction ofseveral butterfly species around the world, while othershave managed to thrive in urban areas. Butterflies of thegenus Eumaeus are among the most striking and colorfullycaenid butterflies in the Americas, but their neurotoxichostplants, cycads, are a highly threatened plant group.The main threats for cycads are the loss and modificationof their habitats and their removal for ornamental pur-poses, which in addition to their slow growth rate, makethem highly vulnerable. Ornamental cycads are takenfrom natural habitats to urban areas, where they areplaying an important role for Eumaeus reproduction. Wehere report two cases in which two Eumaeus species (E.childrenae, E. atala) are following and utilizing ornamen-tal cycads to reproduce in urban areas, showing how sig-nificant urban areas can be, ecologically speaking. Asidefrom having enormous potential as flagship species forconservation in urban areas, these butterfly and plant spe-cies, and their interactions, shed encouraging light on theidea of putting reconciliation ecology ideas into action.

Keywords Cycads . Hostplants . Urban ecology .

Lycaenidae . Eumaeus childrenae . Eumaeus atala

Introduction

Modern urban practices and the sprawling of cities have beenassociated with the four major components of global change(i.e., land-use change, biological invasions, climate change,biogeochemical cycle shifts; Vitousek et al. 1997; Grimmet al. 2008), setting urbanization as a major threat to biodiver-sity (Czech and Krausman 1997; Güneralp and Seto 2013). Ascities continue to expand and establish, it becomes urgent tounderstand them and their effects on biodiversity (New andSands 2002; Aronson et al. 2014).

Urban systems are frequently considered inhospitable forbiodiversity (Davis and Glick 1978; McKinney 2002); yet,because the effects of urbanization on wildlife communitiesare intense and extend way beyond its limits (McDonnell andMacGregor-Fors 2016), urban ecologists have made patentthe need to consider biological conservation within urbanareas (McKinney 2002; Kowarik 2011). Some reasons behindthis idea range from the direct ecological benefit (most peoplecurrently live in urban areas; Grimm et al. 2008), to restoringthe human–nature relationship and the impact of urban areasoutside their boundaries, making urban conservation a matterof conservation of nature elsewhere (Sanderson andHuron 2011).

Among the most charismatic and well-studied animalgroups in urban areas, birds and butterflies head the list(McKinney 2008; Ramírez-Restrepo and MacGregor-Fors2016). Particularly for butterflies, urbanization has causedthe local extinction of several species (Tilden 1956; Minno2010). In Rome (Italy), 27 butterfly species disappeared be-tween 1900 and 1999, due to urban sprawl and habitat loss(Fattorini 2011). Also, urban sprawl caused the extinction ofthe endemic Xerces Blue butterfly (Glaucopsyche xerces) inthe San Francisco Bay area, mainly due to the loss of itshostplant (Tilden 1956). Yet, as recorded for other wildlife

* Ian MacGregor-Forsian.macgregor@inecol.mx

1 Red de Ambiente y Sustentabilidad, Instituto de Ecología, A.C.Carretera antigua a Coatepec 351, El Haya, Xalapa,91070 Veracruz, Mexico

2 McGuire Center for Lepidoptera and Biodiversity, 3215 Hill Road,Gainesville, FL 32611, USA

Urban EcosystDOI 10.1007/s11252-016-0599-0

groups, some butterfly species have been reported to thrive inurban areas (Smith 2000; Koi 2013; Koi and Daniels 2015).Although the study of urban butterflies is on the rise (New andSands 2002; Ramírez-Restrepo and MacGregor-Fors 2016),there are important gaps in our understanding of the responseof butterflies to urbanization (Ramírez-Restrepo and Halffter2013; Pauchard et al. 2006). Additionally, few publicationsprovide evidence of butterfly species that actually breed andthrive in urban habitats (Graves and Shapiro 2003; Koi 2013;Koi and Daniels 2015).

As part of two independent urban ecology studies, one car-ried out in Xalapa (Veracruz, southeastern Mexico), and anoth-er one in Southeast Florida (United States), we recorded twobutterfly species of the genus Eumaeus with conservation con-cerns using ornamental cycads for breeding. In Xalapa, a small-to-medium sized green neotropical city (~600,000 inhabitants;19°29′–19°36′ N, 96°51′–96° 58′ W; 1120–1720 m asl;Castillo-Campos 1991; Williams-Linera et al. 2002; INEGI2011; Lemoine 2012), we recorded the Great Cycadian(Eumaeus childrenae (G. Gray 1832)), recently included in aregional Red List (Hernández-Baz and Rodríguez-Vargas2014), during citywide surveys in 2012 and 2013 (seeRamírez-Restrepo et al. 2015 for survey details). Afterwards,we surveyed in other greenspaces of Xalapa in which we knowthere are ornamental cycads (i.e., Botanical Garden “FranciscoJavier Clavijero”, Library Services and Information Unit(USBI), Universidad Veracruzana). We sighted four colonies(i.e., eggs, larvae and/or pupal stages) of E. childrenae inXalapa associated with three ornamental cycads (i.e., Dioonedule, Ceratozamia chimalapensis, C. mexicana) (Fig. 1).

In Southeast Florida, we have worked with the Atala(Eumaeus atala (Poey 1832)), considered extinct in theUnited States during the 1950s due to habitat and hostplant loss.More than 300 ephemeral colonies of the Atala butterfly havebeen documented in the Miami-Dade, Broward, and PalmBeach tri-county area (~6 million inhabitants by 2015; USCensus Bureau 2016a,b,c) since 2001 (http://e-atala.blogspot.mx/; Fig. 2). Most of the existing colonies occur in home

gardens. Self-established urban colonies have been documentedas occurring in the median strips of four-lane highways (Davie,Broward Co.; Boca Raton, Palm Beach Co.), along two-lanestreets (Pompano, Broward Co.), parking lots of derelict build-ings (Delray Beach, Broward Co.), parking lots of busy retailstores (Broward and Palm Beach counties), city halls (Browardand Palm Beach counties), coastal parks (Riviera Beach, andHollywood Beach, Broward Co.), parks and nature centers (tri-county) and many of the local nurseries that grow the nativecycad hostplant coontie (tri-county). In botanical gardens, theAtala butterfly has been found to use nearly forty cycad species(i.e., Fairchild Tropical Botanic Garden and MontgomeryBotanical Center, both in Miami-Dade County; Hammer 1996;Koi 2013). At all sampling locations, adults and all immaturestages of the Atala butterfly were recorded.

Our observations show that the presence and abundance ofa fundamental component for two butterfly species(E. childrenae, E. atala), their hostplants (cycads), determinestheir existence and numbers in two urban areas. Aside fromthe baggage of knowledge regarding the negative effects ofurbanization on butterflies (Ramírez-Restrepo andMacGregor-Fors 2016), there are a few published examplesof butterflies thriving in urban areas due to the presence andabundance of their hostplants (Fattorini 2011; Ruszczyk 1986;Smith 2000; Shapiro 2002; Koi 2013). For example, in PortoAlegre (Brazil), one of the least common papilionids in theperipheral areas of the city has higher abundances inside thecity (Ruszczyk 1986). Also, in Davis (CA, USA) 13 species ofbutterflies have shown remarkable ecological plasticity,shifting to alternative hosting and feeding sources in urbanareas (Shapiro 2002).

It is noteworthy that both Eumaeus species succeed inMexico and Florida under different circumstances. In Xalapa,there has been no intentional management seeking to protect ornurture the Great Cycadian butterfly; however, the species istaking advantage of the presence of cycads in private and pub-lic greenspaces. In Southeast Florida, although some city andcounty officials use pesticides to control the herbivory of theAtala butterfly on ornamental cycads, or remove the cycads

Fig. 1 Great Cycadian butterflies (Eumaeus childrenae (G. Gray, 1832))recorded in Xalapa. Left: larvae feeding in a cycad at downtown Xalapa.Right: adult laying eggs in a cycad

Fig. 2 Atala (Eumaeus atala (Poey, 1832)) recorded in SoutheastFlorida. Left: larvae feeding in a cycad Right: adult on a cycad at NovaSoutheastern University

Urban Ecosyst

altogether, this species has become a much sought-after butter-fly, even in botanical gardens. In fact, the Atala butterfly is apopular attraction in botanical gardens and, because of its strik-ing beauty, acts as a charismatic species (Koi 2013).

Our observations demonstrate that some species that wouldoften avoid urban areas, can reproduce within cities if funda-mental requirements are offered and managed appropriately.In our case, both species are highly charismatic and couldhave enormous potential as flagship species for conservationand to root educational programs, and consequently generateawareness of the importance of urban biodiversity in Xalapaand Southeast Florida. This does not only apply to these but-terfly species, but to all wildlife species that could dwell andsucceed in properly managed and planned habitats within thecomplex environmental matrices that urbanization generates.However, actions related to management in urban areas oughtto be carefully analyzed, seeking win-win scenarios(Rosenzweig 2003). In the case of the Great Cycadian inXalapa, for example, the presence of cycads in the city is theresult of poaching from natural areas or the introduction ofexotic species. Due to the effects that exotic species can have(Vitousek et al. 1997), we suggest managing the process withsustainable practices using native plant species. Finally, ifour goal is to set a balance between the quality of humanlife and our effects on biodiversity, following reconciliationecology approaches (Rosenzweig 2003), we need to consid-er human-modified systems into our biological conservationplans.

Acknowledgments We are most grateful to Keith R. Willmott andMadhusudan Katti for their comments and suggestions to a previousversion of this work. Andrew Vovides provided valuable informationabout the cycads of Xalapa. SK thanks the dedicated volunteers who helpmonitor the Atala butterfly colonies throughout southeast Florida. LR-Racknowledges the scholarship and financial support provided by theNational Council of Science and Technology (CONACYT 213179/244461, Convocatoria 290649), COLCIENCIAS (Convocatoria 568-2012), and the Doctoral Program of INECOL.

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