(Lepidoptera: Pieridae) Butterflies Are Palatable to Avian Predators

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(Lepidoptera: Pieridae) Butterflies Are Palatable to Avian Predators insects Article Evaluating an Alleged Mimic of the Monarch Butterfly: Neophasia (Lepidoptera: Pieridae) Butterflies are Palatable to Avian Predators Dale A. Halbritter 1,2,* , Johnalyn M. Gordon 3, Kandy L. Keacher 4, Michael L. Avery 4,5 and Jaret C. Daniels 2,6 1 USDA-ARS Invasive Plant Research Laboratory, 3225 College Ave, Fort Lauderdale, FL 33314, USA 2 Entomology and Nematology Department, University of Florida, 1881 Natural Area Dr, Steinmetz Hall, Gainesville, FL 32611, USA; jdaniels@flmnh.ufl.edu 3 Fort Lauderdale Research and Education Center, University of Florida, 3205 College Ave, Davie, FL 33314, USA; johnalynmgordon@ufl.edu 4 Florida Field Station, USDA-APHIS National Wildlife Research Center, 2820 E University Ave, Gainesville, FL 32641, USA; [email protected] (K.L.K.); [email protected] (M.L.A.) 5 2906 NW 14th Pl., Gainesville, FL 32605, USA 6 McGuire Center for Lepidoptera and Biodiversity, Florida Museum of Natural History, 3215 Hull Road, Gainesville, FL 32611, USA * Correspondence: dhalb001@ufl.edu or [email protected]; Tel.: +1-661-406-8932 Received: 28 September 2018; Accepted: 22 October 2018; Published: 29 October 2018 Abstract: Some taxa have adopted the strategy of mimicry to protect themselves from predation. Butterflies are some of the best representatives used to study mimicry, with the monarch butterfly, Danaus plexippus (Lepidoptera: Nymphalidae) a well-known model. We are the first to empirically investigate a proposed mimic of the monarch butterfly: Neophasia terlooii, the Mexican pine white butterfly (Lepidoptera: Pieridae). We used captive birds to assess the palatability of N. terlooii and its sister species, N. menapia, to determine the mimicry category that would best fit this system. The birds readily consumed both species of Neophasia and a palatable control species but refused to eat unpalatable butterflies such as D. plexippus and Heliconius charithonia (Lepidoptera: Nymphalidae). Given some evidence for mild unpalatability of Neophasia, we discuss the results considering modifications to classic mimicry theory, i.e., a palatability-based continuum between Batesian and Müllerian mimicry, with a quasi-Batesian intermediate. Understanding the ecology of Neophasia in light of contemporary and historical sympatry with D. plexippus could shed light on the biogeography of, evolution of, and predation pressure on the monarch butterfly, whose migration event has become a conservation priority. Keywords: bird; butterfly; Danaus plexippus; mimicry; Neophasia; palatability; predation 1. Introduction Mimicry within animals is evident when one species to some degree matches another in visual appearance, chemical profile, and/or behavior. Butterflies have served as excellent models to investigate mechanisms of mimicry, with emphasis on the Neotropical genus Heliconius (Lepidoptera: Nymphalidae) [1–7], sex-limited mimicry within Papilio spp. (Lepidoptera: Papilionidae) [8–11], and the well-known Limenitis-Danaus (Lepidoptera: Nymphalidae) system [12–15]. Mimics can evade predation because they emulate a toxic, distasteful, or dangerous model that predators learn to identify and avoid. In Batesian mimicry, a mimic emulates another toxic or distasteful species, but the mimic is not toxic or distasteful. The Batesian mimic is considered deleterious to its model, especially if the Insects 2018, 9, 150; doi:10.3390/insects9040150 www.mdpi.com/journal/insects Insects 2018, 9, x FOR PEER REVIEW 2 of 10 Insects 2018, 9, 150 2 of 9 deleterious to its model, especially if the mimic is comparably abundant [16–19]. In Müllerian mimicmimicry, is comparably a toxic or distasteful abundant species [16–19 visually]. In Müllerian mimics mimicry, another toxic a toxic or ordistasteful distasteful species. species Müllerian visually mimicsmimicry another complexes toxic experience or distasteful less species. predation Müllerian pressure mimicry because complexes it is easier experience for predators less to predation learn to pressureavoid one because common it is pattern. easier for Mimicry predators may to learnnot be to confined avoid one to commona strict dichotomy, pattern. Mimicry as the maylevel not of beunpalatability confined to amay strict vary dichotomy, in some asprey the levelspecies of unpalatabilityand different predator may vary species in some may prey vary species in their and differentperception predator of unpalatability species may, adding vary in complexity their perception to the ofspectrum unpalatability, between adding Batesian complexity and Müllerian to the spectrummimicry [20] between. However, Batesian there and is Müllerianoften a fine mimicry threshold [20 ].within However, the palatability there is often spectrum a fine thresholdat which withinpredators the reject palatability their prey spectrum [17], suggesting at which predators that classical reject Batesian their prey and [Müllerian17], suggesting mimicry that would classical be Batesianmost common and Müllerian [19]. Additionally, mimicry would the spectrum be most commonis likely [driven19]. Additionally, by variations the in spectrum the reactions is likely of drivendifferent by predator variations species in the when reactions they of encounter different predatorthe mimic species [17]. when they encounter the mimic [17]. OurOur studystudy isis thethe firstfirst to empirically examineexamine thethe naturenature ofof anan alleged casecase ofof mimicry inin Neophasia (Lepidoptera:(Lepidoptera: Pieridae), an unusualunusual genusgenus ofof NorthNorth AmericanAmerican butterflies.butterflies. Female NeophasiaNeophasia terlooii, thethe MexicanMexican pinepine whitewhite butterfly,butterfly, areare orangeorange withwith blackblack markings resembling the monarch butterfly, butterfly, DanausDanaus plexippusplexippus (Figure(Figure1 ).1). TheThe suggestionsuggestion thatthat femalefemale N. terlooii mimic D. plexippusplexippus waswas firstfirst publishedpublished by Poulton [21] [21] and and has has yet yet to to be be empirically empirically investigated. investigated. The The black black markings markings on on male male N. N.terlooii terlooii resembleresemble those those on on female female N.N. terlooii terlooii, but, but the the background background color color is is white white in in males males (Figure (Figure 11).). Currently,Currently, the only other other recognized recognized species species of of NeophasiaNeophasia is N.is N.menapia menapia, the, thepine pine white white butterfly, butterfly, and andboth both males males and andfemales females are arewhite white with with black black markings, markings, but buttheir their black black markings markings are are like like those those on onN. N.terlooii terlooii (Figure(Figure 1).1 ).NeophasiaNeophasia menapia menapia hashas one one summer summer brood brood and and is is found found from from southwestern BritishBritish ColumbiaColumbia toto Guadalupe Guadalupe Mountains Mountains National National Park Park in extreme in extreme southwest southwest Texas Texas [22,23 ].[22,23].Neophasia Neophasia terlooii hasterlooii a small has summera small summer brood and brood a larger and fall a larger brood andfall bro is foundod and from is thefound sky from islands the of sky southeastern islands of Arizonasoutheastern to central Arizona México to central [22,24 ].México As larvae, [22,24].Neophasia As larvae,spp. Neophasia feed on conifers spp. feed and on we conifers considered and thewe possibilityconsidered that the larvaepossibility sequester that larvae unpalatable sequester host unpalatable plant compounds, host plant retaining compounds, them through retaining the adultthem stagethrough and the potentially adult stage rendering and potentially the adults rendering unpalatable the adults to predators. unpalatable to predators. Figure 1. A visual comparison between allegedly mimetic Neophasia spp. (Lepidoptera: Pieridae) and theirFigure proposed 1. A visual model, comparisonDanaus plexippusbetween (Lepidoptera:allegedly mimetic Nymphalidae). Neophasia spp. Based (Lepidoptera: on the visible Pieridae) spectrum, and femaletheir proposedN. terlooii model,are the Danaus most likely plexippus mimics (Lepidoptera: of D. plexippus Nymphalidae). Photographs. Based by author on the Dale visible A. Halbritter.spectrum, female N. terlooii are the most likely mimics of D. plexippus. Photographs by author Dale A. Halbritter. Under the assumption that Neophasia spp. mimic D. plexippus, our objective was to determine whereUnderNeophasia the assumptionspp. reside that on theNeophasia Batesian-Müllerian spp. mimic D. mimicry plexippus spectrum., our objective In a was manner to determine like that employedwhere Neophasia by Long spp. et al. reside [25], weon usedthe Batesian caged birds-Mü asllerian representatives mimicry spectrum. of visual predatorsIn a manner to determine like that theemployed butterflies’ by Long palatability. et al. [25], w Jonese used [26 caged,27] wasbirds the as representatives first to use wild of visual birds predators to assess to palatability determine andthe butterflies’ aposematism palatability in insects,. Jones and Brower[26,27] [was8,12 ,the13] first was to the use first wild to empirically birds to assess investigate palatability mimicry and mechanismsaposematism in in North insects, American and Brower butterflies [8,12,13] using was caged the birds. first Into theempirically latter studies, investigate birds learned mimicry to recognizemechanisms and in avoid North consuming American toxicbutterflies butterflies using and caged subsequently birds. In
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