Journal of the Torrey Botanical Society 131(3), 2004, pp. 252±256

Presence of aposematic (warning) coloration in vascular plants of southeastern Ohio1 Darrin L. Rubino2 and Brian C. McCarthy3 Department of Environmental and Plant Biology, Ohio University, Athens, OH 45701

RUBINO,D.L.AND B. C. MCCARTHY (Department of Environmental and Plant Biology, Ohio University, Athens, OH 45701). Presence of aposematic (warning) coloration in vascular plants of southeastern Ohio. J. Torrey Bot. Soc. 131: 252±256. 2004.ÐAposematic coloration, use of conspicuous colors to advertise unpleasant qualities to potential predators, is well documented in the animal kingdom. However, similar use of warning coloration in plants to advertise physical armaments (spines, thorns, or prickles) has been, until recently, unre- ported. A preliminary survey of physically armed plants in southeastern Ohio (USA) revealed a high incidence of aposematic colorationÐthe presence of physical armaments colored differently than the structure on which they are borne. Furthermore, aposematic coloration was found in a wide variety of taxonomically diverse vascular plants. Future research into the possible role of aposematic coloration in vascular plants could greatly expand our knowledge of plant/herbivore interactions. Key words: aposematic coloration, warning coloration, southeastern Ohio, thorn, prickle, spine, herbivory.

Aposematic coloration (conspicuous adver- physical armaments are commonly thought to tisement of a prey's unpleasant qualities) or have evolved as a defense against herbivory; warning coloration is found in a wide array of however, other uses (cooling and climbing ap- animals (e.g., Cott 1957). Although given much paratuses) have also been proposed (Grubb consideration in the animal literature, little work 1992). Physical armaments of plants are often has been performed regarding this phenomenon categorized into three types: thornsÐmodi®ed in plants (Lev-Yadun 2001). Plant use of color branches arising in axils of leaves; spinesÐhard for pollination and seed dispersal has received and pointy modi®ed leaves; pricklesÐsharp out- considerable attention, but the use of color to growths from the cortex and epidermis (Raven advertise physical armaments in plants has only et al. 1999). Due to the proposed similarity in recently been proposed (Lev-Yadun 2001, function among thorns, spines, and prickles, we 2003a, 2003b; Lev-Yadun and Inbar 2002; Lev- will hereafter generically refer to all plants bear- Yadun et al. 2002). Prey use of color to advertise ing them as armed. unpro®tability to predators is considered advan- The main objective of this investigation was tageous because predators will learn to avoid a to document the occurrence of aposematic col- certain color or color pattern due to its associa- oration in the native and naturalized vascular tion with unpleasant consequences (Cott 1957). ¯ora of southeastern Ohio (USA). Additionally, Plants using aposematic coloration to advertise we wanted to gain a rudimentary idea regarding physical armaments (either colored armaments the commonality of this phenomenon among or highly conspicuous color patterns on armed various taxonomic groups in the region. We plant parts) may be protected from future bouts chose to perform this preliminary study in of herbivory if herbivores associate color or a southeastern Ohio due to the availability of tax- color pattern with unpleasantness (Lev-Yadun onomic treatments and ¯oras for the region and 2001; Lev-Yadun 2003b). our familiarity with the local ¯ora. Due to their ability to wound herbivores, Methods. To identify putative aposematic 1 We would like to thank S. Lev-Yadun for encour- plants of southeastern Ohio, we ®rst examined agement and ®eld assistance, D. Swanson of the Wa- taxonomic keys and species distribution lists terloo Wildlife Research Station, Ohio Department of provided by Braun (1961), Cusick and Silber- Natural Resources, for providing logistical support, and B. Kirchoff, A. BuÂrquez, and J. Mickle for com- horn (1977), Fisher (1988), Gleason and Cron- ments that greatly improved the manuscript. quist (1991), and Cooperrider (1995) to identify 2 Current address: Biology Department, Hanover armed taxa of the region. Once a preliminary College, Hanover, IN 47243. listing of armed plants was created, we per- 3 Corresponding author: E-mail: mccarthy@ohio. edu. formed ®eld studies to locate these plants in Received for publication February 20, 2002, and in Athens County, Ohio. If we were unable to ®nd revised form April 1, 2004. the plants in the ®eld, we studied herbarium

252 2004] RUBINO AND MCCARTHY: APOSEMATIC COLORATION IN PLANTS 253

Table 1. Vascular plant species of southeastern Ohio (USA) observed to exhibit aposematic coloration.

CLASS:LILIOPSIDA Agavaceae CLASS:MAGNOLIOPSIDA (cont) Yucca ®lamentosa L. Fabaceae Smilacaceae Robinia pseudoacacia L.* Smilax glauca Walter Grossulariaceae S. hispida Muhl. Ribes cynosbati L. S. rotundifolia L. R. rotundifolium Michx. CLASS:MAGNOLIOPSIDA Malvaceae Amaranthaceae Sida spinosa L. Amaranthus spinosus L. Moraceae Apiaceae Maclura pomifea (Raf.) C.K. Schneider* Eryngium yuccifolium Michx. Polygonaceae Aquifoliaceae Polygonum arifolium L. Ilex opaca Aiton P. sagittatum L. Araliaceae Rosaceae Aralia spinosa L. Crataegus L.* Rosa carolina L. Asteraceae R. multi¯ora Thunb. Carduus nutans L. R. palustris Marshall Cirsium altissimum (L.) Sprengel R. rugosa Thunb. C. arvense (L.) Scop. R. setigera Michx. C. discolor (Muhl.) Sprengel R. virginiana Miller C. vulgare (Savi) Tenore. Rubus allegheniensis T. C. Porter Onopordum acanthium L. R. argutus Link Silybum marianum (L.) Gaertner R. enslenii Tratt. Sonchus arvensis L. R. ¯agellaris Willd. S. asper (L) Hill R. hispidus L. S. oleraceus L. R. laciniatus Willd. Berberidaceae R. occidentalis L. Berbis thunbergii DC R. pensilvanicus Poiret Cactaceae R. phoenicolasius Maxim. Opuntia humifusa (Raf.) Raf. Rutaceae Caesalpiniaceae Zanthoxylum americanum Miller Gleditsia triacanthos L. Solanaceae Dipsacaceae Solanum carolinense L. Dipsacus laciniatus L. S. rostratum Dunal D. sylvestris Hudson * Not all specimens studied exhibited aposematism. specimens deposited in the Bartley Herbarium tatsÐupland and lowland hardwood forests, (BHO) of Ohio University (Athens, OH). Since pine plantations, riparian areas, wetlands, regen- color changes in plant tissues may occur during erating clear-cuts, old-®elds, and grassy mead- drying and storage, we limited our study to only ows (Small and McCarthy 2001). recently collected and well-preserved material. We de®ned aposematic plants as those with Results and Discussion. Aposematic colora- thorns, spines, or prickles which are colored so tion was observed in 49 plants from the region that they contrast (easily detectable difference in (total of both the preliminary ®eld and herbari- color or hue) with the vegetative structure(s) um study and the ¯ora study). Aposematism was (leaf, stem, twig, rachis, petiole) on which they observed in a wide variety of taxonomically di- are borne. Taxonomy follows Gleason and Cron- verse vascular plants (19 families, 25 genera; quist (1991). Table 1). Aposematic plants exhibited yellow, The ®eld and herbarium study permitted us to yellow-green, red, tan, brown, maroon, black, or document aposematism in the native and natu- white thorns, spines, or prickles. Aposematic ralized vascular ¯ora of the region. However, it plants varied in the number of colors present on did not enable us to provide any estimates re- their armaments. For example, Polygonum sag- garding the commonality of this phenomenon in ittatum L. exhibited only one color (white) while the region. Subsequently, to determine the pro- plants such as Smilax rotundifolia L. and Rubus portion of armed, unarmed, aposematic, and pensilvanicus Poiret exhibited three different non-aposematic plants present, we selected and colors per prickle (Fig. 1). Additionally, plants studied a ¯ora prepared from a local 505 ha re- such as Rosa multi¯ora Thunb. exhibited differ- search area that contains several diverse habi- ent colors of prickles both among individual 254 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 131

FIG 1. Aposematic vascular plants of southeastern Ohio. (A) Prickles of Rosa carolina L. (B) Multi-colored prickle of Smilax rotundifolia (Top to bottom: green, yellow, brown). (C) White and (D) black prickles of Rosa multi¯ora. (E) Highly visible, multi-colored prickles of Rubus pensilvanicus (arrows). Scale bar ϭ 0.5 cm throughout. 2004] RUBINO AND MCCARTHY: APOSEMATIC COLORATION IN PLANTS 255 plants and on different stem segments of an in- physical armaments but are not sharp). See Lev- dividual plant (Fig. 1). Similar colors and color Yadun (2001) and Lev-Yadun et al. (2002) for a patterns were reported by Lev-Yadun (2001) in further discussion of alternative hypotheses re- his analysis of Old and New World Cactaceae garding coloration patterns. Juss., Agave L., Aloe L., and Euphorbia L. Additional work needs to be done to further Quanti®cation of the number of plants exhibiting elucidate the relationships between conspicuous single and multiple armament color and different physical defenses (or the lack thereof) with her- colors throughout an individual plant would be bivory, plant life history, and ecological require- ideal. However, armament color varies during ments and pressures (Lev-Yadun 2001; Lev-Ya- development, and quanti®cation of different dun and Inbar 2002; Lev-Yadun et al. 2002). For hues of a single color is not feasible or practical. example, could the frequency of aposematic col- Of the 655 species of plants reported in a lo- oration in taller-statured taxa be in¯uenced by cal ¯ora by Small and McCarthy (2001), 25 now extinct arboreal herbivores in temperate re- (3.8%) were armed. Of these armed plants 24 gions of North America (sensu Janzen and Mar- were aposematic (Pyrus coronaria L. was armed tin 1982)? Also, many of the aposematic taxa but not aposematic). Thus, although aposema- identi®ed from southeastern Ohio often occupy tism is common (96% of armed plants), it is not edges or old-®eld habitats. Could the high de- present in all physically armed plants even in gree of aposematism in these taxa be related to closely related taxa (S. Lev-Yadun, pers. their conspicuousness in these habitats? Future comm.). Additionally, not all taxa that we scored experimental and observational studies address- as aposematic consistently exhibited aposema- ing aposematism could greatly expand our tism; individual Maclura pomifera (Raf.) C. K. knowledge of this phenomenon in higher plants Schneider, Crataegus L., and Robinia pseudoa- and interactions between plants and herbivores cacia L. plants exhibited aposematic and non- (Lev-Yadun 2001, 2003a, 2003b; Lev-Yadun aposematic coloration. and Inbar 2002; Lev-Yadun et al. 2002). The total number of aposematic plants re- ported for southeastern Ohio likely represents a Literature Cited minimum. Lack of fresh, reliably-colored her- barium specimens, access to living populations, BRAUN, E. L. 1961. The woody plants of Ohio: trees, and inadequate or lacking descriptions of ar- shrubs, and woody climbers native, naturalized, maments in regional ®eld and taxonomic man- and escaped. Ohio State University Press, Colum- uals did not permit characterization of all armed bus, OH. 362 p. COOPERRIDER, T. S. 1995. The Dicotyledoneae of Ohio, taxa. Additionally, taxonomically troubling taxa Part 2: Linaceae through Campanulaceae. Ohio such as Crataegus makes identi®cation and State University Press, Columbus, OH. 656 p. quanti®cation of aposematic species extremely COTT, H. B. 1957. Adaptive coloration in animals. Me- dif®cult. However, we were successful in ob- thuen and Co. LTD, London, UK. 508 p. serving this potentially important ecological and CUSICK,A.W.,AND G. M. SILBERHORN. 1977. The vas- cular plants of unglaciated Ohio. Bulletin of the evolutionary phenomenon in the native and nat- Ohio Biological Survey. New Series: Vol. 5 No. 4. uralized ¯ora of the region and in determining Ohio Biological Survey, Ohio State University, Co- the extent of aposematism in a local ¯ora. lumbus, OH. 157 p. We agree with Lev-Yadun (2001) that the FISHER, T. R. 1988. The Dicotyledoneae of Ohio, Part presence of colored physical armaments sug- 3: Asteraceae. Ohio State University Press, Colum- bus, OH. 280 p. gests a bene®t to plants so marked. Herbivores GLEASON, H. A., AND A. CRONQUIST. 1991. Manual of may associate the warning colors and patterns vascular plants of northeastern United States and with injury and avoid future attempts of herbiv- adjacent Canada. 2nd ed. The New York Botanical ory. Lev-Yadun (2001) states that the diversity Garden, New York, NY. 910 p. of taxonomic and geographic groups exhibiting GRUBB, P. J. 1992. A positive distrust in simplicityÐ lessons from plant defences and from competition aposematic coloration suggests that such a trait among plants and among animals. J. Ecol. 80: 585± was selected for repeatedly throughout evolu- 610. tionary history. Lev-Yadun (2003a) further JANZEN,D.H.,AND P. S. MARTIN. 1982. Neotropical states that the presence of aposematic coloration anachronisms: the fruits the Gomphotheres ate. Sci- is so widespread that aposematic mimics can ence 215: 19±27. LEV-YADUN, S. 2001. Aposematic (warning) coloration even be found (i.e., plants with brightly colored, associated with thorns in higher plants. J. Theor. elongated, and pointy structures such as buds, Biol. 210: 385±388. fruits, and awn-like leaf projections that mimic LEV-YADUN, S. 2003a. Weapon (thorn) automimicry 256 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 131

and mimicry of aposematic colorful thorns in of plants deserve more research attention. Trends plants. J. Theor. Biol. 224: 183±188. Plant Sci. 7: 59±60. LEV-YADUN, S. 2003b. Why do some thorny plants re- RAVEN, P. H., R. F. EVERT, AND S. E. EICHHORN. 1999. semble green zebras? J. Theor. Biol. 224: 483±489. Biology of plants. 6th ed. W. H. Freeman and Co., LEV-YADUN, S., AND M. INBAR. 2002. Defensive ant, New York, NY. 944p. aphid and caterpillar mimicry in plants? Biol. J. SMALL, C. J., AND B. C. MCCARTHY. 1991. Vascular Linn. Soc. 77: 393±398. ¯ora of the Waterloo Wildlife Research Station, LEV-YADUN, S., M. INBAR,I.IZHAKI,G.NEEÁ MAN, AND Athens County, Ohio. Castanea 66: 363±382. A. DAFNI. 2002. Colour patterns in vegetative parts