Oecologia DOI 10.1007/s00442-006-0496-y
PL AN T AN IM AL IN TE R ACT IO N S
A Weld test of the directed deterrence hypothesis in two species of wild chili Douglas J. Levey · Joshua J. Tewksbury · Martin L. Cipollini · Tomás A. Carlo
Received: 15 December 2005 / Accepted: 27 June 2006 © Springer-Verlag 2006
Abstract The directed deterrence hypothesis posits that secondary metabolites in ripe fruit function to deter fruit consumption by vertebrates that do not disperse seeds, while not impacting consumption by those that do. We tested this hypothesis in two species of wild chilies (Capsicum spp.). Both produce fruits that contain capsaicinoids, the compounds responsible for the pungency of chilies. Previous work suggests seeddispersing birds but not seed-destroying rodents consume chili fruits, presumably because rodents are deterred by capsaicin. However, fruit removal from chili plants by rodents and other mammals has not been previously explored. Because laboratory rodents can develop a preference for capsaicin, it is quite possible that wild rodents are natural consumers of chili fruits. We monitored the fate of 125 marked fruits of Capsicum chacoense and 291 fruits of Capsicum annuum. For both species, essentially all fruit removal occurred during the day, when rodents are inactive. Video monitoring revealed fruit removal only by birds, mostly by species known to disperse chili seeds in viable condition. Furthermore, these species are from Communicated by Phyllis Coley D. J. Levey (&) Department of Zoology, University of Florida, 118525, Gainesville, FL 32611-8525, USA e-mail:
[email protected] J. J. Tewksbury · T. A. Carlo Department of Biology, University of Washington, Seattle, WA 98115, USA M. L. Cipollini Department of Biology, Berry College, 430, Mount Berry, GA 30149-0439, USA
taxonomic groups that tend to specialize on lipid-rich fruits. Both species of chili produce fruits that are unusually high in lipids (35% in C. chacoense, 24% in C. annuum). These results support the directed deterrence hypothesis and suggest that fruiting plants distinguish between seed predators and seed dispersers by producing fruits that repel the former and attract the latter. Keywords Birds · Capsaicin · Chili · Directed deterrence · Fruit
Introduction Many of the most intricate and fundamental interactions between plants and their consumers are mediated by secondary metabolites, compounds with no known physiological role in the plants that produce them (Bernays and Chapman 1994; Coley and Barone 1996; Adler et al. 2001). In seeds, leaves, and unripe fruit, the primary function of secondary metabolites is to deter consumption by granivores and herbivores. In ripe fruits, their function is more complex because fruit consumption can be either beneWcial or detrimental to plants, depending on whether the consumer disperses or destroys seeds. Thus, fruiting plants face the evolutionary challenge of packaging their seeds in pulp with compounds that simultaneously attract seed-dispersing frugivores and deter seed-destroying frugivores (Janzen 1977; Herrera 1982; Cipollini 2000). The directed deterrence hypothesis (Cipollini and Levey 1997b) posits that some plant species have met this challenge through the production of secondary metabolites that are inhibitory toward organisms that are likely to
123
Oecologia
destroy seeds, but relatively non-toxic and non-deterrent to seed-dispersing vertebrates. The directed deterrence hypothesis remains largely untested. Among studies that have examined responses of both seed predators and seed dispersers to isolated fruit secondary metabolites (not extracts), most have concluded that fruit metabolites deter all consumers, not just seed predators (Cipollini and Levey 1997a, c, 1998; Levey and Cipollini 1998; Cipollini 2000; Izhaki 2002; Tsahar et al. 2002). The only metabolites that so far appear to be selectively toxic to seed predators are capsaicinoids (mostly capsaicin and dihydrocapsaicin), the compounds responsible for pungency in chili fruits (Iwai et al. 1979; Cordell and Araujo 1993). Feeding trails with captive animals have demonstrated that capsaicin is an irritant to rodents and not to birds (Norman et al. 1992; Mason and Clark 1995; Tewksbury et al. 1999; Tewksbury and Nabhan 2001). Furthermore, this diVerence in sensitivity appears general across all birds and mammals, due to taxon-speciWc diVerences in the vanilloid receptors responsible for pain perception (Mason et al. 1991; Jordt and Julius 2002). In the Weld, deterrence of mammals is likely advantageous to chili plants because granivorous rodents are the most common mammals in habitats where chilies occur. Many common species of birds in the same habitat are seed dispersers. Indeed, seed-dispersing birds are well-known consumers of wild chili fruits, whereas nocturnal rodents appear to avoid them (Tewksbury and Nabhan 2001). We suggest that acceptance of the directed deterrence hypothesis for chilies is premature. Records of avian consumption are limited to casual observations, short-term (4-h) trials of chili fruits on plates on the ground, and some video monitoring (Tewksbury et al. 1999; Tewksbury and Nabhan 2001). More problematical, Weld data on mammalian consumption of chili fruits are restricted to 2 nights of trials in which small piles of chilies were placed on the ground (Tewksbury et al. 1999; Tewksbury and Nabhan 2001). Although no removal of chili fruits was detected, fruits were not monitored on plants, where consumers would be most likely to search for fruit. Directed deterrence posits that chemistry is used as a pre-dispersal Wlter, changing the identity of organisms consuming fruits on the plant. Thus, trials conducted with fruit on the ground are not appropriate tests of this hypothesis. Further, because removal of chili fruits is rare and episodic (Tewksbury et al. 1999; Tewksbury and Nabhan 2001), short-term trials will often fail to detect it. Many experiments with laboratory rodents have revealed the irritant properties of capsaicin (Hilker et al. 1967; Rozin et al. 1979; Prescott 1999; Shumake
123
et al. 2000; Simmons et al. 2001), but a deeper exploration of the literature yields at least four reasons to suspect rodents and other mammals may frequently consume chili fruits in the Weld. First, Weld studies on the application of capsaicin to reduce damage to crops and electrical wiring by rodents and other mammals often conclude that capsaicin either has no eVect or an eVect that quickly disappears over time (Swihart and Conover 1991; Andelt et al. 1994; Wagner and Nolte 2000; Bosland 2001; Santilli et al. 2004). Second, laboratory studies show that mammals become desensitized to capsaicin when they are exposed to it in a way that simulates repeated feeding bouts (Green 1989, 1991; Karrer and Bartoshuk 1991; McBurney et al. 1997; Prescott 1999). Third, rodents and primates that are initially repelled by capsaicin can develop a strong preference for it (Rozin et al. 1981; Rozin and Kennel 1983a, b; Galef 1989; Dib 1990; Prescott and Stevenson 1995). Fourth, wild-derived strains of mice are highly variable in their sensitivity to capsaicin (Furuse et al. 2002). The primary purpose of this study was to document the natural consumers of two wild chili species, Capsicum annuum in Arizona (USA) and Capsicum chacoense in Bolivia. We identiWed consumers by conducting censuses of fruits on plants at dawn and dusk and by using video cameras trained on chili plants during the day. The fruit censuses allowed us to monitor a large number of fruit under natural conditions for daytime (bird) and nighttime (mammal) removal. The cameras allowed us to continuously and unobtrusively observe chili fruits and to identify consumers. We also looked for clues about consumer identity by examining fruit traits. C. annuum and C. chacoense fruits are small (5–10 mm), red when ripe, and ovate— all traits that tend to characterize bird-dispersed species (Janson 1983; Debussche and Isenmann 1989; Herrera 2002; Pizo 2002). Their nutrient composition is potentially important because the nutrient content of pulp is often linked to diVerences in disperser assemblages (McKey 1975; Snow 1985; Fuentes 1994; Witmer and Van Soest 1998). In particular, mammals tend to avoid lipid-rich fruits (Martin et al. 1951; Debussche and Isenmann 1989; Jordano 1995; Corlett 1996; Bollen et al. 2004) and at least some taxa of birds tend to specialize on them (McKey 1975; Moermond and Denslow 1985; Snow 1985; Place and Stiles 1992; Fuentes 1994; Witmer 1996; Witmer and Van Soest 1998). In the New World, these avian taxa include Xycatchers (Tyrannidae), thrushes (Turdidae), and mimids (Mimidae) (Loiselle and Blake 1990; Stiles 1993; Witmer 1996; Witmer and Van Soest 1998). In contrast to cultivated species of Capsicum, fruits of C. annuum and C. chacoense feel oily when crushed. If they are indeed lipid-rich, they
Oecologia
would be less likely consumed by mammals and more likely consumed by Xycatchers, thrushes, and mimids.
Materials and methods Study sites In Arizona, we worked at the Tumucacori Chili Reserve, Santa Cruz County (31°33⬘N, 111°04⬘W). Vegetation is predominantly semi-desert grassland and mesquite woodland (Brown 1982). The population of approximately 500 C. annuum var. glabriusculum plants at this site represents the northernmost extent of Capsicum. Fruiting individuals are 0.5–1.5 m in height and occur disproportionately under the canopies of desert hackberry (Celtis pallida) and netleaf hackberry (Celtis reticulata) (Tewksbury et al. 1999). Crop sizes of ripe fruits are typically small (< 100 fruits) but can range to 1,000. When ripening, chili fruits of both study species pass through a pre-ripe stage during which they are bright orange and diYcult to remove from the peduncle. When ripe, they are bright red and easily removed from the peduncle. Red fruits can persist for more than a month. In Bolivia, we worked at Rancho San Julian, Santa Cruz (19°77⬘S, 62°70⬘W). The vegetation is xeromorphic, with approximately 75 C. chacoense in a forest stand dominated by Schinopsis, Aspidosperma, Ziziphus, and Prosopis. In stature, C. chacoense is similar to C. annuum, but less bushy and with smaller fruit crops. Several species at our site produced fruit concurrently with C. chacoense, including Celtis, Vallesia, Capparis, and Rivina. C. chacoense was not obviously associated with these species. At both sites, we monitored fruit removal at the height of the fruiting season (March and April in Bolivia; September–November in Arizona). In Bolivia, we counted ripe fruits on each of ten plants at dawn and at dusk. Chili fruits are displayed at the end of peduncles that contain bracts. These bracts remain intact when a fruit is plucked, thereby allowing us to verify fruit removal. Because we found no evidence of fruits being removed and then dropped under the parent plant, we assume that all removed fruits were consumed and we use the terms “removed” and “consumed” interchangeably. Further support for this assumption comes from analysis of video tapes (see Results). After each fruit census, we removed all empty bracts. In Bolivia, we monitored from Wve to 14 ripe fruits (average = 9.4; SD = 3.0) on each of ten plants for approximately 8 days (average = 7.7; SD = 1.2). In Arizona, we followed a similar protocol, monitoring from
three to 55 fruits (average = 22.4; SD = 3.4) on each of 13 plants for exactly 11 days. For video monitoring, we positioned high deWnition 8-mm video cameras 2–3 m from chili plants and Wlmed for approximately 12 h/day, including dawn and dusk. We operated six cameras simultaneously on six diVerent plants, often on the same plants that we monitored by fruit counting. Each camera was positioned to record animal activity in all or most of the plant’s crown. In the morning, we determined if any fruit had been removed from a given plant during the previous 24 h. If there had been no fruit removal, we continued Wlming the same plant. If there had been fruit removal, we changed camera location and started to Wlm a new individual. Tapes were reviewed by fast-forwarding until animal activity was seen, at which point we watched in real time. We recorded the species of animal and how many fruits it consumed per foraging bout. We did not review tapes that did not contain at least one incidence of fruit removal. If a fruit was present at dusk 1 day and was not present the following morning, we assumed it had been removed at night, even though it was often possible for birds to have removed fruits between when we departed one day and returned the next. Nutritional analyses C. annuum and C. chacoense fruits were Xash-frozen on dry ice and lyophilized. After removal of seeds, the dried pulp was ground with a mortar and pestle, passed through a no. 40 mesh screen, and stored at ¡20°C. Pulp samples were analyzed for: 1. Total reducing (simple) sugars via methanol extraction, followed by the anthrone assay (Smith 1981), using a 1:1 glucose:fructose standard. 2. Total nonstructural carbohydrates (TNC) via amylase extraction, followed by the anthrone assay (Spiro 1966; Smith 1981), using the same standard. 3. Total lipids via petroleum ether extraction and gravimetric analysis (Williams 1984). 4. Total protein via the Bradford assay (Jones et al. 1989), using a ribulose 1,5-biphosphate oxygenasecarboxylase standard. 5. Ash via residual mass following combustion at 525°C for 24 h. All assays were run in triplicate and were recorded as average percent of dry pulp mass. Fiber was estimated for each sample by subtracting average values for TNC, lipids, proteins, and ash from 100%. Complex carbohydrates (e.g., starches, hemicelluloses, pectins) were estimated by subtracting simple sugars from TNC.
123
Oecologia
Results In Bolivia, 24 marked fruits of C. chacoense were removed during 699 fruit-days (one fruit monitored for 1 day = one fruit-day) and in Arizona, 111 fruits of C. annuum were removed during 3,201 fruit-days. Likewise, video monitoring yielded 125 instances of removal in 1,840 h of taping C. chacoense plants and 45 instances of removal in 362 h of taping C. annuum plants. Removal of marked fruits at night was essentially non-existent for both species. In Bolivia no fruits disappeared between dusk one day and dawn the next day. In Arizona only one of 111 removed fruits disappeared between dusk and dawn. For this fruit, we could not rule out the possibility that a bird visited the plant before we did that day. Alternatively, it could have been dislodged by deer, which were common in the area. Video monitoring revealed that all fruit removal during the day was by birds. Birds almost always immediately swallowed the fruits they removed and the few times they did not, they Xew out of sight carrying the fruit. We never observed a bird reject a fruit, once it had plucked it from the plant. One or two species of birds at each site were responsible for the vast majority of fruit removal (Fig. 1). In Bolivia, the most common consumer was the small-billed elaenia (Elaenia parvirostris), accounting for 49% of total fruits consumed. (Some individuals may have been Elaenia albiceps, which is similar in appearance but rare in the region; Jahn et al. 2002.) Creamy-bellied thrush (Turdus Fig. 1 Fruit consumption of Capsicum annuum and Capsicum chacoense by birds recorded on video tape swallowing fruits. Also shown are study site locations, approximate range boundaries for C. annuum (hatching) and C. chacoense (cross-hatching), and the approximate range of the genus Capsicum (light gray)
123
amaurochalinus) was another common visitor at C. chacoense plants in Bolivia, accounting for 36% of consumed fruits. A total of six additional species, including three Xycatchers, accounted for the remaining 15% of fruit consumption. In Arizona, curve-billed thrashers (Toxostoma curvirostre) were by far the most common consumers of C. annuum (69% of fruits consumed), followed by northern mockingbirds (Mimus polyglottos; 18%; Fig. 1). Blue-gray gnatcatchers (Polioptila caerulea), rock wrens (Salphinctes obsoletus), and white-crowned sparrows (Zonotrichia leucophrys) were rare consumers (4% each). Nutrient content Lipid content of ripe chili fruits was high, averaging 35% of pulp dry mass in C. chacoense and 24% in C. annuum (Table 1). Simple sugars (mostly glucose and fructose) constituted approximately 16% dry mass in C. chacoense and 24% in C. annuum. Protein content was 10% and 12% in C. chacoense and C. annuum, respectively. Fiber was slightly higher in C. chacoense than C. annuum and complex carbohydrates were higher in C. annuum than in C. chacoense.
Discussion Our results provide the Wrst support for the directed deterrence hypothesis in naturally occurring fruits. The prevalence of consumption by birds and absence of
Oecologia Table 1 Nutritional content of Capsicum annuum and Capsicum chacoense fruits from Arizona and Bolivia, respectively. Values are mean percentage dry mass of pulp § 1 SE Constituent
C. annuum
C. chacoensea
Simple sugars Complex carbohydrates Proteinc Lipids Fiberd
24.4 § 0.2 7.7 § 1.1 11.5 § 1.2 23.7 § 0.3 25.1 § 1.8
16.4 § 2.6 0b 9.6 § 1.4 34.8 § 0.2 32.5 § 2.3
a
Values in table are for pungent C. chacoense fruits. Values for non-pungent C. chacoense fruits are: simple sugars = 15.9 § 2.4; complex carbohydrates = 0.9 § 0.2; protein = 9.7 § 3.8; lipids = 28.7 § 0.3; Wber = 36.7 § 1.3 b Trace c Includes free amino acids d Calculated by diVerence. Ash content = 7.6%
consumption by mammals was consistent across two species of Capsicum on diVerent continents and exposed to non-overlapping communities of birds and mammals. Capsaicin may therefore provide a mechanism by which plants can prevent consumption of their seeds by mammalian seed predators without decreasing the probability of consumption by avian seed dispersers. We now address Wve additional conditions that must be met for strong support of the directed deterrence hypothesis. First, birds that consume chili fruits must pass chili seeds in viable condition. Indeed, seeds of C. annuum defecated by their most common consumer in Arizona, curve-billed thrashers, germinate at the same rate (ca. 50%) as control seeds (Tewksbury and Nabhan 2001). In Bolivia, we have fed C. chacoense fruits to captive individuals of the two most common consumers, elaenias and creamy-bellied thrushes. Of seeds defecated by elaenias, 70–80% germinated within 60 days—approximately the same frequency as seeds removed directly from fruits (J. Tewksbury and D. Levey, unpublished data). We did not attempt to germinate seeds defecated by creamy-bellied thrushes, but none appeared damaged in any way. In another study that used similar species and examined the eVect of gut passage on germination, seeds of two species of Solanum defecated by American robins (Turdus migratorius) were nearly 100% viable (Cipollini and Levey 1997c). More generally, germination of seeds in Xeshy fruits is typically enhanced by gut passage of fruit-eating birds (Traveset 1998). Taken together, this evidence suggests that the most common consumers of C. annuum and C. chacoense fruits are legitimate seed dispersers. Second, small mammal consumers of fruits and seeds must be common at our study sites. This condition is
necessary to dismiss the explanation that we failed to detect removal by small mammals because they were not present. Rodents are abundant and diverse in arid regions of southwestern North America, where they comprise a major guild of granivores (Heske et al. 1994; Brown et al. 2001). At our Arizona study site, the two most abundant species that consume seeds and fruits are the cactus mouse (Peromyscus eremicus) and desert woodrat (Neotoma lepida); non-Capsicum fruits are frequently consumed by them (Tewksbury et al. 1999; Tewksbury and Nabhan 2001). Because both of these rodents are good climbers (Caras 1967; HoVmeister 1971), C. annuum fruits on branches would be accessible to them. The small mammal community of our Bolivian study site is totally unstudied. Experiments comparing removal of seeds in cages (protected from rodents) to removal of uncovered seeds have revealed higher removal of uncovered seeds, a diVerence that we attribute mostly to the foraging of granivorous rodents (J. Tewksbury and D. Levey, unpublished data). In nearby chaco habitat, at least ten species of small rodents in seven genera have been recorded (Anderson 1997; Taber et al. 1997; Chu et al. 2003). At least three of these genera (Graomys, Oligoryzomys, and Oryzomys) are generally considered to be arboreal and to consume seeds (Eisenberg and Redford 1999). Third, removal of chili fruits by birds must not be unusually rare for a bird-dispersed shrub. Although the directed deterrence hypothesis does not require total deterrence of seed predators or total lack of deterrence of seed dispersers, it is important to rule out the possibility that all types of fruit consumers are generally deterred (general toxicity hypothesis; Cipollini and Levey 1997c). In this respect, the low removal rates of fruits by birds at both of our study sites (ca. 3% per day), might indicate that fruit-eating birds avoid consumption of chili fruits—that capsaicin is generally toxic. We do not believe this to be the case because similarly low removal rates typify bird-dispersed shrubs with small crop sizes (Willson and Whelan 1993; Li et al. 1999; Delgado Garcia 2002; McCarty et al. 2002; Tsahar et al. 2003; Kwit et al. 2004) and because ripe chili fruits can persist for > 1 month and almost all are eventually consumed (J. Tewksbury and D. Levey, unpublished data). Furthermore, birds are physiologically incapable of sensing capsaicin (Jordt and Julius 2002). Fourth, small mammals must be likely to destroy any chili seeds that they consume. If this were not the case, these mammals would not be seed predators and the directed deterrence of capsaicin would not apply to them. When cactus mice and packrats are oVered seeds from pungent Capsicum fruits, they totally avoid them (Tewksbury and Nabhan 2001). However, when the
123
Oecologia
same species are oVered naturally non-pungent Capsicum fruits, they consume them and destroy the seeds (Tewksbury and Nabhan 2001). We have been unable to test treatment of Capsicum seeds by Bolivian small mammals but we expect similar results. With a related species of rodent (Peromyscus maniculatus) that consumes fruits and seeds from two species of Solanum (which is in the same family as Capsicum), essentially no seeds are passed intact (Cipollini and Levey 1997c). Finally, capsaicin is expected to occur in Capsicum plants primarily where it will be most likely to deter seed predators—i.e., in and around the seeds. If it occurred in abundance throughout Capsicum plants, its primary function would unlikely be directed toward seed predators (Ehrlen and Eriksson 1993; Cipollini and Levey 1998). Unlike many secondary compounds, which occur throughout the plants that produce them (Ehrlen and Eriksson 1993), capsaicin indeed occurs at high concentrations only in fruit and it is concentrated around the seeds (Suzuki et al. 1980; Fujiwake et al. 1982). Fruit nutrient content Nutritionally, chili fruits of both species are extraordinarily rich in lipids. Values of 24 and 35% lipid (C. annuum and C. chacoense, respectively) are approximately 6–9 times higher than the average of 21 other fruit species in the same family (Solanaceae; Jordano 2000), and higher than the averages of species in 22 additional families with vertebrate-dispersed fruits, including families characterized by lipid-rich fruits (Jordano 2000). As typical of fruits with high lipid content (Jordano 1995), the carbohydrate content of chili fruits we assayed was relatively low, 16–24%, compared to an average of 65% across 25 families of fruiting plants (Jordano 2000). Protein, which tends to vary independently of lipid and carbohydrate content across families was comparable to other solanaceous fruits (9– 10%) and higher than the averages of 24 of 25 additional families (Jordano 2000). Field and laboratory studies demonstrate the importance of fruit nutrient content in diet selection of fruiteating birds (Levey 1987; Jordano 2000; Schaefer et al. 2003). Some species prefer fruits that are high in carbohydrates and low in lipids, whereas others prefer fruits low in carbohydrates and high in lipids (Fuentes 1994; Witmer 1996; Witmer and Van Soest 1998; Levey and Martínez del Rio 2001). The former tend to have rapid transit of digesta through the gut, whereas the latter have slower transit times and feed frequently on insects or seeds (Fuentes 1994; Witmer and Van Soest 1998; Levey and Martínez del Rio 2001). This general pattern Wts our results. Most avian species that we
123
observed consuming wild chili fruits are omnivores that consume mostly insects or seeds, at least during part of their annual cycle (Martin et al. 1951). Our observations also agree with previous work documenting that thrushes, mimids, and some species of Xycatchers specialize in lipid-rich fruits (Loiselle and Blake 1990; Stiles 1993; Fuentes 1994; Witmer and Van Soest 1998). Indeed, these taxa comprised the vast majority of chili fruit consumption records at both sites (Fig. 1). Further tests of the directed deterrence hypothesis A unique opportunity exists for testing the directed deterrence hypothesis in Bolivia, where at least three species of Capsicum are polymorphic for production of capsaicinoids (Tewksbury et al. 2006). In these species, individuals that bear only pungent fruit can be found near individuals that produce only non-pungent fruit. Also, the ratios of pungent to non-pungent individuals vary geographically (Tewksbury et al. 2006). The directed deterrence hypothesis predicts that mammals would more likely consume fruits from non-pungent individuals than from pungent individuals and that birds would consume pungent and non-pungent fruits equally. This prediction assumes that fruit nutrient proWles do not co-vary with pungency. For at least one species, C. chacoense, this is indeed the case; proportions of lipids, proteins, simple sugars, and complex carbohydrates do not diVer between pungent and nonpungent fruits (Table 1, footnote a). It remains unclear how common directed deterrence may be among other fruiting plants. Although it is diYcult to record all fruit consumers of a given species, it appears that many bird-dispersed fruits are left alone by granivorous rodents (e.g., squirrels in north temperate forests). This pattern is consistent with the directed deterrence hypotheses, suggesting that a primary reason directed deterrence is rarely documented is because it is rarely studied. Acknowledgements We thank Robert Dobbs, Meribeth Huzinga, Dan Cariveau, and Melissa Simon for Weld help in Bolivia and Arizona. Rebecca Neal, Sarah Stephan, and Christopher Worrell helped with the nutritional analyses. Chris Whelan and an anonymous reviewer provided constructive comments that greatly improved the manuscript. This work was supported by the National Geographic Society and the National Science Foundation (NSF DEB-0129168).
References Adler LS, Karban R, Strauss SY (2001) Direct and indirect eVects of alkaloids on plant Wtness via herbivory and pollination. Ecology 82:2032–2044
Oecologia Andelt WF, Burnham KP, Baker DL (1994) EVectiveness of capsaicin and Bitrex repellents for deterring browsing by captive mule deer. J Wildl Manage 58:330–334 Anderson S (1997) Mammals of Bolivia: taxonomy and distribution. American Museum of Natural History, New York Bernays EA, Chapman RF (1994) Host-plant selection by phytophagous insects. Chapman & Hall, New York Bollen A, Van Elsacker L, Ganzhorn JU (2004) Relations between fruits and disperser assemblages in a Malagasy littoral forest: a community-level approach. J Trop Ecol 20:599–612 Bosland PW (2001) Preliminary Weld tests of capsaicinoids to reduce lettuce damage by rabbits. Crop Prot 20:535–537 Brown DE (1982) Biotic communities of the American Southwest: United States and Mexico. Desert Plants 4:1–342 Brown JH, Whitham TG, Ernest SKM, Gehring CA (2001) Complex species interactions and the dynamics of ecological systems: long-term experiments. Science 293:643–650 Caras RA (1967) North American mammals. Meredith, New York Chu YK, Owen RD, Gonzalez LM, Jonsson CB (2003) The complex ecology of hantavirus in Paraguay. Am J Trop Med Hyg 69:263–268 Cipollini ML (2000) Secondary metabolites of vertebrate-dispersed fruits: evidence for adaptive functions. Rev Chil Hist Nat 73:421–440 Cipollini ML, Levey DJ (1997a) Antifungal activity of Solanum fruit glycoalkaloids: implications for frugivory and seed dispersal. Ecology 78:799–809 Cipollini ML, Levey DJ (1997b) Secondary metabolites of Xeshy vertebrate-dispersed fruits: adaptive hypotheses and implications for seed dispersal. Am Nat 150:346–372 Cipollini ML, Levey DJ (1997c) Why are some fruits toxic? Glycoalkaloids in Solanum and fruit choice by vertebrates. Ecology 78:782–798 Cipollini ML, Levey DJ (1998) Secondary metabolites as traits of ripe Xeshy fruits: a response to Eriksson and Ehrlen. Am Nat 152:908–911 Coley PD, Barone JA (1996) Herbivory and plant defenses in tropical forests. Annu Rev Ecol Syst 27:305–335 Cordell GA, Araujo OE (1993) Capsaicin: identiWcation, nomenclature, and pharmacotherapy. Ann Pharmacother 27:330– 336 Corlett RT (1996) Characteristics of vertebrate-dispersed fruits in Hong Kong. J Trop Ecol 12:819–833 Debussche M, Isenmann P (1989) Fleshy fruit characters and the choices of bird and mammal seed dispersers in a Mediterranean region. Oikos 56:327–338 Delgado Garcia JD (2002) Interaction between introduced rats and a frugivore bird-plant system in a relict island forest. J Nat Hist 36:1247–1258 Dib B (1990) After two weeks habituation to capsaicinized food, rats prefer this to plain food. Pharmacol Biochem Behav 37:649–653 Ehrlen J, Eriksson O (1993) Toxicity in Xeshy fruits—a non-adaptive trait? Oikos 66:107–113 Eisenberg JF, Redford KH (1999) Mammals of the neotropics. The central neotropics. University of Chicago Press, Chicago, Ill. Fuentes M (1994) Diets of fruit-eating birds: what are the causes of interspeciWc diVerences? Oecologia 97:134–142 Fujiwake H, Suzuki T, Iwai K (1982) Formation and metabolism of the pungent principle of Capsicum fruits. II. Capsaicinoid formation in the protoplast from the placenta of Capsicum fruits. Agric Biol Chem 46:2591–2592 Furuse T, Blizard DA, Moriwaki K, Miura Y, Yagasaki K, Shiroishi T, Koide T (2002) Genetic diversity underlying capsaicin
intake in the Mishima battery of mouse strains. Brain Res Bull 57:49–55 Galef BG (1989) Enduring social enhancement of rats’ preferences for the palatable and the piquant. Appetite 13:81–92 Green BG (1989) Capsaicin sensitization and desensitization on the tongue produced by brief exposures to a low concentration. Neurosci Lett 107:173–178 Green BG (1991) Temporal characteristics of capsaicin sensitization and desensitization on the tongue. Physiol Behav 49:501–505 Herrera CM (1982) Defense of ripe fruits from pests: its signiWcance in relation to plant–disperser interactions. Am Nat 120:218–241 Herrera CM (2002) Seed dispersal by vertebrates. In: Herrera CM, Pellmyr O (eds) Plant–animal interactions: an evolutionary approach. Blackwell Science, Oxford, pp 185–210 Heske EJ, Brown JH, Mistry S (1994) Long-term experimental study of a Chihuanhuan desert rodent community: 13 years of competition. Ecology 75:438–445 Hilker DM, Hee J, Higashi J, Ikehara S, Paulsen E (1967) Free choice consumption of spiced dishes by rats. J Nutr 91:129–131 HoVmeister DF (1971) Mammals of the Grand Canyon. University of Illinois Press, Urbana, Ill. Iwai K, Suzuki T, Fujiwake H (1979) Formation and accumulation of pungent principle of hot pepper fruits, capsaicin and its analogs, in Capsicum annuum var. annuum cv. karayatsubusa at diVerent growth-stages after Xowering. Agric Biol Chem 43:2493–2498 Izhaki I (2002) Emodin—a secondary metabolite with multiple ecological functions in higher plants. New Phytol 155:205–217 Jahn AE, Davis SE, Saavedra AM (2002) Patterns of austral bird migration in the Bolivian Chaco. J Field Ornithol 73:258–267 Janson CH (1983) Adaptation of fruit morphology to dispersal agents in a neotropical forest. Science 219:187–189 Janzen DH (1977) Why fruits rot, seeds mold, and meat spoils. Am Nat 111:691–713 Jones CG, Hare JD, Compton SJ (1989) Measuring plant protein with the Bradford assay. I. Evaluation and standard method. J Chem Ecol 15:979–992 Jordano P (1995) Angiosperm Xeshy fruits and seed dispersers: a comparative analysis of adaptation and constraints in plant– animal interactions. Am Nat 145:163–191 Jordano P (2000) Fruits and frugivory. In: Fenner M (eds) Seeds: the ecology of regeneration in natural plant communities. CAB International, London, pp 105–151 Jordt SE, Julius D (2002) Molecular basis for species-speciWc sensitivity to “hot” chili peppers. Cell 108:421–430 Karrer T, Bartoshuk LM (1991) Capsaicin desensitization and recovery on the tongue. Physiol Behav 49:757–764 Kwit C, Levey DJ, Greenberg CH, Pearson SF, McCarty JP, Sargent S (2004) Cold temperature increases winter fruit removal rate of a bird-dispersed shrub. Oecologia 139:20–24 Levey DJ (1987) Sugar-tasting ability and fruit selection in tropical fruit-eating birds. Auk 104:173–179 Levey DJ, Cipollini ML (1998) A glycoalkaloid in ripe fruit deters consumption by Cedar Waxwings. Auk 115:359–367 Levey DJ, Martínez del Rio C (2001) It takes guts (and more) to eat fruit: lessons from avian nutritional ecology. Auk 118:819–831 Li X, Baskin JM, Baskin CC (1999) Contrasting dispersal phenologies in two Xeshy-fruited congeneric shrubs, Rhus aromatica Ait and Rhus glabra L. (Anacardiaceae). Can J Bot 77:976–988 Loiselle BA, Blake JG (1990) Diets of understory fruit-eating birds in Costa Rica: seasonality and resource abundance. Stud Avian Biol 13:91–103
123
Oecologia Martin AC, Zim HS, Nelson AL (1951) American wildlife and plants. A guide to wildlife food habitats. McGraw-Hill, New York Mason JR, Clark L (1995) Mammalian irritants as chemical stimuli for birds: the importance of training. Auk 112:511–514 Mason JR, Bean NJ, Shah PS, Clark L (1991) Taxon-speciWc diVerences in responsiveness to capsaicin and several analogs: correlates between chemical structure and behavioral aversiveness. J Chem Ecol 17:2539–2551 McBurney DH, Balaban CD, Christopher DE, Harvey C (1997) Adaptation to capsaicin within and across days. Physiol Behav 61:181–190 McCarty J, Levey D, Greenberg C, Sargent S (2002) Spatial and temporal variation in fruit use by wildlife in a forested landscape. For Ecol Manage 164:277–291 McKey D (1975) The ecology of coevolved seed dispersal systems. In: Gilbert LE, Raven PH (eds) Coevolution of animals and plants. University of Texas Press, Austin, Tex., pp 159–191 Moermond TC, Denslow JS (1985) Neotropical avian frugivores: patterns of behavior, morphology, and nutrition with consequences for fruit selection. In: Buckley PA, Foster MS, Morton EW, Ridgely RS, Buckley F (eds) Neotropical ornithology. American Ornithologists’ Union, Washington, D.C., pp 865–897 Norman DM, Mason JR, Clark L (1992) Capsaicin eVects on consumption of food by cedar waxwings and house Wnches. Wilson Bull 104:549–551 Pizo MA (2002) The seed-dispersers and fruit syndromes of Myrtaceae in the Brazilian atlantic forest. In: Levey DJ, Silva WR, Galetti M (eds) Seed dispersal and frugivory: ecology, evolution, and conservation. CAB International, Wallingford, pp 129–144 Place AR, Stiles EW (1992) Living oV the wax of the land: bayberries and yellow-rumped warblers. Auk 109:223–245 Prescott J (1999) The generalizability of capsaicin sensitization and desensitization. Physiol Behav 66:741–749 Prescott J, Stevenson RJ (1995) Pungency in food perception and preference. Food Rev Int 11:665–698 Rozin P, Kennel K (1983a) Acquired preferences for piquant foods by chimpanzees. Appetite 4:69–77 Rozin P, Kennel K (1983b) The nature and acquisition of a preference for chili pepper by humans. Appetite 4:69–77 Rozin P, Gruss L, Berk G (1979) Reversal of innate aversions: attempts to induce a preference for chili peppers in rats. J Comp Physiol Psychol 93:1001–1014 Rozin P, Mark M, Shilter D (1981) The role of desinitization to capsaicin in chili pepper ingestion and preference. Chem Senses 6:23–31 Santilli F, Mori L, Galardi L (2004) Evaluation of three repellents for the prevention of damage to olive seedlings by deer. Eur J Wildl Res 50:85–89 Schaefer HM, Schmidt V, Bairlein F (2003) Discrimination abilities for nutrients: which diVerence matters for choosy birds and why? Anim Behav 65:531–541 Shumake SA, Sterner RT, Gaddis SE (2000) Repellents to reduce cable gnawing by Norway rats. J Wildl Manage 64:1009–1013
123
Simmons CT, Dessirier J-M, Jinks SL, Carstens E (2001) An animal model to assess aversion to intra-oral capsaicin: increased threshold in mice lacking substance P. Chem Senses 26:491–497 Smith D (1981) Removing and analyzing total nonstructural carbohydrates from plant tissue. Wis Agric Exp Stn Bull No. 2107 Snow DW (1985) The web of adaptation: bird studies in the American tropics. Cornell University Press, Ithaca, N.Y. Spiro RG (1966) Analysis of sugars found in glycoproteins. In: NewWeld EG, Ginsberg V (eds) Methods in enzymology, vol VIII. Complex carbohydrates. Academic Press, New York, pp 3–26 Stiles EW (1993) The inXuence of pulp lipids on fruit preference by birds. Vegetatio 107/108:227–235 Suzuki T, Fujiwake H, Iwai K (1980) Formation and metabolism of pungent principle of Capsicum fruits. 5. Intracellularlocalization of capsaicin and its analogs, capsaicinoid, in Capsicum fruit. 1. Microscopic investigation of the structure of the placenta of Capsicum annuum var. annuum. Plant Cell Physiol 21:839–853 Swihart RK, Conover MR (1991) Responses of woodchucks to potential garden crop repellents. J Wildl Manage 55:177–181 Taber A, Navarro G, Arribas MA (1997) A new park in the Bolivia Gran Chaco: an advance in tropical dry forest conservation and community-based management. Oryx 31:189–198 Tewksbury JJ, Nabhan GP (2001) Directed deterrence by capsaicin in chilies. Nature 412:403–404 Tewksbury JJ, Nabhan GP, Norman DM, Suzan H, Toxill J, Donovan J (1999) In situ conservation of wild chiles and their biotic associates. Conserv Biol 13:98–107 Tewksbury JJ, Manchego C, Haak D, Levey DJ (2006) Where did the chili get its spice? Biogeography of capsaicinoid production in ancestral wild chili species. J Chem Ecol 32:547–564 Traveset A (1998) EVect of seed passage through vertebrate frugivores’ guts on germination: a review. Perspect Plant Ecol Evol Syst 1/2:151–190 Tsahar E, Friedman J, Izhaki I (2002) Impact of fruit removal and seed predation of a secondary metabolite, emodin, in Rhamnus alaternus fruit pulp. Oikos 99:290–299 Tsahar E, Friedman J, Izhaki I (2003) Secondary metabolite emodin increases food assimilation eYciency of yellow-vented bulbuls (Pycnonotus xanthopygos). Auk 120:411–417 Wagner KK, Nolte DL (2000) Evaluation of Hot Sauce (R) as a repellent for forest animals. Wildl Soc Bull 28:76–83 Williams S (1984) OYcial methods of analysis of the Association of Analytical Chemists, 14th edn. Association of OYcial Analytical Chemists, Arlington Willson MF, Whelan CJ (1993) Variation of dispersal phenology in a bird-dispersed shrub, Cornus drummondii. Ecol Monogr 63:151–172 Witmer MC (1996) Annual diet of cedar waxwings based on U.S. Biological Survey records (1885–1950) compared to diet of American robins: contrasts in dietary patterns and natural history. Auk 113:414–430 Witmer MC, Van Soest PJ (1998) Contrasting digestive strategies of fruit-eating birds. Funct Ecol 12:728–741
