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Does Gut Passage Affect Post-dispersal Seed Fate in a Wild Chili, Capsicum annuum?
Clay F. Noss and Douglas J. Levey

Southeastern Naturalist, Volume 13, Issue 3 (2014): 475–483

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Southeastern Naturalist 475 C.F. Noss and D.J. Levey 22001144 SOUTHEASTERN NATURALIST 1V3o(3l.) :1437,5 N–4o8. 33 Does Gut Passage Affect Post-dispersal Seed Fate in a Wild Chili, Capsicum annuum? Clay F. Noss1,2,* and Douglas J. Levey3,4 Abstract - Seeds of Capsicum spp. (wild chilies ) are coated with capsaicin, which deters mammalian seed predators. During gut passage through frugivorous birds, its presence on seeds likely is greatly reduced, presumably increasing the seeds’ susceptibility to postdispersal seed predation by mammals. We tested whether gut passage influences the rate at which dispersed seeds are removed from dispersal sites by different types of seed consumers. We predicted that seeds passed through birds (passed seeds) would be removed at higher rates than seeds taken directly from fruits (non-passed seeds). Removal rates of passed seeds were either lower or no different than removal rates of non-passed seeds, contrary to our prediction. In a second set of trials, we placed caged and exposed (control) seeds in pairs on the ground to determine whether vertebrates or invertebrates were primarily responsible for post-dispersal seed removal. We found an inconsistent effect of caging on frequency of seed removal, indicating that both invertebrates and vertebrates harvest chili seeds at our site. These results suggest that capsaicin’s role in mediating interactions with vertebrate seed dispersers and predators is largely restricted to the wild chilies’ fruiting stage. Introduction Seed dispersal by animals is a critically important process in the ecology and evolution of fruiting plants (Jordano 2000, Tiffney 2004). Despite many potential advantages of fruits being ingested, carried, and deposited away from parent plants, most plant-oriented studies of seed dispersal have narrowly focused on consequences of where seeds are dispersed (Howe and Miriti 2004, Nathan and Muller-Landau 2000). Relatively few studies have examined how gut treatment may impact condition and subsequent fate of seeds, and of those studies, the vast majority have tested solely for the effect of gut treatment on germination (Barnea et al. 1991, Samuels and Levey 2005, Traveset et al. 2007). Any advantages associated with germination, however, would be rendered irrelevant if seeds are consumed soon after dispersal. In this context, it is becoming increasingly apparent that gut treatment can change the chemical and physical structure of seeds in ways that impact post-dispersal seed predation (Andresen and Levey 2004, Fricke et al. 2013, Manzano et al. 2010, Mártinez-Mota et al. 2004). Capsicum spp. (wild chilies ) provide an unusually good study system for examining effects of gut treatment on the post-dispersal fate of animal-dispersed seeds. 1Department of Wildlife Ecology and Conservation, University of Florida, Gainesville, FL 32611-8525. 2Current address - Department of Enviornmental Science, Policy, and Management, University of California - Berkeley, Berkeley, CA. 3Department of Biology, University of Florida, Gainesville, FL 32611-8525. 4Current address - National Science Foundation, 4201 Wilson Boulevard, Arlington, VA 22230. *Corresponding author - claynoss@gmail.com. Manuscript Editor: Frank Moore Southeastern Naturalist C.F. Noss and D.J. Levey 2014 Vol. 13, No. 3 476 First, because chili fruits contain capsaicinoids, which elicit pain in mammals but not birds (Jordt and Julius 2002, Mason and Clark 1995, Tewksbury and Nabhan 2001), practically all chili seeds are dispersed by birds (Levey et al. 2006). Given that taxonomically dissimilar frugivorous birds process fruits in a similar manner (Karasov and Levey 1990), there is presumably much less variation in the condition of defecated chili seeds than in the seeds of species consumed and defecated by both birds and mammals. Second, mechanisms by which gut passage of chili seeds may affect seed condition are already established (Fricke et al. 2013). Digestive processing likely reduces the presence of capsaicinoids that coat the outside of chili seeds, thus leading to the prediction that chili seeds passed through a bird’s gut will be more susceptible to post-dispersal seed predation by mammals than seeds not passed through a bird’s gut. If this capsaicin-stripping prediction is supported, it will provide a rare example of how vertebrate seed dispersal may be detrimental to a fruiting plant. We experimentally tested effects of gut passage by birds on seed removal of a wild chili, Capsicum annum L. (Bird Pepper). Our study had two goals: (1) to test the capsaicin-stripping prediction, and (2) to determine whether vertebrates or invertebrates are the most common post-dispersal seed predators at our study site. The second goal was important in interpreting results of the experiment we conducted to test the prediction. In particular, if ants removed most chili seeds then we would not have expected a difference in seed removal of gut-passed and non-gutpassed seeds because ants are not deterred by capsaicin (D.J. Levey, pers. observ.). Methods Field site description This study took place on Seahorse Key, a 64-ha island in the Big Bend region of Florida’s west coast, approximately 8 km from mainland Florida (29°07'30''N, 83°2'W; Lillywhite et al. 2002, Spears 1987). As part of the Lower Suwannee National Wildlife Refuge, the island is undeveloped and retains much of its original flora and fauna. In temperate woodlands (like Seahorse Key), rodents are generally the most important granivores (Hulme 1998), but ants are usually better at locating small seeds at low densities (like those used in this study; Kaspari 1993, Manzano et al. 2010), and in Bolivia, ants are post-dispersal predators of chilies (Fricke et. al. 2013). Common mammalian seed predators present on Seahorse Key include various rodents (Peromyscus spp. [deer mice], other Muridae, Sciurus carolinensis Gmelin [Carolina Squirrel]), and common invertebrate seed predators include several species of ants (Pogonomyrmex badius (Latrelle) [Florida Harvester Ant], Solenopsis invicta Buren [Red Imported Fire Ant], and Pheidole spp. [big-headed ants], D.J. Levey, pers. observ.). Avian seed predators are uncommon—the only one we have detected is Cardinalis cardinalis L. (Northern Cardinal). We worked on the interior of the island within Quercus virginiana Mill. (Southern Live Oak) woodlands (Spears 1987) where chili plants are common in the understory. Southeastern Naturalist 477 C.F. Noss and D.J. Levey 2014 Vol. 13, No. 3 Field experiments We collected all fruits and seeds used in this study on the island and we handled them with latex gloves and tweezers to reduce the presence of human scent, which is known to affect seed removal by ants and rodents (Duncan et al. 2002). Fruits were fed to captive Corvus ossifragus Wilson (Fish Crows) and Acridotheres tristis L. (Common Mynas). Fish Crows are abundant on Seahorse Key and consume a wide variety of fruits (McGowan 2001), almost certainly including those of Bird Peppers, although we have not observed them doing so. Common Mynas also consume fruits (Pell and Tidemann 1997) and occur in southern Florida, although not on Seahorse Key. We included them because we could not obtain a sufficient number of Fish Crows, and because both species were readily available at a nearby National Wildlife Research Center facility. Gut treatment of seeds by the two species is likely to be similar, given their similar body size and omnivorous diet. We fed chili fruits to birds, collected defecated (passed) seeds, and placed the seeds in a refrigerator the next day. We removed a similar number of seeds from fruits by hand (non-passed) and placed them in a refrigerator. We lightly blotted all seeds with damp paper towels before storage to simulate removal of fecal material by rain and to standardize the amount of pulp and feces remaining on seeds. In 2009, we tested the capsaicin-stripping prediction by placing 122 pairs of passed and non-passed seeds within 1 cm of each other, making it likely that seed predators would encounter both seeds of a pair and make a choice between them (Hulme 1994). We placed a Magnolia grandiflora L. (Southern Magnolia) leaf supported by a toothpick over each pair of seeds (station), providing protection from rain while allowing access by all granivores. Stations were placed every 5 m along a transect, and presence or absence of seeds was recorded every 2–6 days (daily at first) over the next 16 days, at which point very few seeds were being removed. We assumed removal of seeds indicated seed predation, although this is not necessarily the case (Levey and Byrne 1993). To meet our second objective, we conducted a similar experiment in which two passed seeds were placed within 2 cm of each other. We covered 1 seed in each pair with an 8-cm3 cage of 1-cm-wire mesh (hardware cloth) to exclude vertebrate granivores and left the other seed fully accessible to all granivores (control). One Southern Magnolia leaf protected each seed pair from rain. We placed 40 of these stations 5 m apart along eight 25-m transects, and recorded the presence or absence of seeds for 15 days. We repeated both experiments in 2010 with 64 replicates that we checked for 14 days. In both years, approximately 10% of stations were disrupted by wind or rain; such cases were excluded from analysis. Data analysis Data were analyzed using Pearson’s chi-squared test. We used data only from stations where, on the last day of the experiment, one of the paired seeds was missing and the other remained. Southeastern Naturalist C.F. Noss and D.J. Levey 2014 Vol. 13, No. 3 478 Results Removal rates of passed and non-passed seeds differed dramatically in 2009 (Fig. 1a). In 2009, over 50% of seeds disappeared in the first 4 days, and the removal rate of non-passed seeds was higher than that for passed seeds. After the initial divergence, the removal rate was similar for both seed types. At the end of the trial, significantly fewer non-passed than passed seeds remained (c2 = 12.73, Figure 1. Percentage of chili seeds defecated by birds (passed) or taken directly out of ripe fruit (non-passed) remaining at stations on successive days in 2009 (a) and 2010 (b). The difference in number of passed and non-passed seeds remaining at the end of the trial was significant in 2009 but not in 2010. Southeastern Naturalist 479 C.F. Noss and D.J. Levey 2014 Vol. 13, No. 3 df = 1, P < 0.001), contrary to our prediction. In 2010 the pattern of seed removal was obviously different; removal rates were lower, more constant, and closely similar between passed and non-passed seeds (c2 = 0.06, df = 1, P < 0.81; Fig. 1b), also contrary to our prediction. Figure 2. Percentage of chili seeds protected from vertebrate granivores (caged) or unprotected (exposed) remaining at stations on successive days in 2009 (a) and 2010 (b). The difference in number of caged and exposed seeds remaining at the end of the trial was significant in 2010 but not in 2009. Southeastern Naturalist C.F. Noss and D.J. Levey 2014 Vol. 13, No. 3 480 There was an inconsistent effect of caging on seed removal between years. In 2009, most seed removal occurred in the first 4 days and then co ntinued at a lower rate for the remainder of the experiment, resulting in an insignificant difference between exposed and caged seeds by the end of the trial (c2 = 1.92, df = 1, P < 0.17; Fig. 2a). In 2010, there was a relatively steady decline in caged seeds remaining during the experiment but the removal rate for exposed seeds was variable between checks. At the end of this experiment, significantly more caged than exposed seeds remained (c2 = 4.76, df = 1, P = 0.0291; Fig. 2b), indicating that mammalian granivores were present and had been prevented from removing caged seeds. We did not observe moved seeds, seed fragments, or other indicators of consumption by granivores near the experimental trials. Discussion We found no support for the prediction that treatment of chili seeds in bird guts increases the seeds’ risk of post-dispersal seed predation. To the contrary, gut passage apparently decreased the overall risk of seed removal in both years of our study, but the difference between passed and non-passed seeds was significant only in 2009. Results of the caging experiment in 2010 (but not 2009) showed that vertebrate (as well as invertebrate) granivores were present at our study site and that they removed chili seeds passed through bird guts, a finding that suggests that vertebrate granivores may be significant post-disperal seed predators. Seed removal by vertebrate granivores was important for us to document at our site because the capsaicin-stripping prediction assumes presence of mammalian seed predators. Previous studies have documented many benefits to plants of seed dispersal by vertebrates, including escape from high levels of seed and seedling mortality near the parent plant, reduction in microbial infection, directed dispersal to especially suitable microhabitats, and colonization of disturbed or novel habitats (Fricke et al. 2013, Herrera 2002). Our study, based on an examination of gut treatment, provides yet another potential benefit of vertebrate seed dispersal. We note, however, that the few studies comparing removal of passed and non-passed seeds, or seeds embedded or non-embedded in feces, do not yield a clear or consistent picture of any impact of gut passage on seed predation (Andresen 1999, Bermejo et al. 1998, Cochrane 2003, Fricke et al. 2013, Mártinez-Mota et al. 2004, Roberts and Heithaus 1986). Furthermore, at least some observed impacts from these studies are inconsistent between seasons (Mártinez-Mota et al. 2004) or within a season (Andresen 1999). For small-seeded temperate species like Bird Peppers, post-dispersal predation of defecated seeds is poorly understood; the vast majority of previous studies concern large-seeded tropical species (Manzano et al. 2010). An exception is a recent study by Fricke et al (2013), which found that gut passage increased Capsicum chacoense Hunz. (Tova) seed survival 370% by reducing ant predation and pathogenic fungal infection. Ant predation was reduced through gut removal of volatile chemicals that attract granivorous ants, a mechanism that may also explain the reduction in seed predation of gut-passed seeds that we observed in 2009. Southeastern Naturalist 481 C.F. Noss and D.J. Levey 2014 Vol. 13, No. 3 We provide two explanations for why our results differed between years. First, such variation is not surprising—practically all studies on seed predation that have looked for temporal variation have found it (e.g., Andresen 1999, LoGiudice and Ostdelf 2002, Mártinez-Mota et al. 2004, Schupp 1990, Willson and Whelan 1990). In our study, the rate of removal was appreciably higher in both sets of experiments in 2009 than in 2010, suggesting a biological difference in the community of seed predators. For example, activity of granivorous ants may have been higher in 2009 if daytime temperatures were higher than in 2010 (Traniello et al. 1984, Vickery and Bider 1981). However, average daytime temperature during our study periods did not differ (National Climatic Data Center 2010). A non-mutually exclusive explanation for the annual differences concerns statistical power. In both experiments, significant differences between treatments and controls were found in the year with greater replication—2009 for the comparison of passed and non-passed seeds, and 2010 for the comparison of caged and exposed seeds. This is a likely explanation in the experiments comparing removal of caged and exposed seeds because the sample size in 2010 was more than 50% greater than in 2009 (n = 64 and 40 pairs, respectively) and the overall patterns of removal were similar between years (compare the two panels of Fig. 2). On the other hand, in the experiments comparing removal of passed and non-passed seeds, there was an immediate, large, and lasting difference in removal in 2009 that was not apparent in 2010. Previous studies on dispersal of wild chilies have documented multiple benefits of capsaicinoids, including protection from fungal pathogens, longer gut-retention time in avian seed dispersers (which presumably increases dispersal distance), and deterrence of mammalian seed predators (Chichewicz and Thorpe 1996; Fricke et al. 2013; Levey et al. 2006, 2007; Tewksbury et al. 2008a, b). Although we expected the last of these benefits to be reduced or eliminated by gut treatment in frugivorous birds, we conclude that gut passage can increase any post-dispersal benefits already present due to capsaicin. More generally, we suggest that the traditional emphasis on dispersal benefits related to escape from high mortality near parent plants should be broadened to examine potential advantages associated with gut treatment (Fricke et al. 2013). 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