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Is the Coyote (Canis latrans) a Potential SeedDisperser for the American Persimmon (Diospyrosvirginiana)?Author(s): Katherine Roehm and Matthew D. MoranSource: The American Midland Naturalist, 169(2):416-421. 2013.Published By: University of Notre DameDOI: http://dx.doi.org/10.1674/0003-0031-169.2.416URL: http://www.bioone.org/doi/full/10.1674/0003-0031-169.2.416

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Is the Coyote (Canis latrans) a Potential Seed Disperser for theAmerican Persimmon (Diospyros virginiana)?

KATHERINE ROEHM AND MATTHEW D. MORAN1

Department of Biology, Hendrix College, 1600 Washington Avenue, Conway, AR 72032

ABSTRACT.—The role of carnivores in seed dispersal has only recently been studied in NorthAmerican plants. We investigated the potential effectiveness of the Coyote (Canis latrans) as aseed disperser for American Persimmon (Diospyros virginiana; Ebenaceae) and tested theeffect of experimental design in gut passage experiments. Germination percentage and rateand vigor of seedlings produced by D. virginiana seeds collected from Coyote scat werecompared to seeds removed from or contained in whole fruit in a common gardenexperiment. Germination percentages for Coyote ingested seeds and whole fruit were nearlythe same. Emergence was significantly faster for seedlings produced from ingested seedscompared to those seeds in whole fruit, however the quality of these seedlings wassignificantly poorer. Seedlings produced by seeds artificially removed from fruits had greatersurvival than those resulting from seeds ingested by coyotes or contained in intact fruits. Ourresults suggest that Coyotes can effectively disperse D. virginiana,but whether the positiveaspects of dispersal outweigh the negative effects of gut passage remains an open question.Our experimental results indicate that these two species have not coevolved, as expected,since the range of Coyotes has only recently overlapped substantially with that of D. virginiana.

INTRODUCTION

Authors have proposed that several large fruited plants are anachronistic (Barlow, 2000),in that there is no obvious extant seed disperser, despite the production of large, apparentlyedible fruit. Presumably, the coevolved mutualistic animal disperser is recently extinct. Aclassic example includes the Tombalacoque Tree (Calvaria major) of Mauritious (Temple,1977), which may have coevolved with the Dodo Bird (Raphus cucullatus), although thisexample has come under intense scrutiny in recent years. (Barlow, 2000; Witmer and Cheke,1991). North America may have an especially rich variety of anachronistic fruits, due to thelate Pleistocene megafaunal extinction that occurred about 10,000 years ago. The AmericanPersimmon (Diospyros virginiana) produces a large true berry which has been described aseither a strong (Janzen and Martin, 1982) or moderate (Barlow, 2000) candidate as ananachronistic fruit.

The American Persimmon ranges throughout the eastern half of the United States fromthe Great Plains to the Atlantic Coast, north to the 40th parallel (Halls, 1981). The fossilrecord of Diospyros extends from the mid Cretaceous Period and Diospyros virginiana waspresent and presumably abundant in North America during the Pleistocene (Skallerup,1953). Although it is unknown if there was a now-extinct megafaunal seed disperser for theAmerican Persimmon (Mastadons have been suggested, Barlow, 2000), it is too large to beconsumed by typical temperate North American dispersers such as birds (Skallerup, 1953).However, with its fleshy pericarp, it appears to be a large potential food reward (Chambersand MacMahon, 1994). The fruit is consumed by several native carnivores which mayrepresent an example of an atypical seed disperser. Species from the Order Carnivora havenot typically been considered good candidates for coevolution with plants as seed dispersers,since they feed predominately on other animals. However, many carnivores frequently

1 Corresponding author: Moran@hendrix.edu

Am. Midl. Nat. (2013) 169:416–421

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include plant material in their diet (Herrera, 1989; Willson, 1993) especially fruits with highcaloric value (Traba et al., 2006; Alves-Costa and Eterovick, 2007; Guitian and Munilla,2010), and it has been suggested that carnivores contribute to seed dispersal, particularly infleshy fruited temperate North American plants (Willson, 1993). Carnivores may evenprovide advantages such as larger foraging ranges and longer seed passage times (Zhou etal., 2008).

One candidate seed disperser for the Diospyros virginiana is the Coyote (Canis latrans)which is known to frequently include fruit in its diet. The seeds of various plants are knownto survive gut passage in Coyotes and in some cases appear to benefit from the interaction(Silverstein, 2005). Coyotes consume persimmon fruits in large quantities (Chavez-Ramirezand Slack, 1993; Cypher and Cypher, 1999). An Illinois study showed that Persimmon seedscould survive gut passage through Coyotes, but the authors argued against coevolutionbecause seeds had higher mortality when eaten (Cypher and Cypher, 1999).

Here we report the effect of Coyote ingestion on germination success, seedlingemergence time, and growth after emergence. There have been several experimentaldesign issues raised about seed dispersal experiments, especially in terms of proper controls.For instance, many researchers compare ingested seeds with seeds dissected from fruits.Samuels and Levey (2005) and Robertson et al. (2006) have stressed the importance ofincluding planted whole fruits which is more representative of an unconsumed fruit innature. We therefore included different experimental groups, some mimicking naturalconditions and some representing common experimental procedures from the literature todetermine how design affects results.

MATERIALS AND METHODS

All collections were performed in Faulkner and Conway Counties, in central Arkansas.Freshly fallen persimmon fruits were collected from Nov. 5–12, 2010 and twelve Coyote scatswere collected from Nov. 5–6, 2010 along trails and gravel roads within the two counties(seeds per scat: mean 6 SE 5 16.0 6 3.72). Scats and fruits from trees were collected in thesame area, although we could not determine from what tree the scat seeds originated. Wefirst dissected 35 persimmon fruits to determine the average number of seeds per fruit(mean 6 SE 5 2.68 6 0.34), a necessary calculation for the experimental design.

We established four experimental groups. The first experimental group consisted ofwhole fruit (WF) planted intact and unmanipulated. We did not determine number ofseeds per fruit a priori since this process would have damaged the fruit. Seeds that werecollected from Coyote scat were planted three to a pot (Coyote Multiple: CM), which is theaverage number of seeds found per fruit (mean 5 2.68). The last two experimental groupswere seeds dissected from fruits, one group consisted of a single planted seed (DissectedSingle: DS) and the other group consisted of three planted seeds (Dissected Multiple: DM)in order to match the CM experimental group. Seeds from the CM, DM, and DS groupswere randomly assigned to pots. Dissected seeds had the entire pericarp removed so thatonly the seed and seed coat remained. We consider the first two experimental groups (WFvs. CM) to be most natural, while the latter two experimental groups less natural, althoughthese types of experimental treatments have been used in many published studies(Samuels and Levey, 2005).

On Nov. 11–12, 2010, seeds and fruits were planted 1 cm deep in 200 ml plastic pots filledwith GardenPlusTM all-purpose potting soil. Number of pots per treatment groups (i.e.,replicates) were 50 (WF), 50 (DS), 36 (CM), and 36 (DM). Total number of seeds for DS,CM, and DM were 50, 108, and 108 respectively. Number of seeds in the WF treatment was

2013 ROEHM & MORAN: COYOTES AS SEED DISPERSERS 417

104 and determined at the end of the experiment when pots were carefully searched for anyseeds that failed to germinate. We placed the pots in a refrigerator at 4 C for 68 d to cold-stratify the seeds, which is a requirement for the American Persimmon to germinate (Halls,1981). On Jan. 19, we placed the pots in a greenhouse, watered and observed every otherday for 95 d, after which the experiment was terminated. Germination rate and emergencetime was determined by the first appearance of the seedling above the ground. At the end ofthe experiment, seedlings were cut at the ground level, dried at 50 C for 24 h and weighedto determine above ground biomass. We also examined all seeds that had not produced aseedling to determine if germination had begun (in no cases had this occurred).

We analyzed germination rate by Chi-square analysis followed by pairwise comparisons.Since the measure was germination success (positive or negative) and some treatments havemultiple seeds per plot, there is inevitable pseudoreplication in the Chi-square analysis. Forseedling emergence times and final mass, we calculated the mean values per pot beforeanalysis to avoid pseudoreplication. Seedling emergence time and final seedling mass wereanalyzed by One-way ANOVA followed by a Tukey post-hoc test if significance was found. Allanalyses were performed on IBM SPSS statistical package.

RESULTS

Experimental treatment had significantly different seedling emergence proportions(Chi square 5 46.56, df 5 3, P , 0.001). Seeds that had passed through Coyotes (CM) hadalmost the same percentage of seeds germinate (45.2%) as seeds from the whole fruit(WF) experimental group (45.4%). The other two experimental groups had much highergermination success (dissected single seeds (DS) 5 84.0%, dissected multiple seeds (DM)5 78.5%). Pairwise comparisons indicated that the proportion of seeds that germinatedwere not significantly different for WF and CM treatments (Chi-square 5 0.001, df 5 1, P5 0.98) but they differed significantly from DM and DS treatments (WF vs. DM, Chi square5 24.86, df 5 1, P , 0.001; WF vs. DS, Chi square 5 20.85, df 5 1, P , 0.001; CM vs. DM,Chi square 5 25.01, df 5 1, P , 0.001; CM vs. DS, Chi-square 5 20.89, df 5 1, P , 0.001)while DM and DS treatments were not significantly different (Chi square 5 0.65, df 5 1, P5 0.42).

There was a significant effect of experimental treatment (One-way ANOVA, F3,121 5

16.51, P , 0.001) on number of days to emerge with whole fruits taking the longest time(mean 5 54 6 2.8 days). Dissected single seeds had the shortest emergence time (mean 5

30 6 2.0 days) while dissected multiple seeds had an intermediate emergence time (mean 5

40 6 2.2 days). Seeds that had been consumed by Coyotes had a significantly shorteremergence time (mean 5 35 6 2.5 days) when compared to only whole fruits, but were notdifferent from the two dissected seed experimental groups.

The mass of the persimmon seedlings at the end of the experiment was significantlydifferent between experimental groups (One-way ANOVA, F3,121 5 2.95, P 5 0.036). Seeds thatpassed through Coyotes produced seedlings with significantly smaller masses, approximately29% smaller than the whole fruit experimental group. The seedling masses in the two dissectedseed groups and whole fruit group did not differ significantly at the end of the experiment(Fig. 1). Both the whole fruit group and the dissected single group had significantly higherseedling masses compared to seedlings from seeds that passed through Coyotes.

There appeared to be a qualitative difference in seedlings among the experimentalgroups. The seed coat often remained attached to seedlings in coyote ingested seeds, whichappeared to damage the young plants and affect post-emergence growth. Seedlingsresulting from seeds contained in whole fruits almost always lacked the seed coat.

418 THE AMERICAN MIDLAND NATURALIST 169(2)

DISCUSSION

Clearly the seeds of Diospyros virginiana can survive gut passage through Coyotes whichagrees with the results of Cypher and Cypher (1999). In fact, the germination rate forCoyote ingested seeds was almost exactly the same as those planted in whole fruits, our mostnatural comparison group. Interestingly, our two dissected seed groups had much highergermination success compared to our two more natural experimental groups, showing theimportance of experimental design in these types of studies (Samuels and Levey, 2005). Ourexperiment demonstrates the necessity of including whole fruit experimental groups in seeddispersal studies. If we had not incorporated this treatment in our experiment and onlycompared Coyote ingested seeds to those artificially removed from fruit, we would haveconcluded that Coyote passage has a substantial negative effect on seed germination.

Coyote gut passage and artificial removal of seeds decreased the time required foremergence when compared to whole fruits. It is well known that some fruits contain growthinhibitors which delay seed germination (Robertson et al., 2006), presumably as anadaptation to ensure animal consumption before germination. Although persimmon fruitdelayed emergence, maintaining the intact fruit did not affect final germinationpercentages. It has been suggested that fruit inhibition is a strategy to distributegermination over a longer period of time (Kelly et al., 2004) increasing the probabilitythat at least some seedlings survive. Indeed, the range for the Coyote ingested was 70 dayscompared to 91 days for whole fruit seeds.

Seedlings that resulted from seed that had passed through Coyotes had significantlysmaller mass by the end of the experiment than the WF and DS treatments, but not the DMseed treatment. This result was surprising considering that Coyote seedlings also emerged inless time, giving them more potential time to grow. Therefore, we suggest that Coyote gut

FIG. 1.—Mean weight of seedlings (61SE) for the four experimental groups at the end of the study.Letters indicate statistically different groups after post-hoc (Tukey) analysis

2013 ROEHM & MORAN: COYOTES AS SEED DISPERSERS 419

passage of seeds retarded early seedling growth. Seeds that had passed through Coyotes(98%) and those that were artificially dissected from fruits (multiple seed pots 5 89%, singleseed pots 5 93%), tended to have the seed coat remaining on the seedling to the pointwhere growth was inhibited and obvious leaf and stem damage occurred. Seeds contained inintact fruits tended to produce seedlings without the seed coat attached (23% attached)which apparently allowed them to grow rapidly after germination. The effect was probablycaused by damage to the ruminate endosperm which affected adherence to the seed coat(Bayer and Appel, 1996).

More experiments (field experiments) will be necessary to determine if Diospyrosvirginiana seeds benefit from being consumed by Coyotes. Considering the reduction inseedling quality in Coyote ingested seeds and similar germination rates between thoseseedlings from intact fruit and Coyote ingested seeds, we agree with Cypher and Cypher(1999) that there is no evidence of coevolution between these two species. Indeed it appearsfrom this experiment that seedlings from Coyote scat will start their developmentsubstantially behind those that have not experience gut passage. This result is notnecessarily surprising since Coyotes only recently expanded eastward in the eastern part ofNorth America where the D. virginiana is abundant. Whether there is a net positive effect onpersimmons will be dependent on the dispersal advantage outweighing the reduction inseedling quality shown in this experiment and will require field studies to determine.Cypher and Cypher (1999) showed that the Raccoon (Procyon lotor) may increase thegermination percentage for persimmons and is a more likely coevolution candidate.Coyotes, with their recent range expansion into eastern North America, substantialpopulation increase (Gompper, 2002), and heavy consumption of Persimmon fruit maytherefore be exerting a negative effect on persimmon recruitment.

Acknowledgments.—We wish to thank M. Raney for help in the field and A. Willyard for advice onexperimental design, reading an earlier draft of the manuscript, and help in the laboratory. R. Brownassisted with the greenhouse portion of the study. J. Penner assisted in the statistical analysis. RogerAnderson and two anonymous reviewers made valuable suggestions to improve the manuscript.

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SUBMITTED 12 DECEMBER 2011 ACCEPTED 19 JULY 2012

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