Germination rates of tree seeds ingested by coyotes and raccoons.
Abstract: The effect of ingestion by coyotes (Canis latrans) and raccoons (Procyon lotor) on seed germination was investigated for four tree species in Illinois. The germination rate of persimmon (Diospyros virginiana) seeds ingested by raccoons was significantly higher than the rate for uningested seeds. Both were significantly higher than the rate for coyote-ingested seeds. Among coyote-ingested seeds, germination rates of persimmon were significantly higher when seeds were protected by undigested fruit pulp or intact seed sheaths thus reducing the exposure of seeds to gastrointestinal enzymes. American plum (Prunus americana) seeds ingested by coyotes had a significantly lower germination rate compared to uningested seeds, whereas germination of pawpaw (Asimina triloba) seeds was similar between coyote-ingested and uningested seeds. Germination was significantly lower for hackberry (Celtis occidentalis) seeds ingested by raccoons compared to uningested seeds. Ingestion improved germination only for persimmon seeds consumed by raccoons, but tree species may realize other benefits from dispersal by coyotes and raccoons (e.g., decreased parental competition).
Subject: Germination (Research)
Tree seeds (Research)
Coyotes (Environmental aspects)
Raccoons (Environmental aspects)
Authors: Cypher, Brian L.
Cypher, Ellen A.
Pub Date: 07/01/1999
Publication: Name: The American Midland Naturalist Publisher: University of Notre Dame, Department of Biological Sciences Audience: Academic Format: Magazine/Journal Subject: Biological sciences; Earth sciences Copyright: COPYRIGHT 1999 University of Notre Dame, Department of Biological Sciences ISSN: 0003-0031
Issue: Date: July, 1999 Source Volume: 142 Source Issue: 1
Accession Number: 55329674
Full Text: INTRODUCTION

Seed dispersal in numerous species of plants is achieved through the process of endozoochory (van der Pijl, 1972) in which plants produce nutritious fleshy fruits that are consumed by animals which later defecate the seeds. The adaptive value of this mutualistic relationship can be inferred by its prevalence in nature and by the number of plant and animal species involved. Willson (1993) estimated that in North America alone seeds of species in about 100 genera are dispersed by animals, whereas 50-75% of tree species in tropical forests produce fruits adapted for animal dispersal (Howe and Smallwood, 1982). Passage through the gastrointestinal tracts of animals can have a beneficial, detrimental or neutral effect on seeds (Murray et al., 1994). Potential beneficial effects include thermal, chemical or mechanical scarification of seed coats, thereby facilitating germination (Clergeau, 1992). Potential detrimental effects include destruction or damage to seeds from mastication, mechanical abrasion or gastrointestinal enzymes, thereby reducing germination (van der Pijl, 1972; Murray et at., 1994). Although endozoochory has been extensively documented through animal food habit studies, the effects of gastrointestinal passage on seeds is rarely evaluated (Willson, 1993).

Seeds of plants producing fleshy fruits are usually dispersed by a suite of animal species (Howe and Smallwood, 1992). Specialized relationships between plants and animal dispersers are relatively rare (Howe and Smallwood, 1982), particularly in temperate regions (Willson, 1993). In North America, rapid post-Pleistocene changes in species ranges and assemblages resulted in relatively unspecialized mutualisms between animals and plants producing fleshy fruits (Willson, 1993). Thus, fruits of such plants are typically dispersed by multiple species and the effects of gastrointestinal passage on seeds likely varies among species.

Coyotes (Canis latrans) and raccoons (Procyon lotor) are highly frugivorous, consume fleshy fruits from a variety of plant species and are considered important seed dispersers (Willson, 1993). Coyotes, in particular, have been identified as significant dispersers for certain plant species (e.g., Cornett, 1985; Schupp et al., 1997). We investigated the effects of passage through the gastrointestinal tracts of coyotes and raccoons on seeds from four tree species in southern Illinois. We determined germination rates for persimmon (Diospyros virginiana), American plum (Prunus americana) and pawpaw (Asimina triloba) seeds ingested by coyotes, and for persimmon and hackberry (Celtis occidentalis) seeds ingested by raccoons. Germination rates for ingested seeds were compared to rates for uningested seeds to determine whether gastrointestinal passage produced a positive, negative or neutral effect on seed germination rates.

METHODS

Ripe fruits were collected from trees at the Crab Orchard National Wildlife Refuge (CONWR), Williamson and Jackson counties, Illinois. American plums were collected in July and August, pawpaws in September, persimmons in October and hackberries were collected in February. All fruits were gently macerated by hand-agitating on a mesh screen to remove fruit coats and mesocarps from seeds. Care was taken to avoid mechanically damaging seeds during cleaning.

Coyote scats were collected semimonthly along dirt roads as part of an investigation of coyote foraging ecology at CONWR (Cypher, 1991). Raccoon scats were collected from the top of concrete walls associated with abandoned munitions bunkers at CONWR. Scats of coyotes and raccoons were distinguished from each other and from the scats of other carnivores (e.g., gray foxes [Urocyon cinereoargenteus]) based on location, size and shape (Cypher, 1991). When handling scats precautions (e.g., rubber gloves, dust masks) were taken to minimize exposure to eggs and cysts of zoonotic parasites such as hydatid tapeworms (Echinococcus multilocularis) in coyote scats and ascarid roundworms (Baylisascaris procyonis) in raccoon scats. Seeds were hand separated from scats and carefully washed over a mesh screen. Seeds with obvious mechanical damage from mastication were excluded from the study.

Persimmon seeds collected from coyote scats were categorized based on the contents of the scats. Passage rates of seeds through the gastrointestinal tract may vary depending upon whether other foods were consumed concurrently. For example, passage rates of seeds from meals consisting entirely of fruit are likely to be more rapid due to the presence of laxatives (e.g., chemicals, bulk fiber) in fruit (e.g., Murray et al., 1994). Passage rates may be slower for seeds ingested with foods in addition to fruits. Therefore, seeds from scats visually estimated to consist of [greater than]90% persimmon and [less than or equal to]10% animal remains (e.g., hair, feathers, bone) were categorized as being from "fruit-meal" scats. Seeds from scats with [greater than]50% animal remains were categorized as being from "animal-meal" scats. Seeds from scats with 1050% animal remains were excluded from the study.

Fruit-meal scats of coyotes occasionally contained undigested mesocarp that surrounded persimmon seeds, and the sheath-like structures surrounding the seeds were sometimes entirely intact. Such mesocarp and sheaths may reduce the exposure of seeds to gastrointestinal enzymes, thereby influencing germination rates. Thus, persimmon seeds in fruit-meal scats from coyotes were further categorized as follows: (1) "mesocarp-protected" seeds had intact sheaths and were encompassed by undigested fruit mesocarp (2) "sheath-protected" seeds had intact sheaths but were not encompassed by mesocarp and (3) "unprotected" seeds lacked intact sheaths and were not encompassed by mesocarp.

Seeds from both fruits and scats were sorted by tree species and origin (i.e., coyote, raccoon or uningested fruit). All seeds were cold-stratified by mixing them with wet peat in 0.5-liter plastic containers and refrigerated at 2 C for 90-120 d (U.S. Department of Agriculture, 1974). Water was added to containers as needed to keep the peat and seeds moist. Following cold stratification seeds were removed from the peat and rinsed. Seeds were then planted 1 cm deep in potting soil in 60 X 45 X 5-cm flats. The fiats were placed on benches in a greenhouse and watered daily. Flats were checked weekly and the proportion of germinated seeds (i.e., germination rate) was determined by counting the number of seedlings. Flats were checked for approximately 12 wk: most seeds germinated during the first 8 wk. Checking was terminated when no new seedlings were observed for 3 consecutive wk. All seeds were then unearthed to identify any seeds that had germinated but had not produced above-ground shoots.

For persimmon, three comparisons were conducted. Germination rates were compared among raccoon-ingested, coyote-ingested and uningested seeds. Rates were also compared between fruit-meal and meat-meal seeds from coyotes. Finally, rates were compared among mesocarp-protected, sheath-protected, unprotected seeds ingested by coyotes and uningested seeds. For American plum and pawpaw, germination rates were compared between seeds ingested by coyotes and uningested seeds. For hackberry, germination rates were compared between seeds ingested by raccoons and uningested seeds. Contingency-table analyses employing a chi-square statistic were used to test for differences in germination rates (Zar, 1984). When multi-way comparisons were significant, pairwise comparisons were conducted to determine which rates differed. A Yate's-correction-for-continuity of 0.5 was used in all 2 X 2 contingency table analyses (Zar, 1984). P values [less than or equal to] 0.05 were considered statistically significant.

RESULTS

Germination rates of persimmon seeds differed significantly ([[Chi].sup.2] = 27.15, 2 df, P [less than] 0.001) among raccoon-ingested (57.2%, n = 250), coyote-ingested (34.0%, n = 250) and uningested seeds (45.2%, n = 250). The rate for raccoon-ingested seeds was significantly higher than uningested seeds ([[Chi].sup.2] = 6.73, 1 df, P = 0.009), and the rate for uningested seeds was significantly higher than coyote-ingested seeds ([[Chi].sup.2] = 6.096, 1 dr, P = 0.014). Among persimmon seeds ingested by coyotes, the germination rate for fruit-meal seeds (34.0%, n = 250) was significantly higher ([[Chi].sup.2] = 8.97, 1 df, P = 0.003) than meat-meal seeds (21.5%, n = 246). Among fruit-meal seeds from coyotes, germination rates also differed significantly ([[Chi].sup.2] = 9.89, 3 df, P = 0.20) among mesocarp-protected (41.6%, n = 125), sheath-protected (49.6%, n = 125), unprotected (31.2%, n = 125) and uningested seeds (45.2%, n = 250). Germination rates for sheath-protected, uningested and mesocarp-protected seeds were not significantly different ([[Chi].sup.2] = 1.31, 2 df, P = 0.524), but the rate for mesocarp-protected seeds was significantly higher than unprotected seeds ([[Chi].sup.2] = 2.49, 1 df, P = 0.115).

Among the other tree species, the germination rate for uningested American plum seeds (29.2%, n = 250) was significantly higher ([[Chi].sup.2] = 20.07, 1 df, P [less than] 0.001) than the rate for coyote-ingested seeds (6.1%, n = 98). However, the germination rates for uningested (48.0%, n = 98) and coyote-ingested pawpaw seeds (41.5%, n = 65) were not significantly different ([[Chi].sup.2] = 0.42, 1 df, P = 0.519). The germination rate for uningested hackberry seeds (81.2%, n = 250) was significantly higher ([[Chi].sup.2] = 95.10, 1 df, P [less than] 0.001) than the rate for raccoon-ingested seeds (38.0%, n = 250).

DISCUSSION

Observed germination rates for persimmon seeds could reflect a coevolutionary relationship between persimmons and raccoons, and the absence of such a relationship between persimmons and coyotes. Persimmon primarily occurs in the deciduous forest of the eastern United States (U.S. Department of Agriculture, 1974). Raccoons occur throughout the range of persimmons and have done so historically (Kaufmann, 1982). This sympatry likely resulted in some degree of coevolution between these two species, which would explain the higher germination rates among raccoon-ingested seeds. Conversely, the historical range of coyotes was mostly allopatric with that of persimmons. Before the 1900s, coyotes primarily occurred in nonforested habitats west of the Mississippi River (Moore and Parker, 1992). Due to anthropogenic changes in habitat composition (e.g., clearing of forests) and carnivore communities (e.g., decreased abundance of gray wolves [Canis lupus]) in eastern North America associated with European settlement, coyotes began expanding their range eastward in the 1900s and currently occur throughout the range of persimmons (Moore and Parker, 1992). Thus, although coyotes feed on persimmons extensively (Willson, 1993), the duration of interactions between these two species may not have been sufficient (on an evolutionary scale) to accommodate any significant coevolution thereby resulting in the reduced germination rate among coyote-ingested persimmon seeds.

However, pair-wise coevolution between specific plants and animal dispersers is relatively rare (Mckey, 1975; Howe, 1986), particularly in North America where dispersal relationships are usually unspecialized (Willson, 1993). More likely, the higher germination rate of raccoon-ingested persimmon seeds compared to coyote-ingested seeds is a function of differences in foraging patterns between the two carnivores. Raccoon scats with persimmon seeds at CONWR rarely contained other food remains whereas coyote scats rarely consisted entirely of persimmons..its the proportion of fruit in the diet increases, gastrointestinal passage of food items is more rapid due to the laxative qualities in fruits (Murray et al., 1994). Shorter retention time in the gut reduces the exposure of seeds to gastrointestinal enzymes, potentially resulting in higher germination rates (Howe, 1986), whereas longer gut retention can reduce seed germination (Janzen, 1983; Murphy et al., 1993). Murray et al. (1994) reported that germination rates for seeds of Witheringia solanaceae increased as retention time in the gut decreased.

Similarly, the comparison of germination rates of seeds from fruit-meal and meat-meal scats of coyotes indicated that prolonged exposure to gastrointestinal enzymes reduces germination. A more rapid rate of gastrointestinal passage for fruit-meal seeds would have exposed seeds to gastrointestinal enzymes for a shorter time compared to that of seeds from meat-meal scats which probably passed through the gastrointestinal tract more slowly. Furthermore, the higher germination rates among mesocarp-protected and sheath-protected seeds compared to unprotected seeds constitutes additional evidence that exposure to gastrointestinal enzymes reduced germination. Undigested mesocarp and intact seed sheaths would have reduced the exposure of seeds to gastrointestinal enzymes. Persimmons at CONWR exhibited synchronous ripening (pers. obs.) resulting in a higher proportion of fruit in coyote diets (Cypher, 1991). This increased the occurrence of fruit-meal scats with undigested mesocarp and intact seed sheaths.

The higher germination rate of raccoon-ingested persimmon seeds compared to noningested seeds indicated that some exposure to gastrointestinal enzymes was beneficial. Scarification improves persimmon germination (U.S. Department of Agriculture, 1974). Thus, limited exposure to enzymes could help scarify seed coats and improve germination. Higher germination rates for ingested seeds compared to uningested seeds have been reported for seeds of numerous plants consumed by a diversity of frugivorous mammals (e.g., Krefting and Roe, 1949; Lieberman et al., 1979; Murray et al., 1994; Traveset and Willson, 1997).

Germination rates of American plum seeds were also reduced by gastrointestinal passage through coyotes. Coyote scats with plum seeds collected at CONWR always contained animal remains, and plum seeds rarely comprised [greater than]50% of scat contents. Also, undigested plum mesocarp was never observed in coyote scats. Thus, exposure of plum seeds to enzymes during gastrointestinal passage apparently was sufficient to reduce germination.

Germination of hackberry seeds was negatively affected by gastrointestinal passage through raccoons. This reduced germination rate was observed despite the fact that none of the raccoon scats with hackberry seeds contained animal remains. The relatively small size of hackberry seeds indicates that they are more adapted for dispersal by birds (van der Pijl, 1972).

Germination of pawpaw seeds was not affected by gastrointestinal passage through coyotes despite the fact that pawpaw seeds always occurred in scats consisting of [greater than]50% animal remains. Pawpaw seeds are relatively large and are well-adapted for dispersal by mammals (Willson, 1993). Pawpaw also possess certain characteristics (e.g., thicker seed coats) that render the seeds resistant to detrimental effects from the gastrointestinal enzymes of mammals. Seeds with thicker coats are more resistant to the scarifying action of gastrointestinal enzymes (Barnea et al., 1990; Izhaki et al., 1995).

Consumption and gastrointestinal passage is only one aspect of seed dispersal by animals. Thus, before determining whether or not a given plant-animal relationship is mutualistic other aspects of dispersal, as well as the consequences of nondispersal, need to be evaluated to fully understand the costs and benefits associated with dispersal by a particular animal species. Other potential benefits of dispersal include reduced seed predation, reduced competition with parents and siblings, reduced potential for inbreeding, deposition in a location more conducive to germination and/or growth and deposition in dung which may provide some protection from seed predators as well as nutrients for growth (Howe and Smallwood, 1982; Nadakavukaren and McCracken, 1985). Seeds of Aglaia flavida ingested by dwarf cassowaries (Casuarius bennetti) were deposited in favorable sites up slope from parent trees, thereby facilitating population expansion (Mack, 1995). Longer gut retention may reduce seed germination, but also results in larger seed shadows, particularly when far-ranging animals like coyotes are the disperser. Traveset and Willson (1997) concluded that movement of seeds away from the parent plant was the most important advantage provided by dispersers. Thus, even in situations where germination rates were reduced by gastrointestinal passage, the four tree species in this investigation still may derive benefits from dispersal of seeds by raccoons and coyotes.

Acknowledgments. - Support for field and laboratory work was provided by the Cooperative Wildlife Research Laboratory, Southern Illinois University at Carbondale, Greenhouse facilities were provided by the Department of Plant Biology, Southern Illinois University at Carbondale. Greenhouse assistance was provided by G. Gillooly. Helpful comments on the draft manuscript were provided by an anonymous reviewer.

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