The Effects of White Nosed Coatis Nasua narica on Seed Dispersal and Germination Success. Nada L. Wigand Department of Fisheries and Wildlife, University of Minnesota Twin Cities ____________________________________________________________ _______ ABSTRACT: Seed dispersal is an important part in ecosystem functions, yet little is known about the various animal dispersers Howe 1993. Coatis are opportunistic feeders and consume a wide variety of fruits. This study looked at the difference between ge rmination rates of those seeds passed through the digestive system of a coati and those that were never consumed. Twenty six Coati Nasua narica scats were collected in Monteverde, Puntarenas, Costa Rica and analyzed for types of seeds and various weight contents. Three types of seeds were found; Cecropia obtusifolia, Citharexylum.sp, and F icus tuerckheimii. It was found that coatis are good dispersers of some generalized seeds and bad dispersers for others more specific in dispersal requirements. For the more generalized species, like C. obtusifolia, the timing of germination was faster number of days, for those that have passed through the digestive tract of a coati, but have a lower germination rate overall. For those plant species more specialized in terms of dispersers, the coati can actually slow down the germination time. Therefore coatis can have a strong impact on plant communities and forest composition. RESUMEN: DispersiÃ³ n de semillas es un factor importante en la funciÃ³n de los ecosistemas, pero solamente un poco es conocido de los vario s dispersores animales. Howe 1993. Pizotes no son selectivos en lo que comen, tambiÃ©n comen una gran variedad d e frutas. Este estudio investigÃ³ si hay un a diferencia entre la taza de germinaciÃ³ n de las semillas que fueron comidas por los p izotes y las que no fueron comi dos. Veinte seis excrementos de los pizotes Nasua narica fueron colectados en Monteverde, Puntarenas, Costa Rica, y an alizados por los tipos de las semillas y pesos. Tres tipos de semillas fueron encontradas; Cecropia obtusifolia, Citharexylum sp. , and Ficus tuerckheimii. Los pizotes son dispersores buenos para las plantas generalizadas y dispersores malos para las plant as especializadas en sus mÃ©todos de disperso . Para las especies generalizadas como, Cecropia obtusifolia, el tiempo de primera germinaciÃ³n es mÃ¡ s rÃ¡pido para las semill as que pasaron por en un proporciÃ³n menor. Para las plantas especializadas , los pizotes pueden bajar la proporciÃ³n de las semillas que germinan. Por eso, los pizotes pueden tener un impacto muy fuerte en las comunidades del bosque . INTRODUCTION: Seed dispersal is a critical part of a plant 's reproductive biology MedellÃ n 1994. Plants show different seed dispersal mechanisms both abiotic and biotic reflecting their possible co evolution with their various dispersers Murray et al. 2000. There are many dispersal
mechanisms. Mammals are important dispersers for many prima ry forest species Haber et al. 2000, Wilson 1989. Vertebrates disperse seeds in three ways. The first is caching, where the animal buries or hides seeds for later consumption. Animals may also physically carry the seeds on their fur by barbs or hooks and involuntarily disperse these seeds. The third is the actual consumption of the fruits and seeds and the later passage through the digestive system of the animal Murray et al. 2000. Plants whose seeds are adapted for vertebrate stomachs provide rich rewa rds of carbohydrates and lipids for their animal dispersers Murray et al. 2000. These seeds are usually contained within a fruit of some kind that is attractive to the type of disperser they hope to attract Russell 1982. Depending on the type of disper ser plants are co evolved for, passage through the gut can impact germination success in different ways. Some plants' seeds require passage through the gut for scarification and later seed germination. For example, Guazuma ulmifolia and Cresentia data demonstrate this with their large mammal dispersers. Alternatively there are seeds that will have lowered germination success when passed through the gut, while others do not specifically require passage for germination Murray et al. 2000. The coati, Nas ua narica Procyonidae, is an opportunistic and highly omnivorous consumer eating whatever plant or animal material presently available de la Rosa and Nocke 2000. When fruit is abundant coatis feed almost exclusively on fruits Kaufmann 1983. However i n the wet season, when arthropod species are more available and abundant, they spend most of their time feeding on insects and supplement their diet with fruit Kaufmann 1983. Coatis time their reproductive season to when fruit is abundant in order for th eir offspring to benefit from this extra nutrient resource Smythe 1986. Coatis have been observed eating fruits like those of Dipteryx panamensis, Ficus. sp., Spondias mombin, and Scheelea zonensis Russell 1982. There are several important characterist ics involving coati seed dispersal; coatis often swallow fruits whole, because as carnivores they lack the crushing and grinding teeth like those of herbivores. They also lack complicated stomachs and digestive ceca, therefore seeds leave the gut relativel y intact and generally unharmed when passing through the digestive system Kaufmann 1983. Opportunistic frugivory may lead to inappropriate dispersers or inappropriate seeds being preyed upon. Frugivores or opportunistic carnivores often eat fruit that appear to have been evolved to attract other dispersers, which may result in poor dispersal Smythe 1986. Therefore coatis can be "good" dispersers or "bad" dispersers, depending on the plant. Good dispersers help the plant by dispersing seeds to favorabl e areas or by accelerating germination, while bad dispersers will retard or stop the germination entirely. This study was to determine how passage through the coati gut affects germination rates. I predict that seeds that have passed through the digestive system of the coati would be more likely to germinate and would have a faster germination rate than those of the same species that have not passed through the digestive system. Depending on what kind of seeds found, will determine if coatis are good disper sers or bad dispersers for each species. I hypothesized that for some seeds, coatis will accelerate the germination process and in others it will slow this process. Noting that coatis are very prominent members of the numerous life zones in the Monteverde, Puntarenas, Costa Rica area, it is important to understand and identify their importance as dispersers.
METHODS : This study was conducted in the height of the dry season during April and early May of 2001 in Monteverde, Puntarenas, Costa Rica. There were two study sites, one was located at the Finca EcolÃ³ gica and the other was located near th e compost pit beside the EstaciÃ³ n BiolÃ³ gica Monteverde EBM. The Finca EcolÃ³gica is located in Premontane Moist forest and the EstaciÃ³n BiolÃ³ gica is located in Lower Montane Wet forest Holdrige, 1967. Both locations are secondary growth forests. Coati scats were first located in the field at the Finca EcolÃ³gica or near the compost p it EBM. They were then processed and cleaned with water and then poured into soil separators to separate organic material from seeds. The seeds were then removed with the help of a dissecting scope, and placed in petri dishes lined with filter paper. Fif ty seeds were placed into each petri dish in rows of ten. The following seeds were found: Cecropia obtusifolia, Cecropiaceae n = 980, Citharexylum sp., Verbenaceae n = 75, and Ficus tuerckheimii, Moraceae n = 300. A piece of paper towel was the n placed over the seeds. The fungicide Orthocide 50WP, at a concentration of one gram per liter, was used to keep seeds free of mold and fungi. A solution of one gram per liter of water was made. The petri dishes were sprayed with the solution of fungicide and water, three times a day for 19 days. The seeds were then placed into a germination box 42.5 cm. in height, covered with plastic and screen, and then exposed to the sun. The seeds were then monitored every day for signs of germination, and then remo ved when these signs were observed. To test the germination rates of seeds not passed through the digestive tract of the coati, seeds from C. obtusifolia n = 270 and F. tuerckheimii n = 100 fruits were collected and used as controls. They were then placed into petri dishes in rows often with a total of fifty in each petri dish, and placed into the germination box. Citharexylum sp. was not located in the field. A total of five coati scats from the same locations were collected and placed into the dry box over night. They were then weighed using an electronic scale in grams +/ 0.001. They were cleaned with water and using soil sifters and then dried in the dry box overnight. The dif ferent components were separated into; insect parts, seeds, and organic material, then each portion was weighed using an electronic scale in grams +/ 0.001. RESULTS: A total of 26 coati scats were found and examined for seeds. Cecropia obtusifolia was t he most common species. Figure 1. Ficus sp. and Citharexylum sp. were also found in the scats but in lower abundance. The germination rates of C. obtusifolia found in scats were compared with those not passed through the digestive system of the coati Figure 2. Germination rates were faster for those seeds that had passed through the coati versus those that had not. A significant difference was found between t he germination rates for those seeds that had passed through the coati versus those that had not passed. Kolmogorov Smirnov p = 0.007, However; the overall germination rate i.e., the number of seeds germinating per day, were higher for those seeds not passed through the coati. Zero Ficus tuerckheimii seeds, both passed and not passed, germinated. Citharexylum sp. had an overall germination rate of 18%. According to figure 3, there is a higher average weight for seeds than insect parts, but a Kruskall Wallis test was used to test the difference in contents between the five scats
analyzed for weight and it was not significantly different p = 0.0935. As shown in Figure 3, the high standard deviation for weight of seeds can be explained by the unusually high amount of seeds found in scat number two more than 50% of total weight. Cecropia obtusifolia seeds were weighed to determine the amount of seeds in the average coati scat. Scat one contained 5,538 seeds, scat two contained 5,994 seeds, and scat three contained 422 seeds. Of the three scats that contained seeds, the average number of seeds was 3,98 5. The Standard Deviation of seeds found in the coati scats was 3,093. DISCUSSION: Germination was higher in C. obtusifolia that had passed through the coati but the numbers of germinations, i.e. the number of seeds germinating per day, were greater for th ose seeds not passed. Estrada et al. 1984 found that the viability of ingested seeds of C. obtusifolia are higher 57.6% Viability percentage for those consumed by Alouatta palliata than those of the control seeds that did not pass through the digestive system 0.5%. Chapman 1989 found that seeds passed through; Ateles geof froyi, Alouatta palliata, and Cebus capucinus, had a germination success rate of 60 percent. Cecropia obtusifo lia is a pioneer species that germinates in light gaps, and develops a fleshy infructescense with hundreds of small red seeds that are dispersed by birds and mammals Estrada et al. 1984. Cecropia obtusifolia does not have a specific co evolutionary dispe rser. Estrada et al. 1984. Cecropia obtusifolia has been observed, to be eaten by 48 different species of animals, including coatis Estrada et al. 1984. Being a generalist permits exploitation by both specialists and opportunistic frugivores Estrada e t al. 1984. Although being a generalist favors poor quality dispersal and unreliable dispersers, it insures that seeds will be more likely to be collectively dispersed over a larger area and are dispersed over many different germination sites Flehming 19 91, Howe 1993. This also ensures that many seeds will be deposited away from the parent tree and thus it will avoid density dependent seed mortality Howe and Smallwood 1982. Given its wide distribution range and its high abundance, Cecropia obtusifolia is described as a keystone species Medellin 1994. Ficus tuerckheimii is the most common species of fig in Monteverde Nadkarni et al. 2000 and its fruits are animal dispersed Haber et al. 2000. Figs fruit year round and are a reliable food source. Figs are also considered a keystone species Futuyama 1997. At the very end of the dry season, food is scarce, so opportunistic members of the feeding guild need to become even less selective. Koptur et al. 1988 shows that in April and May the fruit abundances are declining, because it is the end of the dry season, therefore only the few species that produce fruit all year round are available for frugivore consumption. None of the F. tuerckheimii, those passed or those not pas sed, germinated. Many rainforest trees do not always germinate rapidly when first planted Richards 1996, this could possibly be explained by the effects of seasonal germination. Garwood 1984 has shown that half of the seeds planted were dormant due to their seasonal timing mechanisms. Seasonal timing of germination increases the chances of seedling survival due to environmental stress avoidance i.e., flood, drought, or extreme insect abundance Garwood 1984. A germination rate of 18% for Citharexylum s p. shows that it is not suitable for vertebrate stomachs. It is commonly dispersed by more than 20 species of birds Haber et al.
2000; therefore the passage through a carnivorous digestive tract may do damage to the seeds themselves or slow down their germination rate. Even if seeds remain viable after passage through the digestive system, it is not guaranteed that these seeds will survive in order to germinate. Post dispersal seed mortality is an important aspect of seed dispersal Janzen 1986. If seeds are concentrate d in a small specific location they are more vulnerable to seed predators. Janzen 1986 found that seed predators like Liomys salvini; remove seeds from the scats of horses and cows, and either consume them right away or cache them in underground burrows, where they eventually die. Seeds removed by secondary seed dispersers influence the germination rates of those seeds found in the scats. Not taking these effects into account is liable to influence results. Chapman 1989 found that 51.8 percent of seeds found in the artificial dung piles created were removed by secondary dispersers, or killed by seed predators, within five days of initial placement. If these seeds do survive they will compete with each other for nutrients and light, thereby lowering fitne ss Janzen 1986. Zoologists have limited knowledge of seed dispersal, while plant ecologists have relatively little interest of the animals that disperse seeds Howe 1993. An integration of these two aspects in the scientific community would lead to bett er understanding of our own natural world. A better understanding of our natural world will lead to a better understanding of future needs in conservation efforts. ACKNOWLEDGMENTS: I want to thank God and the children for making this all possible. I couldn't do this without the fans, so this is for you. I wo uld like to thank Mauricio Garcia C. for ALL his help, patience, and humor through the duration of this study, I'll see you on " A Todo Dar". Thank you to the Finca EcolÃ³gica for allowing me to work on your property. Thank you to Rodrigo Solano for helping me identify seeds. Thanks to Andrew Rodstrom for all his timely and good humored supply runs. It was greatly appreciated. Thanks to Ali Deines for being the Diosa de espaÃ±ol and pseudoThundercat. Thank you to la EstaciÃ³n BiolÃ³ gica Monteverde.. I'd like to shout out to K pac Kay for the hardcore laughs no es facil cuando etoy fea, conoces?. Thank you to my family for always bein g there, I'll see you soon. LITERATURE CITED: Chapman, C. A. 1989. Primate Seed Dispersal: the Fate of Dispersed Seeds. Biotropica21: 148 154. de la Rosa, C. L., and Nocke, C. 2000. A Guide to the Carnivores of Central America. University of Texas Press. Austin, TX. pp. 77 89. Estrada, A., Coates Estrada R., and Vasquez Yanes. C. 1984. Observations on Fruiting and Dispersers of Cecropia obtusifolia at Los Tuxtlas, Mexico. Biotropica 16: 315 318. Fleming, T. H . 1991. Fruiting Plant Frugivore Mutualism: The Evolutionary Theatre and the Ecological Play. In: Plant and Animal Interactions; Evolutionary Ecology. In Tropics and Temperate Regions. Eds. P. W. Price, T. M. Lewinsohn, G. W. Fernandez , and W.W. Benson. John Wiley and Sons Inc. New York, New York. Pp. 119 144. Futuyma, D. J. 1997. In Meffe, G. and C. Ronald Corroll. 1997. Principles of Conservation Biology, 2 nd Ed. Sinauer Press; Sunderland MA.
Garwood, N. C. 1982. "Rhythm of Seed Germinat ion in Semi deciduous Tropical Forest." In: E.G. Leigh, A .S. Rand, and D. M. Windsor, eds. Ecology of a Tropical Rainforest, The Smithsonian Institution Press, Washington D.C., pp. 173 185. Haber, W. A., Zuchowski, W. and Bello, E. 2000. An Introduction to Cloud Forest Trees, Monteverde. Costa Rica. Second edition. Mountain Gem Publications.Monteverde, Puntarenas, Costa Rica. Holdridge, L. R. 1967. Life Zone Ecology. Tropical Science Center. San Jose, Costa Rica. Howe, H .F. 1993. Specialized and Generalized Dispersal Systems: Where Does "The Paradigm" Stand? Vegetation 107/108: 3 13. Howe, H. F. 1991. Seed Dispersal By Birds and Mammals; Implications for Seedling Demography. In: M. Hadley, and K. Bawa, Reproductive Ecology of Tropical Plants. UNESCO. Parthenon Publishing Company Inc. New Jersey, pp. 191 218. Howe, H. F. and Smallwood, J. 1982. Ecology of Seeds Dispersal. Annual Review of Ecological Systems. 13:201 228. Kaufmann, J. H.1983. Nasua narica coati. In: D. H. Janzen ed. Costa Rican Natural History. The University of Chicago Press, Chicago, IL, pp. 478 480. Kopture, S., Haber . A., Frankie, G. W., and Baker, H. G. 1988. Phenological Studies of Shrub and Treelet Species in Tropical Cloud Forests of Costa Rica. Journal of Tropical Ecology. 4: 323 346. Janzen, D. H. 1986. Mice, Big Mammals, and Seeds: It Matters Who Defecates Where. In: A. Estrada, and T. H. Flehming. Frugivores and Seed Dispersal. Dr. junk Publishers, Dordrecht. Medellin, R. A. 1994. Seed Dispersal of Cecropia obtusifolia by Two Species of Opossums in the Selva Lacandona, Chiapas, Mexico. Biotropica 26: 400 407. Murray, K. G., Kinsman, S., Bronstein, J. 2000. "Animal and Plant Interactions" In: pp. 256 263. N.M. Nadkarni and N. T. Wheelwright, eds. Monteverde: The Ecology and Conservation of a Tropical Cloud Forest. The Oxford University Press, New York. Nadkarni, N. M. and Wheelwright, N. T. eds. Monteverde Ecology and Conservation of a Tropical Cloud Forest. The Oxford University Press, New York. Russell, J. K. 1982. Timing of Reproduction by Coatis in Relation to Fluctuations in Food Resources. In: E.G. Leigh, A. S. Rand, and D. M. Windsor eds.. The Ecology of a Tropical Rainforest. The Smithsonian Institution Press, Washington D.C. pp. 413 431. Smythe, N. 1986. Competition and Resource Partitioning in the Guild of Neotropica l Terrestrial Frugivorous Mammals. Annual Review of Ecological Systems 17: 169 Wilson, M. F. Vertebrate Dispersal Syndromes in Some Australian and New Zealand Plant Communities, with Geographic Comparisons. Biotropica 21: 133 147.