Seed preference in the Central American Agouti, Dasyprocta punctata

Kristen Coogan

Department of Wildlife and Conservation Biology, University of Rhode Island

ABSTRACT

Scatter-hoarding animals in the tropics typically depend on a cached supply of reserves when food is scarce. The Optimal Foraging Theory seeks to explain the behaviors these organisms exhibit upon prey selection. It is important for these scatter-hoarding animals to choose the most beneficial food item that will increase their energy intake. Central American agouties (Dasyprocta puncata) were presented with two differently sized seed species, the water apple (Syzygium malaccense) and the peach palm (Bactris gasipaes). A total of 400 flagged seeds were used, 200 of each species in groups of 20 seeds per species, over a 14 day period in Monteverde, Costa Rica. The seeds were collected and observed to determine seed fate. There was a significant difference in seed weight between the two species (T-test, p = <0.0001) and a significant difference between which species D. punctata chose to cache more ((2, p = <0.05), although there was no significant difference between which seed species D. punctata chose to eat (2, p=>0.05). Although D. punctata chose to cache more of the larger seed species, size and weight alone may not be the only measure for seed selection, therefore D. punctata may exhibit other selection processes in order to obtain its energy intake.

RESUMEN

Los animales dispersores y acaparadores tropicales dependen típicamente del suministro oculto de reservas cuando el alimento es escaso. La Teoría de Forrajeo Óptimo procura explicar las conductas que estos organismos exhiben en la selección de presa. Es importante para estos animales dispersores y acaparadores escoger el artículo de alimento más beneficioso que aumentará su toma de energía. Se presentaron dos especies de semillas de diferentes tamaños, la manzana de agua (Syzygium malaccense) y el pejibaye (Bactris gasipaes) a la guatusa centroamericana (Dasyprocta punctata). Se utilizó un total de 400 semillas marcadas; 200 de cada especie en grupos de 20 semillas por especie en un período de 14 días en Monteverde, Costa Rica. Las semillas se colectaron y fueron observadas para determinar el destino de cada una. Se encontró una diferencia significativa en el peso de las semillas entre las dos especies (prueba de t, p = <0.0001) y una diferencia significativa entre cuál especie D. punctata enterró más frecuentemente (2, P = <0.05). Sin embargo, no hubo diferencias significativas entre las especies que D. punctata prefirió consumir (2, P = >0.05). Aunque D. punctata escogiera enterrar más semillas de la especie más grande, el tamaño y el peso por si solos no pueden ser los únicos criterios para la selección de la semilla; por lo tanto, puede que D. punctata utilice otros procesos de selección para obtener su energía. INTRODUCTION

The goal of every organism in their lifetime is to survive and reproduce. Natural selection determines what phenotypes will be represented in future generations based on adaptation to selective pressures in the surrounding environments (Osborne 2000). Organisms must evaluate resource availability, foraging techniques, and survival probability in order to guarantee their survival and fitness. The Optimal Foraging Theory states that an organism will choose a feeding method that will maximize their net rate of energy intake. The net energy is measured as the amount of energy in the food minus the energy expended in finding, investing, and digesting it (Osborne 2000). The Optimal Foraging theory seeks to explain certain behaviors exhibited by organisms upon their diet selection. Selection of prey is made by evaluating both the positive and negative outcomes, and selection may be influenced by prey density, prey size, and nutrient content. Organisms will generally discriminate against food items which will not optimize their survival or fitness and choose those that will be most beneficial to them. Many animals hoard food from local abundance in order to conserve it for future use. In the case of a scatter-hoarding organism, small amounts of food are dispersed among many spatially spaced caches (Jansen et al. 2002). These individuals need to evaluate their food quality, in order to receive the highest net energy gain for the present time, as well as in the future when retrieving their cached reserves. It is beneficial for organisms which exhibit the scatter-hoarding strategy to manage a small supply of large seeds rather than a large supply of small, less nutritious seeds (Jansen et al. 2002). Seed fate is also important in determining the value of the food source. Scatter-hoarding animals typically eat few seeds while caching others. The seeds they store are presumably more valuable than the seeds they are consuming in order for them to be more beneficial in times of scarcity (Hallwachs 1994). The Central American Agouti, Dasyprocta punctata a scatter-hoarding organism. This species is a ground dwelling rodent, mostly active throughout the day, which can withstand disturbed habitats (Wainwright 2002). The diet of D. punctata consists mainly of fruits and seeds that are high in nutrients. Unlike the equally common seminivore- frugivore related species in the area, Agouti paca, D. punctata is unable to store fat. Their solution to seasonal scarcity is to bury seeds in times of plenty and dig them up later (Smythe 1978). Agoutis are therefore classified as a scatter hoarding rodent that usually caches a surplus of seeds in a dispersed pattern due to the uncertainty of retrieval (Smythe 1978). Seeds that have not been recovered have a possibility of germination, thereby also making D. punctata an important disperser for many plants. The aim of this study was to examine what preferences D. punctata exhibited for seed size. Smaller seeds were expected to be eaten due to their less nutritional value, while larger seeds were expected to be cached in order to benefit the agouti in times of scarcity.

METHODS

This experiment took place from April 23rd through May 7th, 2006 at the Santuario Ecológico located in Cerro Plano, Costa Rica, during the dry season (Fig. 1). The Santuario Ecológico is a secondary, lowland forest that was previously used for banana production and agouties are often observed foraging in a patch of open understory, approximately six meters by two meters in size. Two morphologically different tree seed species were used in choice experiments to determine whether D. punctata commonly took larger seeds over smaller seeds. The two species chosen for this study were Syzygium malaccense and Bactris gasipaes. The value of the seeds picked were placed under three categories based on their fate. The seed fate categories included being eaten, cached, or un-recovered. S. malaccense and B. gasipaes were purchased from a vegetable and fruit stand. The fruit was split with a knife; seeds were removed and then washed and dried. In order to locate the seeds in the field, each seed needed to be marked with flagging tape. Holes were carefully drilled in the center of every seed, and a meter of test nylon fishing line was threaded through the seed and tied. Twelve centimeters of flagging tape were then attached to the fishing line. Seeds were weighed in grams and then each tape was recorded with the seed number and weight. D. punctata bury the seeds not the flagging tape, so cached seeds were easily found. Previous studies have shown that marking seeds in this manner does not alter disperser behavior; however, this cannot be discounted completely (Jansen et al. 2002). Twenty seeds of each species were placed in two separate piles at the site, side by side (Fig. 2). Seeds were placed at 9 a.m. and checked the following morning at 8 a.m. The fates of the seeds were classified into one of the three categories, those being eaten, cached, or lost. Eaten seeds were those with the entire embryo consumed, or if the flagging tape and fishing line were removed from the seed. Cached seeds were those that were removed from the original site and buried shallowly in the nearby soil. Seeds whose flagging was not found were classified as lost. A new supply of seeds was then offered, ensuring that there were twenty of each seed species presented at all times. A t-test was used to determine weight difference in seed species. A Chi-squared test was also conducted in order to test if there was any significant difference in the fate of the seeds.

RESULTS

A total of 400 seeds were presented to D. punctata, 200 of each seed species. One- hundred and eighty one seeds were found and collected for data. Results of the S. malaccense seeds found, 148 seeds were eaten and 43 were cached. One-hundred and seventy-one of the B. gasipaes seeds were eaten, while 19 were cached (Table 1). The average weight for S. malaccense seeds was 10.78 g while the average weight for B. gasipaes seeds was 3.77 g (Fig. 3). An unpaired t-test showed that there was a significant difference in weight between the two chosen seed species (t = 15.70, p < 0.0001, df = 398). S. malaccense was the larger seed species used, while B. gasipaes was the smaller species. A Chi-squared test was used to determine if there were significant differences between the numbers of eaten or cached seeds between both species (Fig. 4). There was no significant difference in the number of seeds eaten between the S. malaccense and B. gasipaes (Chi-squared = 1.65, p >0.05, df = 1). Conversely, there was a significant difference in the numbers of cached seeds between the two species (Chi-squared = 9.2, p <0.05, df = 1). The Chi-squared test found that D. punctata did selectively cache the S. malaccense seeds more often than B. gasipaes. The unpaired t-test found that there was a significant size difference between the two seed species; S. malaccense being the larger of the two species. Therefore, this study showed that D. punctata selectively chose the larger seed species to cache over the smaller species. DISCUSSION

The original prediction of this experiment was that D. punctata would selectively choose the larger seed species over the small. The larger seed species, S. malaccense, was also expected, and is shown, to be cached at a higher frequency than the smaller seed species, B. gasipaes. There were a low number of seeds cached overall; most of the seeds in this study were eaten by the agouties. The high variation of seed weight in S. malaccense shows that size and weight cannot be a good measure for seed fate. If D. punctata chose to cache more S. malaccense seeds, or conversely, eat more B. gasipaes seeds than S. malaccense, there should be a reason other than size and weight upon food selection. The Optimal Foraging Theory predicts that predators choose a diet in order to maximize the net rate of energy intake. Food size is not the only factor that is important upon choosing prey. Nutritional values, as well as handling time and predator avoidance are also important. Predators need to evaluate their prey before consumption in order to receive the greatest energetic reward. D. punctata chose to eat both the large and small seed species showing that size and weight did not play a role upon deciding prey choice. If they chose the smaller species to eat as well, another important characteristic, such as nutritional value, could have influenced their decision. The larger species, S. malaccense, was generally light in weight, and had a green, soft inside. The smaller species, B. gasipaes, was denser and a good source of Vitamin A, starch, and protein (Zuchowski 2005). Also, as Wainwright (2002) states, palms are among the favorite food items of D. punctata, B. gasipaes being one of those palms. There is a possibility that B. gasipaes is more nutritionally valuable to the agoutis, thereby making the smaller seeds an important asset to their diet, as well as perhaps being more appealing in taste. Mixed diets can also be very beneficial to an individual, especially those that rely on plant material for energy and nutrients. First, an organism may accept a low quality food simply because, having encountered them, there may be more to gain in eating them than there would be in ignoring them. Second, a mixed diet is beneficial because different food types contain different nutrients, which may be important to the individual (Begon et al. 1990). A possible explanation as to why the agoutis did not cache more seeds overall could be due to the season in which this study took place. This study was conducted at the end of April and early May, during the dry season. Since fruits and seeds are usually scarce during the dry season, many scatter-hoarding animals that remain frugivorous throughout the year, such as agouties and their allied species, the acouchies (Myoprocta spp.), live off of cached reserves that they collected when fruits and seeds were plentiful, such as during the wet season (Forget et al. 2002). Studies done in Panama have shown that during times of food abundance, agouties hoard more seeds than what they consume, and when fruit begins to become scarce, they rely on those hoarded seeds (Forget et al.2002). In this case, the reason why the D. punctata did not scatter more seeds overall, could have been because the dry season is not normally when caching takes place, however, it is not known whether scatter-hoarding animals, such as D. punctata, show a triggered response in relation so seed fluctuations. If S. malaccense seeds are nutritionally less beneficial to D. punctata, then one may wonder why D. punctata would have hoarded the seeds away for a later time at all. The reason for caching any seeds could be to act as insurance. If fruiting numbers were significantly lower one year, or did not occur due to abiotic factors such as El Niño, there would be no resources for the agouties to consume; therefore, having insurance is important to ensure survival. The agouties may then have cached the less nutritious seeds (S. malaccense) as opposed to the more beneficial seeds merely to act as insurance. It is also not certain that D. punctata will recover all the seeds they cached. Thus, the agouties may eat the more nutritious seeds (B. gasipaes), as opposed to caching them in order to ensure they’ll receive the nutritional benefit instead of taking the chance of losing cached reserves. Studying caching behaviors is important in understanding the foraging strategies among many scatter-hoarding animals. Future studies should include differences between seasons and caching quantities. Differences in seed nutrition should also be considered. Seed preference may be better understood by picking similar seed types, such as those of two palm species.

ACKNOWLEDGEMENTS

I would like to thank Javier Méndez for his patience and guidance throughout this study, from the beginning to the end. Alan and Karen Masters, without them I would not have the supplies to conduct this study. I would like to thank Mireya Salazar Méndez at the Santuario Ecológico for letting me use the property. Last, but not least, I would like to thank Maria José and Ollie Hyman for helping all of my fellow students and me, in getting our needed materials together, and spending many hours helping us complete our projects.

LITERATURE CITED

Alcock, J. 1948. Animal Behavior: An Evolutionary Approach. Sinauer Associates, Inc. Saunderland, MA. Begon, M., J.L. Harper, C.R. Townsend. 1990. Ecology: Individuals, Populations, and Communities. Blackwell Scientific Publications, M.A. Brown, L. and J.F. Downhower 1951. Analysis in Behavioral Ecology. Sinauer Associates, Inc. Saunderland, MA. Forget, P.M., D.S. Hammond, T. Milleron, and R. Thomas. 2002. Seasonality of fruiting and food hoarding rodents in Neotropical forests: consequences for seed dispersal and seedling recruitment. In D.J. Levey, W.R. Silva, and M. Galetti, eds. Seed Dispersal and Frugivory: Ecology, Evolution and Conservation. CABI Publishing. Hallwachs, W. 1986. Agoutis (Dasyprocta punctata): The Inheritors of Guapinol (Hymenaea courbaril: Leguminosae). In A. Estrada and T.H. Fleming, eds. Frugivores and Seed Dispersal. Dr. W. Junk Publishers, Dordrecht. Jansen, P.A., M. Bartholomeus, F. Bongers, J.A. Elizinga, J. den Ouden, and S.E. Van Wieren 2002. The Role of Seed Dispersal by a Scatter-hoarding Rodent. In D.J. Levey, W.R. Silva, and M. Galetti, eds. Seed Dispersal and Frugivory: Ecology, Evolution and Conservation. CABI Publishing. Osbourne, Patrick L. 2000. Tropical Ecosystems and Ecological Concepts. Cambridge University Press, New York, NY. Smythe, N. 1978. The natural history of the Central American Agouti (Dasyprocta punctata). In D.H. Janzen (Ed).Costa Rican Natural History. University of Chicago Press, Chicago. Wainwright, M. 2002. The Natural History of Costa Rican Mammals. Distribuidores Zona Tropical, S.A. Zuchowski, Willow. 2005. A Guide to Tropical Plants of Costa Rica. Distribudores Zona Tropical, S.A. Table 1. Number of seeds eaten, cached, or lost from the study site by D. punctata for the two seed species: Syzygium malaccensis and Bractris gasipaes.

Seed Species Eaten Cached Lost S. malaccensis 148 43 9 B. gasipaes 171 19 10

Figure 1. Map of the Monteverde region in Costa Rica. Study site, Santuario Ecológico is highlighted. Figure 2. Study site in the Santuario Ecológico in Cerro Plano, Costa Rica. Study site was situated in an open understory area behind the Information Center. X’s mark the two piles of seed species.

18 16 14 12 10 8 6 4

Average Weight (grams) Average 2 0 S. malaccensis B. gasipaes Seed Species

Figure 3. Average weight of the two seed species used in this study; Syzygium malaccensis and Bactris gasipaes. Differences were significant (p < 0.0001). 180 160 140 120 100 S. malaccense 80 B. gasipaes 60

Number Number of Seeds 40 20 0 Eaten Cached Seed Fate

Figure 4. Fate of each seed, either cached or eaten, for both seed species: Syzygium malaccense and Bactris gasipaes. There was no significant difference for numbers of eaten seeds between the two species, but numbers of cached seeds between the seeds species were significantly different (2= 9.2, p < 0.05, df = 1).