Mammal Abundances and Seed Traits Control the Seed Dispersal and Predation Roles of Terrestrial Mammals in a Costa Rican Forest

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Mammal Abundances and Seed Traits Control the Seed Dispersal and Predation Roles of Terrestrial Mammals in a Costa Rican Forest BIOTROPICA 45(3): 333–342 2013 10.1111/btp.12014 Mammal Abundances and Seed Traits Control the Seed Dispersal and Predation Roles of Terrestrial Mammals in a Costa Rican Forest Erin K. Kuprewicz1 Department of Biology, University of Miami, 1301 Memorial Drive, Coral Gables, FL, 33146, U.S.A. ABSTRACT In Neotropical forests, mammals act as seed dispersers and predators. To prevent seed predation and promote dispersal, seeds exhibit physical or chemical defenses. Collared peccaries (Pecari tajacu) cannot eat some hard seeds, but can digest chemically defended seeds. Central American agoutis (Dasyprocta punctata) gnaw through hard-walled seeds, but cannot consume chemically defended seeds. The objectives of this study were to determine relative peccary and agouti abundances within a lowland forest in Costa Rica and to assess how these two mammals affect the survival of large seeds that have no defenses (Iriartea deltoidea, Socratea exorrhiza), physical defenses (Astrocaryum alatum, Dipteryx panamensis), or chemical defenses (Mucuna holtonii) against seed predators. Mammal abundances were deter- mined over 3 yrs from open-access motion-detecting camera trap photos. Using semi-permeable mammal exclosures and thread-marked seeds, predation and dispersal by mammals for each seed species were quantified. Abundances of peccaries were up to six times higher than those of agoutis over 3 yrs, but neither peccary nor agouti abundances differed across years. Seeds of A. alatum were predomi- nantly dispersed by peccaries, which did not eat A. alatum seeds, whereas non-defended and chemically defended seeds suffered high levels of predation, mostly by peccaries. Agoutis did not eat M. holtonii seeds. Peccaries and agoutis did not differ in the distances they dispersed seeds. This study shows that seed fates are contingent upon many factors such as seed defenses, frugivore–granivore abundances, and seed-handling capabilities. Mammal–seed interactions are complex; the outcomes of these interactions depend on the inherent characteristics of seeds and their potential dispersers. Abstract in Spanish is available in the online version of this article. Key words: agouti; anti-predation defenses; peccary; seed dispersal; seed predation. ANIMAL-MEDIATED SEED DISPERSAL IS A FUNDAMENTAL PROCESS THAT effects of terrestrial mammals on different plant life stages may CAN POTENTIALLY AFFECT seedling establishment, tree distributions, vary among mammal and plant species. Neotropical mammals and the maintenance and regeneration of forest ecosystems (For- differ in their abilities to consume and process fruits and seeds get 1996, Fragoso 1997, Peres & Baider 1997, Curran et al. 1999, due to differences in physiological characteristics such as Howe & Brown 2001, DeMattia et al. 2004). Vertebrates disperse jaw strength (Kiltie 1982), eating stance, or digestive physiology 70–90 percent of woody plant species in tropical forests (Fleming (Desbiez et al. 2009). et al. 1987). Among vertebrates, mammals act as major seed dis- Reciprocal selection pressures exist between seed-bearing persal agents. Terrestrial mammals may disperse seeds by trans- plants and granivores (Janzen 1980). Plants have evolved seed porting and depositing them either on the soil surface or by defenses to deter predation and to enhance seed dispersal. These burying them in subsurface caches (scatter-hoarding) (Vander protective strategies include physical defenses such as thick, hard Wall 1990). Dispersed seeds may germinate if they are deposited endocarps that serve as deterrents or barriers to seed consump- in suitable microhabitats by mammalian frugivores. Granivorous tion, and chemical defenses that render seeds toxic to seed preda- mammals, however, also consume and destroy many of the seeds tors (Kiltie 1982, Bodmer 1991, Kuprewicz & García-Robledo they encounter while foraging, acting as seed predators (Asquith 2010). Some mammals can circumvent seed defenses and con- et al. 1997, DeMattia et al. 2004, Jansen et al. 2004, Kuprewicz & sume seeds despite physical or chemical protection; however, gra- García-Robledo 2010). nivore species vary in their intrinsic abilities to cope with seed Although it is known that terrestrial mammals affect Neo- defenses (Janzen 1971). tropical trees positively, via dispersal and hoarding (e.g., Vander Disparity in relative local frugivore abundances is an extrin- Wall 1990, DeMattia et al. 2004), and negatively, through preda- sic factor that affects seed encounter rates by animals. Abun- tion, herbivory, and seedling trampling (Beck 2005), little is dances and distributions of terrestrial mammal species vary known about the actual net effects that mammals have on seed throughout Neotropical forests and this might affect seed fates survival. This scenario can be even more complex because the within these habitats. Habitat variation, fruiting tree phenologies, food resource patchiness, predator abundances, home range Received 13 April 2012; revision accepted 21 September 2012. requirements, and anthropogenic effects interact to produce 1Corresponding author: e-mail: [email protected] differences in terrestrial frugivorous mammal abundances within ª 2012 The Author(s) 333 Journal compilation ª 2012 by The Association for Tropical Biology and Conservation 334 Kuprewicz forests (Emmons 1984, Robinson & Redford 1986, Voss & This site receives approximately 4000 mm of rainfall per annum Emmons 1996). Understanding the roles large mammals play in with no distinct dry season (McDade et al. 1994). Hunting in and plant reproductive processes is essential because these animals habitat fragmentation of the areas surrounding La Selva have are detrimentally affected by deforestation and hunting by resulted in the local extinction of some large terrestrial mammals humans (Corlett & Hau 2000, Stoner et al. 2007). (e.g., white-lipped peccaries, Tayassu pecari). Seed dispersers vary in the distances they tend to move seeds (Willson & Traveset 1992). One qualitative measure of seed STUDY SPECIES.—Mammals: Collared peccaries (Pecari tajacu Linna- dispersal effectiveness (sensu Schupp 1993) is seed dispersal dis- eus, 1758; Tayassuidae, Cetartiodactyla) and Central American tance. Seeds benefit from long-distance dispersal by avoiding agoutis (Dasyprocta punctata Gray, 1842; Dasyproctidae, Rodentia) intense predation pressure near parent plants, decreasing potential are the most abundant terrestrial mammal frugivores within La competition with conspecifics, and possibly locating microhabitats Selva (Kuprewicz & García-Robledo 2010). Collared peccaries are favorable to seed germination (Howe & Smallwood 1982 and ref- large (up to 30 kg), terrestrial ungulates that consume fruits and erences therein). Terrestrial mammals vary in their likelihoods of seeds from numerous plant families (Beck 2005, 2006). Collared dispersing seeds and also in the distances they transport intact peccaries range throughout Central America and forage in herds seeds. Mammals that have large home ranges will tend to dis- of 2–50 individuals that travel over large home ranges (e.g., perse seeds farther than mammals that have small home ranges 118 ha in a Costa Rican dry forest, McCoy et al. 1990). Due to (Fragoso et al. 2003). their large body masses and herd sizes, peccaries can substantially In this study, I tested the following hypotheses: (1) seeds on modify natural habitats as they perturb soil, destroy seedlings, the forest floor are encountered first by peccaries rather than and consume seeds when foraging (Kiltie 1982, Beck 2005, agoutis; (2) more non-defended and chemically defended seeds 2006). As seed predators, peccaries play a significant role in seed exposed to peccaries would be destroyed when compared with survival to germination and subsequent seedling recruitment seeds exposed only to agoutis because peccaries can process toxic (Asquith et al. 1997). Peccaries cannot masticate or consume seeds via foregut fermentation (Elston et al. 2005). I hypothesized some seeds protected by thick-walled endocarps, but due to that more physically defended seeds would be destroyed by agou- pregastric fermentation, they can digest many chemically tis than by peccaries because agoutis can use their sharp incisors defended seeds (Kuprewicz & García-Robledo 2010). to gnaw through thick endocarps that collared peccaries cannot Central American agoutis are 3–4 kg terrestrial frugivorous crush. I also tested two alternate hypotheses concerning mammal rodents found throughout Central America (Reid 1997). Dasyproc- seed removal and dispersal kernels: (1) peccaries incidentally dis- ta punctata are frugivore-granivores that consume and disperse a perse seeds farther than agoutis because peccaries cover larger wide variety of seeds (Smythe 1978). Agoutis bury large seeds daily foraging ranges than agoutis; or (2) agoutis move seeds they singly in shallow caches beneath the soil for retrieval when fruit plan to hoard farther from sources than peccaries that inciden- is scarce and they may serve as the main seed dispersers for tally disperse seeds via expectoration; agoutis move hoarded some large-seeded tropical trees (Hallwachs 1986, Smythe 1986). seeds far from sources to escape intense seed predation pressure Agoutis can gnaw through thick-walled seeds, but they likely can- near the parent plant and to prevent kleptoparasitism of cached not consume chemically defended seeds (Kuprewicz & García- seeds by other granivores. Robledo 2010). Other potential medium large-bodied terrestrial mammal METHODS granivores
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