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herbivore communities with top predators; at five sites on Barro Colorado Island (BCI), also a full ..... 455–468 in E. G. Leigh Jr., A. S. Rand, and D. M. Windsor,.
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Ecology, Vol. 78, No. 3

Ecology, 78(3), 1997, pp. 941–946 q 1997 by the Ecological Society of America

DOES MAMMAL COMMUNITY COMPOSITION CONTROL RECRUITMENT IN NEOTROPICAL FORESTS? EVIDENCE FROM PANAMA NIGEL M. ASQUITH,1,4 S. JOSEPH WRIGHT,2 1

AND

MARIA J. CLAUSS3

Department of Biological Sciences, University of Illinois, 845 W. Taylor Street, Chicago, Illinois 60607 USA 2Smithsonian Tropical Research Institute, Apartado 2072, Balboa, Ancon, Republic of Panama 3Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721 USA

Abstract. Patterns of seed predation, germination, and seedling herbivory were investigated in Panamanian forests. We hypothesized that seed and seedling survival would vary with differences in mammal community composition. We tested this hypothesis at five sites in mainland forests adjacent to Gatun Lake, full terrestrial mammalian granivore/ herbivore communities with top predators; at five sites on Barro Colorado Island (BCI), also a full mammalian granivore/herbivore community but without the two largest cats; at one site each on five medium-sized islands, with rats, agouti, rabbit, and paca present; and on five small islands that support rats only. Experiments were replicated for Dipteryx panamensis, Gustavia superba, and Virola nobilis, all of which have large seeds. To assess seed removal, seeds were placed in wire exclosure cages and nearby outside the cages. There was no difference in removal rates between forest types, with almost all unprotected seeds removed at all sites. To assess post-removal seed fate, seeds of Gustavia and Virola were attached to threads and placed on the forest floor. All threaded seeds were victims of predation on small islands, whereas 34, 43, and 77% of threaded seeds were dispersed and buried on BCI, medium islands, and the mainland, respectively. To assess seedling herbivory, half of the wire exclosure cages were removed after germination, and seedling survival was assessed after 13–14 mo. Protection from mammals increased seedling survivorship by more than sixfold on the smallest islands, by threefold on the medium islands, by twofold on the mainland, and by less than twofold on BCI. The absence of the two largest cats and the exclusion of poachers from BCI was associated with lower seedling herbivory and higher seed predation than observed on the mainland. In contrast, extreme mammal defaunation on the small and medium islands had large and consistent effects on seedling recruitment, including increased seed predation and increased seedling herbivory relative to sites with more intact mammal communities. Key words: Dipteryx panamensis; exclosure experiments; forest fragmentation; Gustavia superba; herbivory; islands; mammals; neotropical forests; Proechimys semispinosus; seedling recruitment; seed predation; Virola nobilis.

Ecologists have long debated the role of top-down and bottom-up forces in structuring biological communities (Hairston et al. 1960, Paine 1966). Although top-down effects have more often been observed in aquatic systems (e.g., Carpenter et al. 1985), recent studies have found equally strong top-down forces in terrestrial systems (e.g., McLaren and Peterson 1994). In some circumstances, top-down forces can have im-

Manuscript received 12 February 1996; revised 7 July 1996; accepted 13 July 1996; final version received 8 August 1996. 4 Present address: Department of Zoology, Duke University, Box 90325, Durham, North Carolina 27708-0325 USA, and Smithsonian Tropical Research Institute, Apartado 2072, Balboa, Ancon, Republic of Panama.

portant impacts on vegetation structure and species diversity (Brown and Heske 1990). Terborgh (1992) hypothesized that a top-down interaction may structure vegetation dynamics in neotropical forests. Predators such as jaguar and puma appear to regulate the population densities of mediumsized mammals, which in turn may limit seedling recruitment. Changes in mammal community composition may therefore have profound effects on tree species diversity (Terborgh 1992). Much of the evidence relating to this hypothesis comes from islands in Gatun Lake (Panama), isolated in 1913, which now lack components of a full mammal community. Barro Colorado Island (BCI), an island with neither jaguar nor puma resident, appears to support very high densities of some medium-sized mammals (Glanz

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TABLE 1. The terrestrial mammalian granivore/herbivore community and predators.

Spiny rat (Proechimys semispinosus) Agouti (Dasyprocta punctata) Rabbit (Sylvilagus brasiliensis) Paca (Agouti paca) Collared peccary (Pecari tajacu) Red-tailed squirrel (Sciurus granatensis) White-tailed deer (Odocoileus virginianus) Red brocket deer (Mazama americana) Tapir (Tapirus bairdii) Jaguarundi (Herpailurus yaguarundi) Ocelot (Leopardus pardalis) Margay (Leopardus wiedii) Jaguar (Panthera onca)† Puma (Puma concolor)

Mainland

BCI

x x x x x x x x x x x ? x ?

x x x x x x x x x x x x

Medium islands

Small islands

x x x x

x

Sources: Glanz 1982, 1990, 1991, Adler and Seamon 1991. † Jaguars are known to visit BCI frequently (S. J. Wright, personal observations).

1982, 1991; but see Wright et al. 1994 for an alternative view). DeSteven and Putz (1984) and Sork (1987) found that seed predation was much higher and seedling survival much lower on BCI than on the adjacent mainland (but cf. Terborgh and Wright 1994). Other islands in Gatun Lake are too small (,1.2 ha) to support any terrestrial mammals and are now dominated by a restricted subset of tree species (Leigh et al. 1993). Leigh et al. (1993) postulate that two factors have been of critical importance in the reduction of tree species diversity from small islands in Gatun Lake. Seeds that require burial by agouti (Dasyprocta punctata) to escape insect predation are unable to germinate on small islands (see also Forget 1990). The wind-influenced island microclimate then favors the seedlings of other species, such as the large-seeded Protium panamense (Leigh et al. 1993). As an alternative mechanism, Terborgh (1992) suggests that as medium-sized mammals are absent from small islands, large-seeded tree species can escape predation and are subsequently able to outcompete other species. In this paper we compare rates of seed predation, germination, and seedling herbivory in Panamanian forests with different mammal communities. We experimentally examine factors that influence early mortality of three large-seeded tree species and test two specific predictions: (1) predation of large seeds is low on small islands, allowing escape of large-seeded tree species; (2) germination rates are low on small islands. We then discuss the mechanisms that appear to have caused the loss of tree species diversity from small Gatun Lake islands, and evaluate the hypothesis of mammalian control of neotropical forest dynamics (Terborgh 1992).

Study sites The islands and peninsulas surrounding Gatun Lake are covered by tropical moist forest. Early aerial pho-

tographs suggest that many Gatun Lake islands have been forested since isolation (Leigh et al. 1993). Annual rainfall on BCI (98109 N, 798519 W) is 2600 mm, with a 4-mo dry season beginning in December. We conducted experiments in four forest types around Gatun Lake: five sites in mainland forests adjacent to the lake, five sites on BCI (1600 ha), and one site each on five medium-sized islands (15–80 ha) and five small islands (,2 ha). All experimental sites were within 1 km of BCI, except for four of the medium islands, which were 4–5 km distant. Further details of the forest types are given in Leigh et al. (1982, 1993), Wright (1985), and Adler and Seamon (1991). Our small islands were islands 43, 44, 46, 48, and 49 in Adler and Seamon (1991). All granivorous and herbivorous mammals .1 kg in body mass found on the mainland are also present on BCI. The terrestrial mammalian granivore/herbivore community in each of the different forest types is shown in Table 1. Mainland forests and four medium islands are subject to limited poaching, while BCI, one medium island, and the small islands are not (Glanz 1991, S. J. Wright, personal observation).

Tree species We investigated three native tree species. Dipteryx panamensis (Pitt.) Rec. & Mell (Leguminosae) is a common, large (40–50 m) canopy tree. Its drupes have a thin exocarp, and a hard thick-walled endocarp that encloses a single, large (4 cm) seed (DeSteven and Putz 1984). Gustavia superba (H.B.K.) Berg. (Lecythidaceae) is a small (typical dbh 10–15 cm) pioneer tree, common in the understory of secondary forest on BCI. Its large fruits (150–600 g) contain 5–50 seeds, each weighing 3–15 g (Sork 1987). Virola nobilis A. C. Smith (Myristicaceae) is a dioecious canopy tree. A fibrous capsule dehisces to expose a gray seed (2 3

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1.5 cm) enclosed by a red 1 mm thick aril (Howe 1993). Primary dispersal of V. nobilis seeds is by birds and mammals (Howe 1993), D. panamensis seeds by bats (Bonnacorso et al. 1980), and G. superba fruits by gravity (Sork 1987). Seeds of all three species are consumed by mammalian granivores and may be secondarily dispersed and buried by scatterhoarding agouti (Dasyprocta punctata) (Forget and Milleron 1991, Forget 1992, 1993).

Methods Five experimental sites were randomly located in each of the four forest types. Each site was within 50 m of the lake because more distant sites were unavailable on small islands. During the 1st wk of March 1993, we placed arrays of 10 intact and apparently viable ripe D. panamensis seeds in four wire exclosure cages at each site. The cages were constructed of galvanized wirecloth and were 1 m tall by 0.7 m diameter. They were open at the top and their bases were staked firmly to the soil to prevent passage of small mammals underneath. Although climbing mammals and large mammals such as deer had access through the open tops, Terborgh and Wright (1994) showed the loss of D. panamensis seeds from similar exclosure cages to be ,10% (see also the results of this study). We thus consider seed loss to mammals from within the cages to be minimal. For each wire exclosure, a corresponding array of 10 seeds was placed unprotected on the forest floor. The location of the unprotected array was marked with a stake, 2–3 m from the caged array. Each seed was within 0.3 m of the stake. We repeated the procedure with arrays of eight ripe G. superba seeds during the 1st wk of July 1993 and arrays of eight ripe V. nobilis seeds during the 1st wk of August 1993. The number of seeds in each array mimicked the densities that might result from primary dispersal away from the parent tree. At the time that seeds of each species were set out in the field, 100 seeds were also placed in a screen growing-house on Barro Colorado Island. When 90% of the growinghouse seeds had germinated and seedlings were no longer dependent on endosperm, removal from the experimental arrays was assessed. Seedlings and intact seeds remaining were counted in June 1993 (D. panamensis) and October 1993 (G. superba and V. nobilis). The replicate exclosures and controls were pooled for each site and species. As many groups showed no variance, the proportions of seeds remaining were ranked before analysis by ANOVA (Conover and Iman 1981). To assess the fate of removed seeds, individual G. superba and V. nobilis seeds were threaded with 60 cm long lengths of cotton thread and placed on the forest floor (Forget and Milleron 1991). Two arrays of eight seeds of each species were set out at each site, ø2 wk

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after the first experiment was initiated, and within 10 m of the original sites. After 7 d, threads were relocated by searching within a 5 m radius of the site. If the thread was relocated with the seed still attached and it had been moved and/or buried, secondary dispersal was indicated. If the thread alone was recovered, we assumed that the seed had been predated. We tested this assumption by attaching similar threads to Astrocaryum standleyanum seeds, which unlike G. superba and V. nobilis have an inedible endocarp. Almost 80% (23) of the threads from which the A. standleyanum seed had been removed (n 5 29) were within a few centimeters of an opened, predated endocarp. The fates of the G. superba and V. nobilis seeds were pooled by forest type and subjected to three-way log-linear contingency analysis, with the main effects being tree species, forest type, and seed fate. Seeds that had not been removed and still remained in situ, and those for which neither seed nor thread were recovered, were excluded from the analysis. To assess germination success in the absence of mammals, after 90% of seeds in the growing-house had germinated, we recorded the proportion of seeds that had germinated in each exclosure, pooled values for each site and species, and analyzed the arcsine-transformed data by ANOVA. After the seed removal and germination experiments had been completed (June 1993 D. panamensis; October 1993 G. superba and V. nobilis) we removed half of the wire exclosure cages at each site. This resulted in two groups of seedlings protected from mammalian herbivores, and two unprotected groups at each site. The difference between seedling mortality inside and outside the cages provided an indicator of rates of mammalian herbivory. The proportions of surviving seedlings after 13–14 mo were pooled by treatment, site, and species and arcsine-transformed before analysis by ANOVA. Sites at which no seeds survived to the seedling stage were excluded from analysis, as was one site where the wire cages had disappeared.

Results The proportion of intact seeds and seedlings after 90% of growing-house seeds had germinated are presented in Table 2a. While many protected seeds remained in situ, almost all unprotected seeds were removed at all sites (F 5 865.0, df 5 1, 96, P , 0.001). There was no difference in removal rates between forest types (F 5 2.41, df 5 3, 96, P 5 0.071). However, there were significant differences in the fates of removed seeds among forest types (G 5 66.1, df 5 6, P , 0.01) (Table 2b). On small islands there was no evidence that any removed seeds had been dispersed. On BCI and medium islands, 34% and 43% of the

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TABLE 2. Fate of seeds/seedlings. a) Proportion of intact seeds/seedlings after 90% of growing house seeds germinated (V. nobilis after 3 mo, G. superba and D. panamensis after 4 mo). Mainland BCI Medium islands Small islands

D. panamensis G. superba V. nobilis

Protected

Open

Protected

Open

Protected

Open

Protected

Open

0.89 0.88 0.72

0.01 0.02 0.00

0.74 0.99 0.32

0.00 0.00 0.00

0.78 0.98 0.69

0.01 0.00 0.00

0.46 0.96 0.45

0.00 0.16 0.00

b) Fate of removed seeds after 1 wk (proportions). Mainland

G. superba V. nobilis

BCI

Medium islands

Small islands

Eaten

Dispersed

n

Eaten

Dispersed

n

Eaten

Dispersed

n

Eaten

Dispersed

n

0.18 0.29

0.82 0.71

33 35

0.70 0.63

0.30 0.37

46 32

0.53 0.62

0.47 0.38

38 45

1.00 1.00

0.00 0.00

2 28

c) Fate of seeds protected from mammals (proportion surviving to the seedling stage). Mainland BCI Medium islands

D. panamensis G. superba V. nobilis

0.64 0.79 0.64

0.55 0.98 0.23

d) Proportion of seedlings surviving to 13–14 mo. Mainland

D. panamensis G. superba V. nobilis

Protected 0.37 0.81 0.35

Open

Protected

0.19 0.41 0.00

0.30 0.96 0.09

BCI

0.23 0.90 0.11

Medium islands

Open

Protected

0.23 0.57 0.00

0.41 0.98 0.76

removed seeds were dispersed before being buried. On the mainland 77% were dispersed. There were significant differences in germination success between species (F 5 57.52, df 5 2, 48, P , 0.001) and between forest types (F 5 9.25, df 5 3, 48, P , 0.001) (Table 2c), but the species 3 forest type interaction was also significant (F 5 3.73, df 5 6, 48, P 5 0.004). We tested the following post-hoc comparisons within each species using a Bonferroni-adjusted significance level of P 5 0.006: small islands vs. other sites; medium islands vs. BCI and mainland sites; and BCI vs. mainland sites. Most G. superba germinated in all forest types (no post-hoc comparisons significantly different). D. panamensis had moderate germination at mainland sites and on BCI and medium islands, and very low germination on small islands (small islands vs. other sites, F 5 14.0, df 5 1, 48, P , 0.001; other comparisons not significant). V. nobilis had very low germination on both small islands and BCI (small islands vs. other sites, F 5 15.2, df 5 1, 48, P , 0.001; medium islands vs. BCI and mainland sites, not significant; and BCI vs. mainland sites, F 5 12.14, df 5 1, 48, P 5 0.001). Protection from mammalian herbivores increased survivorship in all forest types (F 5 95.6, df 5 1, 80,

Small islands

0.62 0.98 0.54

Small islands

Open

Protected

Open

0.13 0.28 0.00

0.25 1.00 0.28

0.00 0.15 0.00

P , 0.001) (Table 2d). The species effect was significant (F 5 59.39, df 5 2, 80, P , 0.001) but total survivorship did not differ significantly between forest types (F 5 2.46, df 5 3, 80, P 5 0.069). The species 3 treatment interaction was significant ( F 5 8.21, df 5 2, 80, P 5 0.001), because although moderate numbers of unprotected D. panamensis and G. superba seedlings survived, no unprotected V. nobilis did. The forest type 3 treatment interaction was also significant (F 5 5.02, df 5 3, 80, P 5 0.003). Protection from mammalian herbivores increased D. panamensis and G. superba seedling survivorship by less than twofold on BCI, by twofold on the mainland, by threefold on the medium islands and by more than sixfold on the smallest islands. Discussion Germination of protected seeds and 1-yr survivorship of protected seedlings were similar for medium islands, BCI, and the mainland (Table 2c and d). Physical differences among these three forest types were unimportant in the early stages of tree regeneration. In contrast, the germination of protected seeds of both D. panamensis and V. nobilis was reduced on the small islands (Table 2c). This effect was limited to the es-

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tablishment phase when seedlings were still dependent on seed reserves. Protected seedlings of all three species survived equally well in all forest types (Table 2d). Low rates of germination on the small islands is probably a consequence of their desiccating physical environment. Microclimate thus appears to play a critical role in regulating small-island tree recruitment (Leigh et al. 1993). Mammals influenced the regeneration of the three tree species in all four forest types. Unlike Sork (1987), who found rates of seed removal (of G. superba) to differ between BCI and the nearby Gigante peninsula, we found no such differences between BCI and mainland sites. Rather, seed removal was virtually complete in all forests, despite the radical differences in mammal community composition (Table 2a). On small islands, all of the removed seeds were predated (Table 2a and b), and mortality due to mammalian seedling herbivory was also extraordinarily high (Table 2d). The one resident terrestrial mammal species ( Proechimys semispinosus) maintained extremely high densities on these islands (up to 58 individuals/ha on a nearby 1.8-ha island; Adler, in press). The highest levels of seed and seedling predation occurred on the smallest islands in the absence of mammals .1 kg body mass. The second largest impact of mammals occurred on the medium islands. Here, 57% of V. nobilis and G. superba seeds removed by terrestrial mammals were predated (Table 2b), and 1-yr survivorship of unprotected seedlings of D. panamensis and G. superba was lower than for BCI and the mainland (Table 2d). As the mammal communities in these forests were simplified, both seed predation and the loss of seedlings to browsers increased. Predatory mammals and browsing mammals .1 kg body mass have also been largely extirpated at Los Tuxtlas, Mexico (Dirzo and Miranda 1991). The effects on tree regeneration have, however, been nearly the opposite of those observed on small and medium Gatun Lake islands. Early regeneration has been enhanced at Los Tuxtlas, and dense monospecific carpets of seedlings cover the forest floor (Dirzo and Miranda 1991). Pit vipers (Bothrops spp.) occur at extremely high densities at Los Tuxtlas and consume small rodents (PerezHigarda 1978; H. Greene, personal communication). This may check small-rodent populations and permit the development of dense seedling carpets. Interestingly, similar monospecific seedling stands occasionally cover the forest floor of small Gatun Lake islands. Such occurrences appear to coincide with periods of low spiny rat densities (G. H. Adler, personal communication). It is clear that extreme mammal defaunation alters seedling regeneration. The contrast between Los Tuxtlas and the small Gatun Lake islands indicates

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that both the magnitude and the direction of such effects are contingent on the biota involved. The results of more limited changes in mammal community composition are even less predictable. Although the composition of the terrestrial mammalian herbivore/granivore community is the same on BCI and the adjacent mainland, predation pressure is different. Jaguar and puma are resident only on the mainland, and in addition, poachers are wholly excluded from BCI. The consequences for tree regeneration varied with life history stage, survivorship of unprotected seeds being greater on the mainland (Table 2b), and 1-yr survivorship of unprotected seedlings being greater on BCI (Table 2d). In an earlier comparison of BCI and Manu, Peru, mammal exclosures had dramatic and quantitatively similar effects on seedling recruitment and survivorship, despite apparent differences in the population densities of most mammal species (Terborgh and Wright 1994). In contrast to the effects of the complete extirpation of mammals, the relatively subtle differences in mammal population densities attributable to cats and limited poaching have no clear effects on plant regeneration. However, the loss of certain critical mammal species can cause important top-down changes in plant recruitment (Brown and Heske 1990, McLaren and Peterson 1994). Almost complete loss of terrestrial mammals from Panamanian forests released the one remaining mammal species (Proechimys semispinosus) from competition and predation, allowing it to prevent regeneration of three large-seeded tree species. An intermediate reduction in mammal community diversity also reduced recruitment of these tree species. In a Mexican forest, similar reductions in the mammal community had equally significant but opposite effects on seedling recruitment. Poachers and habitat fragmentation are currently affecting mammal communities throughout the Neotropics (Redford 1992). These human-induced changes in top-down processes may well have profound effects on patterns of forest regeneration. ACKNOWLEDGMENTS We thank Henry Howe, Joel Brown, Bruce Patterson, Frances White, and David Mertz for assistance and advice, and John Terborgh, Greg Adler, Pierre-Michel Forget and two reviewers for improving the manuscript. N. Asquith was supported by a Smithsonian Graduate Fellowship. LITERATURE CITED Adler, G. H. In press. The island syndrome in isolated populations of a tropical forest rodent. Oecologia. Adler, G. H., and J. O. Seamon. 1991. Distribution and abundance of a tropical rodent, the spiny rat, on islands in Panama. Journal of Tropical Ecology 7:349–360. Bonaccorso, F. J., W. E. Glanz, and C. M. Sandford. 1980. Feeding assemblages of mammals at fruiting Dipteryx panamensis (Papilionaceae) trees in Panama: seed predation,

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