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Functional Extinction of Birds Drives Rapid Evolutionary Changes in Seed Size

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Science  31 May 2013:
Vol. 340, Issue 6136, pp. 1086-1090
DOI: 10.1126/science.1233774

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The Birds and the Seeds

When species are lost from ecosystems through local extinction, the pattern of ecological interactions changes. Galetti et al. (p. 1086) show how the loss of large fruit-eating birds from tropical forest fragments in Brazil affects the reduction of seed size in a palm species. A data set was compiled that consisted of >9000 seeds measured in 22 populations over a large area of Atlantic rainforest, including seven areas where large-seed dispersers (toucans, cracids, and large cotingas) were extinct and 15 areas where they are still common.

Abstract

Local extinctions have cascading effects on ecosystem functions, yet little is known about the potential for the rapid evolutionary change of species in human-modified scenarios. We show that the functional extinction of large-gape seed dispersers in the Brazilian Atlantic forest is associated with the consistent reduction of the seed size of a keystone palm species. Among 22 palm populations, areas deprived of large avian frugivores for several decades present smaller seeds than nondefaunated forests, with negative consequences for palm regeneration. Coalescence and phenotypic selection models indicate that seed size reduction most likely occurred within the past 100 years, associated with human-driven fragmentation. The fast-paced defaunation of large vertebrates is most likely causing unprecedented changes in the evolutionary trajectories and community composition of tropical forests.

High rates of human-driven extinctions, estimated to be 100-fold greater than those of natural extinctions (1), have pervasive impacts on the functions and services of ecosystems (2, 3). Despite efforts to understand the immediate and cascading effects of the loss of species on the persistence of other species and biotic interactions (4, 5), little is known about the potential for rapid evolutionary changes in human-modified ecosystems. Rapid evolutionary changes have been shown in short-lived organisms, such as commercially exploited species, microorganisms, and perennial plants (68).

Here we document the rapid evolutionary reduction of seed size in a keystone palm, Euterpe edulis, across the Atlantic rainforest, subsequent to human-driven extensive deforestation (9). Seed size is an important trait, positively correlated with seed reserve amount, germination success, seedling size, and reproductive output (10). At the same time, seed size constrains the range of effective seed dispersers, because only large-bodied frugivores have gapes wide enough to consume large seeds (11).

Populations of large-gape frugivorous birds are directly threatened by hunting. They require extensive tracts of forest and hence are prone to local extinction in smaller forest fragments (12). These frugivores disperse several plant species over distances of several kilometers and eat large-seeded species that cannot be swallowed and successfully dispersed by smaller birds, which often are the only species resilient to large-scale disturbances (13). The functional loss of large frugivores, either by local extinction or by the severe reduction of population abundance (functional extinction), can affect natural regeneration by impairing the main components of the dispersal process: escape, colonization, and recruitment (14). With the functional extinction of large-gape birds, the fruit and seed traits of large-seeded plants might experience evolutionary changes within ecological time scales. We can expect shifts of the phenotypic selection regime and changes in the outcomes of selection after a substantial fraction of the selective agents (i.e., the large-gape frugivores) has been extirpated from their natural habitats.

We compared the seed size distributions of 22 palm populations in nondefaunated and defaunated areas of the two main physiognomic types (semideciduous and rainforest) in the Brazilian Atlantic forest (15) (Fig. 1). We found a consistent trend toward smaller seeds in defaunated forests (Fig. 1 and table S1). We classified an area as "defaunated" when large-gape frugivorous birds (those with a mean gape width >12 mm), such as toucans (Ramphastos dicolorus and R. vitelinus), toucanets (Pteroglossus aracari, P. bailloni, and Selenidera maculirostris), and large cotingas (Procnias nudicollis, Carpornis spp., and Pyroderus scutatus), are locally or functionally extinct (i.e., present with a very low abundance) (15) (fig. S1 and table S3).

Fig. 1 Geographic variation in seed size in palm populations.

Seed size (seed diameter in millimeters, x axis) frequency distributions (number of seeds, y axis) of 22 palm (E. edulis) populations in the remnants of the Brazilian Atlantic forest (green areas). The numbers refer to the population codes given in table S1. The red dots (codes 1 to 7) are defaunated sites, where large-gape frugivores are locally extinct or rare; the black dots are nondefaunated sites (codes 8 to 22). The vertical red line marks the upper size limit for successful dispersal by small birds (gape size 12 mm) in the absence of large-gape frugivores. The solid bars in the histograms indicate seed sizes below this threshold.

Toucans and large cotingas are the major large seed dispersers in nondefaunated forests (the average local richness of large frugivorous birds that disperse palm fruits is 11.9 species; tables S2 and S3). Small-gape thrushes are the most common seed dispersers remaining in defaunated forests, and the species richness of large frugivorous birds is reduced to 5.1 species (tables S2 and S3). A few mammal species very infrequently act as legitimate seed dispersers (table S2). Small-gape frugivores (<12 mm) represent 38% of the species in nondefaunated areas but 49% in defaunated forests (table S2). This distribution, in turn, results in 33% of the fruits being consumed by small-gape frugivores in nondefaunated areas and up to 98% of the fruits in the defaunated areas (table S4). Thus, there is ample potential for small-gape frugivores to have significant selective pressures on fruit traits in defaunated areas.

A nested analysis of variance revealed that variation in seed size is minimally accounted for by the forest physiognomic type (3.7%). In contrast, the defaunation status within each forest type accounted for more than 33.9% of the variance in seed size, with 0.1% accounted for by differences among sites. Most of the total variance in seed size (44.9%) was associated with individual palms within each site, with intra-individual variation (among-year variations and/or positional variation within the infructescence) representing 17.4% (overall nested analysis, F[1, 9195] = 909.8, P < 0.0001). These results demonstrate the marked geographic patterns in seed size potentially related to the local selective regime (the fruit selection process) driven by frugivores according to the defaunation status, with ample among-individual trait variance for natural selection to operate. Many environmental factors can influence seed size. Thus, we modeled seed size as a function of defaunation status and 13 other environmental variables, including climate, soil fertility, relief complexity, and forest cover (table S5). Although biotic variables failed to explain the variation in seed size, the model including defaunation status nested within forest type yielded the best fit to the observed data (table S5) (15). These results show that local variation in seed size is unrelated to any of the abiotic predictors or landscape variables but consistently relates to the defaunation status of each site.

The seeds of E. edulis are not successfully dispersed either when the fruits fall beneath the plant or when birds drop the fruits with the seeds still within the pulp. Seeds that remain with pulp are less likely to germinate (16), and fruits deposited beneath their parent palm usually experience high density-dependent mortality (17) (fig. S2E). The seeds dispersed by birds (defecated or regurgitated) collected in the field and from experiments with captive birds revealed that different bird species disperse seeds of different sizes [generalized linear model (GLM) χ2[6] = 94.1, P < 0.001; Fig. 2A]. The seeds dispersed by thrushes were consistently ≤12 mm in diameter, whereas large-gape birds, mainly toucans, dispersed a broader range of seed sizes (Fig. 2A). To corroborate these findings of fruit size selection with bird fruit choice, we estimated the probability of seed dispersal by birds as a function of seed size by recording the diameter of successfully dispersed seeds (regurgitated) and nondispersed seeds (fruits with beak marks) at four pristine and three defaunated sites. The dispersal probability was near zero for seeds >12 mm at all defaunated sites, which is significantly lower than the estimated probability for nondefaunated sites [binomial generalized additive model (GAM) χ2[1,20] = 40.3, P < 0.001; Fig. 2B]. Seeds wider than 12 mm represent approximately 32% of the overall seeds produced by E. edulis populations in nondefaunated forests. Our data show that defaunated areas have lost this large size range of the phenotypic seed size variation (Fig. 1), suggesting directional selection for reduced seed size of E. edulis at defaunated sites that contrasts with the stabilizing selection observed in nondefaunated sites (Fig. 2B and fig. S3).

Fig. 2 Patterns of fruit preferences by frugivorous birds and consequences for phenotypic selection on seed size.

(A) Seed size variation of the palm (E. edulis) fruits consumed by birds (from left to right): white-necked thrush (Ta, Turdus albicollis), bare-throated bellbird (Pn, Procnias nudicollis), rusty-margined guan (Ps, Penelope superciliaris), spot-billed toucanet and saffron toucanet (Sm, Selenidera maculirostris; Pb, Pteroglossus bailloni), and red-breasted and channel toucan (Rd, Ramphastos dicolorus; Rv, R. vitellinus). The boxes include the mean (horizontal black line), ± 1 SE (gray box), the 95% confidence interval (vertical lines), and outlier values (circles). (B) The probability of the dispersal of palm seeds as a function of seed diameter in defaunated forest sites (orange), where large-gape frugivorous birds are functionally extinct, and in nondefaunated forests (blue) [see (15)for the trends in local areas; fig. S3]. The vertical lines in the rugged plot indicate the individual seed sizes of undispersed and dispersed seeds.

Given that resilient small-gape frugivores (thrushes) only successfully disperse small seeds (≤12 mm), we tested the potential of such differential selection to generate the observed striking reductions in the seed size of E. edulis over time in defaunated areas (Fig. 1, panels 1 to 7). We used a simple evolutionary model based on the breeder's equation (18) to estimate the number of generations of selection on seed size needed to result in such a size difference between nondefaunated and defaunated forests (19, 20). Our simulations indicate that such an evolutionary change in the seed size of E. edulis populations would be possible in less than 100 years after a disturbance event (such as defaunation due to hunting or fragmentation) causing the functional loss of large frugivores (Fig. 3). Our estimates highlight the fact that a period of <75 years after a severe defaunation would be sufficient to cause the observed seed size reduction in palm populations in defaunated areas (Fig. 1). The documented extensive forest conversion to agriculture (mainly coffee) in semideciduous defaunated forests dates back to the 1800s (21, 22), which agrees with the results of our phenotypic selection model and indicates that the observed changes in seed size of E. edulis could have evolved very recently in relation to the remnant frugivore fauna (fig. S4). Thus, we argue that defaunation could have triggered the rapid evolutionary change of a phenotypic plant trait, resulting in a consistent size reduction of seeds in defaunated Atlantic forests.

Fig. 3 Simulated phenotypic trends in seed size after loss of major frugivores.

Expected trajectories over time, estimated from the phenotypic selection model, of the seed size reduction after defaunation in two Atlantic forest types (rainforest and semideciduous forest) (15). The vertical dashed lines with larger open dots denote the position along the mean trajectory when the predicted seed diameter is the closest to the present observed mean seed diameter in defaunated forests. The position where the dashed lines intercept the x axis represents the minimum time for the seeds to reach the present-day seed diameter mean value according to the model. Solid dots show the mean values (±1 SD) of the simulated seed size for consecutive years after defaunation.

From an ecological perspective, the reduction of seed size may have several negative consequences for plant recruitment and population dynamics (23). In E. edulis, it results in reductions in the total, shoot, and root biomasses of 1-year-old seedlings (24, 25). Our experiments indicate that the seed size reduction most likely resulted in the significantly increased vulnerability of E. edulis recalcitrant seeds to desiccation and decreased seedling size in both semideciduous forest and rainforest defaunated areas (15). Thus, seed size reduction may increase seed mortality in drier conditions and result in smaller seedlings, thereby tending to reduce the average fitness of the population. If regeneration becomes critically dependent on small seeds in defaunated areas, extended and intensified periods of drought induced by ongoing climate change, as predicted by climate models for South America (26), may be particularly harmful to the seedling establishment of this threatened palm species.

The seed size reduction documented here may be a generalized phenomenon in human-modified ecosystems where large frugivores that act as seed dispersers have been extinct for a long time. We thus foresee pervasive ecological and evolutionary effects of widespread vertebrate defaunation in tropical ecosystems. In particular, the rapid current defaunation in tropical forests will most likely result in unprecedented shifts of selection regimes on key life-history traits and in their evolutionary trajectories.

Supplementary Materials

www.sciencemag.org/cgi/content/full/340/6136/1086/DC1

Materials and Methods

Figs. S1 to S4

Tables S1 to S6

References (2761)

References and Notes

  1. The palmito or palm heart (E. edulis, Arecaceae) is a dominant palm species endemic to the Atlantic forest and dependent on birds for successful seed dispersal. It also occupies fragmented forest stands originated within the past 200 years since the establishment of extensive coffee plantations in São Paulo state (21, 22).
  2. Materials and methods are available as supplementary materials on Science Online.
  3. We estimated the heritability (h2) of seed size in E. edulis based on the variance of genetic relatedness between palms with available fruit phenotypic data (15). We used seed size data from genotyped individual palms in three populations, yielding h2 = 0.35 (15), and the previously reported value of 18.7 years for the generation time of the palm (20).
  4. The defaunated semideciduous forests are located in the heart of traditional coffee plantations in Brazil. For example, Rio Claro, a typical city in our defaunated region, had 65 coffee farms by 1855.
  5. Acknowledgments: We thank the Fundação de Amparo do Estado de São Paulo (BIOTA - FAPESP); Conselho Nacional de Desenvolvimento Científico (CNPq), (Excellence Grant-Junta Andalucía (to P.J.); and Programa Iberoamericano de Ciencia y Tecnología para el Desarollo (CYTED) for funding support. We thank J. Bascompte, R. Dirzo, D. Hansen, D. Levey, E. Bruna, D. Lapola, D. McCauley, M. A. Pizo, and three reviewers for useful comments and suggestions; T. A. Ferreira, E. Cazetta, M. J. Campos, D. Rother, G. Ambar, C. Dracxler, E. R. Castro, R. Laps, P. Develey, M. R. Francisco, and staff from PN Iguaçu for sending us palm seeds and data on frugivores; Fundação Florestal for allowing our study in the Protected Areas; and S. Nazareth and R. Brandolim for field and laboratory assistance. M.G. and P.R.G. receive a research fellowship from Conselho Nacional de Desenvolvimento Científico e Tecnológico. Data supporting this study are available in the DRYAD repository (http://dx.doi.org/10.5061/dryad.2pm42). Bird plates were done by Carl Buell.
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