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The Reconfiguration of Seed-Dispersal Interactions After Megafaunal Extinction

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The Reconfiguration of Seed-Dispersal Interactions After Megafaunal Extinction View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Biblioteca Digital da Produção Intelectual da Universidade de São Paulo (BDPI/USP) Universidade de São Paulo Biblioteca Digital da Produção Intelectual - BDPI Departamento de Ecologia - IB/BIE Artigos e Materiais de Revistas Científicas - IB/BIE 2014-05 Reconstructing past ecological networks: the reconfiguration of seed-dispersal interactions after megafaunal extinction Oecologia, Heidelberg, v.175, n.4, p.1247-1256, 2014 http://www.producao.usp.br/handle/BDPI/45245 Downloaded from: Biblioteca Digital da Produção Intelectual - BDPI, Universidade de São Paulo Oecologia (2014) 175:1247–1256 DOI 10.1007/s00442-014-2971-1 PLANT-MICROBE-ANIMAL INTERACTIONS - ORIGINAL RESEARCH Reconstructing past ecological networks: the reconfiguration of seed‑dispersal interactions after megafaunal extinction Mathias M. Pires · Mauro Galetti · Camila I. Donatti · Marco A. Pizo · Rodolfo Dirzo · Paulo R. Guimarães Jr. Received: 16 December 2013 / Accepted: 9 May 2014 / Published online: 28 May 2014 © Springer-Verlag Berlin Heidelberg 2014 Abstract The late Quaternary megafaunal extinction extinction and the arrival of humans changed how seed impacted ecological communities worldwide, and affected dispersers were distributed among network modules. How- key ecological processes such as seed dispersal. The traits ever, the recent introduction of livestock into the seed- of several species of large-seeded plants are thought to have dispersal system partially restored the original network evolved in response to interactions with extinct megafauna, organization by strengthening the modular configuration. but how these extinctions affected the organization of inter- Moreover, after megafaunal extinctions, introduced species actions in seed-dispersal systems is poorly understood. and some smaller native mammals became key components Here, we combined ecological and paleontological data for the structure of the seed-dispersal network. We hypoth- and network analyses to investigate how the structure of esize that such changes in network structure affected both a species-rich seed-dispersal network could have changed animal and plant assemblages, potentially contributing to from the Pleistocene to the present and examine the pos- the shaping of modern ecological communities. The ongo- sible consequences of such changes. Our results indicate ing extinction of key large vertebrates will lead to a variety that the seed-dispersal network was organized into modules of context-dependent rearranged ecological networks, most across the different time periods but has been reconfigured certainly affecting ecological and evolutionary processes. in different ways over time. The episode of megafaunal Keywords Ecological networks · Frugivory · Modularity · Mutualisms · Pantanal · Rewilding Communicated by Candace Galen. Electronic supplementary material The online version of this Introduction article (doi:10.1007/s00442-014-2971-1) contains supplementary material, which is available to authorized users. The species in a community form a network of interac- M. M. Pires (*) · P. R. Guimarães Jr. tions whose structure has implications for the ecological Departamento de Ecologia, Instituto de Biociências, Universidade and evolutionary dynamics of the populations (May 1972; de São Paulo, 11294, São Paulo, SP 05508-900, Brazil Pimm 2002; Dunne 2006; Bascompte and Jordano 2007). e-mail: [email protected] Although snapshots in time are required to assess the struc- M. Galetti ture of the community, ecological communities are con- Departamento de Ecologia, Universidade Estadual Paulista, Rio stantly losing and gaining species through extinctions and Claro, SP 13506-900, Brazil invasions, thus network structure is continuously changing C. I. Donatti · R. Dirzo (Petanidou et al. 2008). Insight into how changes in spe- Department of Biology, Stanford University, Stanford, CA 94305, cies composition induce changes in the structure of eco- USA logical networks has been provided by studies focusing on the consequences of extinctions and the impact of species M. A. Pizo Departamento de Zoologia, Universidade Estadual Paulista, Rio invasions (Memmott et al. 2004; Vilà et al. 2009). Extinc- Claro, SP 13506-900, Brazil tion simulations have shown that food webs and mutualistic 1 3 1248 Oecologia (2014) 175:1247–1256 networks can be highly robust to extinctions (Dunne et al. and removal simulations of extinct Pleistocene mammals, 2002; Memmott et al. 2004). Similarly, studies on the humans, and livestock in one of the most diverse seed-dis- effects of species invasions and on the spatial and temporal persal networks recorded to date, which includes species reconfigurations of ecological networks, in which species from major taxonomic groups of seed dispersers—mam- were both lost and gained over time, agree that the overall mals, birds, fish and reptiles—and the plants they interact structure of networks is robust to changes in species com- with in the Pantanal (Donatti et al. 2011). First we com- position (Olesen et al. 2008; Petanidou et al. 2008; Vilà piled, from the literature, a list of mammalian megafauna et al. 2009). Nonetheless, when a considerable number of likely to occur in the Pantanal during the Pleistocene. Sec- species is lost, because of changes in distribution or extinc- ond, we combined data on the feeding ecology of Pleis- tions, major changes in network structure and consequently tocene megafauna (e.g., MacFadden and Shockey 1997; in network dynamics are expected. MacFadden 2000) and information on plant traits and seed- The disruption of ecological networks is a possible out- dispersal anachronisms (Guimarães et al. 2008) to outline come of large extinction events in which many species and the putative interactions among the extinct megafauna and their interactions are removed from the community within a fleshy fruited plants. Finally, we built a potential network relatively short time when compared to background extinc- time series from the end of the Pleistocene to the present tions. A representative example of a drastic change in com- day and used metrics that describe the network organiza- munity composition is the late Quaternary extinction (LQE) tion to evaluate the changes in the patterns of interactions of the megafauna (body mass 44 kg) that occurred close between seed dispersers and plants over time. Because ≥ to the Pleistocene-Holocene transition [between 50,000 and the LQE represented a major change in the composition 10,000 years ago (Martin and Klein 1984)]. In South Amer- of mammalian assemblages (Martin and Klein 1984), we ica alone, approximately 50 genera of large-bodied mam- expected that network organization in the Pleistocene mals went extinct (Koch and Barnosky 2006; Barnosky and would be substantially different and would have experi- Lindsey 2010). Although many studies have focused on the enced a great reconfiguration after most large-bodied mam- causes underlying the LQE (Koch and Barnosky 2006), the mals became extinct. To our knowledge, this is the first consequences of megafaunal extinctions have received con- attempt to reconstruct how a large extinction event and siderably less attention (Galetti 2004; Rule et al. 2012). human arrival reconfigure an ecological network. There is compelling evidence that the large mammals that died out in the LQE were key species in the communi- ties of which they were part (Martin and Klein 1984; Janzen Materials and methods 1986; Gill et al. 2009; Johnson 2009). Evidence supporting this view is represented by seed-dispersal anachronisms, Study site whereby many extant plant species show traits that are best explained as having been shaped by interactions with The seed-dispersal interactions were surveyed in two extinct megafauna (Janzen and Martin 1982; Donatti et al. neighboring locations in the Brazilian Pantanal: Rio Negro 2007; Guimarães et al. 2008). Indeed, anachronistic seed- (19°34′S 56°14′W) and Barranco Alto farms (19°34′S dispersal systems are thought to be the result of the disrup- 56°09′W), covering 7,500 and 11,000 ha, respectively tion of the seed-dispersal services formerly provided by (Donatti et al. 2011). The vegetation in these locations is megafauna due to the LQE (Janzen and Martin 1982; Gui- characterized by gallery forests, savannas, and semi-decid- marães et al. 2008). Those plant species probably suffered uous forests. As in all the South America lowlands (Bush some degree of seed-dispersal limitation after the extinc- et al. 2011), paleoclimatic studies suggest that the Pantanal tion of their large seed dispersers (Janzen 1986), currently experienced climatic fluctuations during the late Pleisto- relying upon seed dispersal by scatter-hoarding rodents, cene and Holocene (Assine and Soares 2004) that resulted surrogate megafauna (e.g., livestock), runoff, flooding, in vegetation shifts (Whitney et al. 2011). Although such gravity, and human-mediated dispersal (Guimarães et al. changes most certainly affected plant communities, palyno- 2008; Jansen et al. 2012). The study of how seed-dispersal logical data show that by 19.5 thousand years before the systems were affected by megafaunal extinction may allow present, when tropical forest communities began to expand us to understand how ongoing defaunation will affect eco- following the full glacial period, most plant taxa repre- logical processes (Galetti and Dirzo 2013). sented in the modern pollen assemblages were already pre- Here,
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