Ant-diaspore interactions during secondary succession in the Atlantic forest of Brazil

Victor P. Zwiener^1*,2*, Jochen H. Bihn^3* & Márcia C. M. Marques²

Abstract

Animal-plant interactions are important for the recovery of diversity and processes in secondary forests, which increasingly dominate the tropical landscape. We used a combination of observational and experimental approaches to study the interactions of ants with diaspores across a successional gradient of forests in Southern Brazil, from August 2007 to April 2008. In addition to diaspore removal rates, we assessed the species richness, diversity and behaviour of ants interacting with diaspores, in three replicated sites of four successional stages of forests. We recorded 22 ant species interacting with diaspores (an estimated 15% of the total species pool in the region). Species richness and diversity did not differ among successional stages but the behaviour of ants towards diaspores changed with the age of secondary forests. In old successional stages the removal of entire diaspores was more common than in young successional stages of forests. Concordantly, diaspore removal rates were lowest in the youngest successional stage of secondary forests and increased with the age of forests. These results indicate that ant-diaspore interactions in secondary forests are disturbed and lower removal rates in secondary forests are likely to constrain the recruitment of plant populations during secondary succession. Rev. Biol. Trop. 60 (2): 933-942. Epub 2012 June 01.

Key words: ant-plant interactions, forest recovery, seed dispersal, seed predation, succession, tropical secondary forests.

Resumen

Las interacciones entre animales y plantas son importantes para la recuperación de la diversidad y los procesos en los bosques secundarios, los cuales cada vez más tienden a dominar el paisaje tropical. Nosotros utilizamos una combinación de métodos experimentales y observaciones para estudiar las interacciones entre hormigas y diásporas a través de un gradiente de sucesión en los bosques del sur de Brasil, entre agosto 2007 y abril 2008. Además de las tasas de eliminación de diásporas, evaluamos la riqueza de especies, la diversidad y el comportamiento de las hormigas que interactúan con las diásporas, con tres repeticiones por sitio de cuatro estadios de sucesión del bosque. Se registraron 22 especies de hormigas que interactúan con diásporas (se estima un 15% del total de especies en la región). La riqueza y diversidad de especies no vario entre las etapas de sucesión, pero el comportamiento de las hormigas hacia las diásporas cambio con la edad de los bosques secundarios. En las etapas sucesionales avanzadas del bosque la eliminación de diásporas fue más común que en las etapas tempranas. En concordancia, las tasas de eliminación de diásporas fueron menores en la etapa más temprana de la sucesión de bosques secundarios y aumenta con la edad de los mismos. Estos resultados indican que las interacciones hormigasdiásporas en los bosques secundarios son alteradas y las menores tasas de extracción en los bosques secundarios es probable que limiten el reclutamiento de las poblaciones de plantas durante la sucesión secundaria.

Palabras clave: interacciones planta-hormiga, recuperación del bosque, dispersión de semillas, depredación de semillas, sucesión, bosques tropicales secundarios.

Tropical old-growth forests are vanishing at alarming rates and are converted into pastures and agricultural lands (Wright 2005, Chazdon et al. 2009). The total area covered by forests, however, is increasing in tropical countries across the globe (Wright & Muller-Landau 2006). This situation arises because of secondary forests, regenerating on former agricultural land increasingly dominate the tropical landscape (FAO 2007). Animal-plant interactions are important for the recovery of diversity and ecological processes in secondary forests (Guariguata & Ostertag 2001, Chazdon 2003). Secondary forests emerging in human-impacted landscapes do not match the original old-growth forests in species composition (Hobbs et ]]> 2006). Therefore, it is still uncertain to what extent secondary forests will maintain similar processes with respect to new combinations of species.

Most plants in tropical forests produce diaspores (fruits, seeds) adapted for animal dispersal (Frankie et al. 1974, Howe & Smallwood 1982). Both seed dispersal and seed ]]> et al. 2004). Thus, a better understanding of how these ecological processes recover during ]]>

Ants (Hymenoptera: Formicidae) are important dispersers and predators of diaspores in tropical forests (Levey & Byrne 1993, Pizo & Oliveira 2000, Passos & Oliveira 2003). Ants contribute to the plant reproductive cycle by transporting fallen diaspores from the forest floor or acting as ]]> et al. 2007) and we found the same ]]> et al. 2008). The interactions between ants and non-myrmecochorous diaspores in tropical forests are mostly not species specific, i.e. ants interact with diaspores of many plant species and vice versa (Pizo & Oliveira 2000, Passos & Oliveira 2003). Thus, the reduced species diversity of ants in secondary forests might have no consequences for the interactions between ants and diaspores as long as a minimum subset of species that interact with diaspores is retained in secondary forests. Instead, the rate of seed removal and ]]> et al. 2007, Manzaneda & Rey 2008, Zelikova & Breed 2008). In the Atlantic forest of Southern Brazil (Bihn et al. 2008) and in other tropical forests (Armbrecht et al. 2004, Silva et al. 2007), the abundance of ant species increases with successional age ]]>

We used a combination of ]]> ant-diaspore interactions across a successional gradient in the Atlantic Forest of Southern Brazil. Exclosure experiments were used to estimate rates of diaspore removal in secondary forests differing in age since abandonment, and in old-growth forests. Additionally, we assessed the diversity and behaviour of ants interacting with diaspores on the forest floor in different successional stages of forests.
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Materials and methods

Study region and sites: Field studies were conducted at the Rio Cachoeira Nature Reserve (25o18’51” S - 48o41’45” W) in the state of Paraná, Southern Brazil, from August 2007-April 2008. The regional climate is classified as humid ]]>
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The experiments were carried out in four successional stages: secondary forests of 9-11years, 15-20years, and 40-55years since abandonment of pastures, and old-growth forests (sensu Clark 1996). Old-growth forests had not been logged for at least 100 years. Three study sites were selected for each successional stage. Land-use history for study sites was established through interviews with residents and reserve staff corroborated by inspection of high ]]> et al. 2008 for a map of the reserve and the location of the study sites within it).

]]> Ant-diaspore interactions: To determine which ants interact with diaspores on the forest floor, as well as how they interact with diaspores, we made observations at experimental diaspore depots, mimicking clumps of dispersed diaspores. In March and April 2008 we established five experimental diaspore depots, separated by a minimum of 10m, in each study site. Diaspore depots consisted of 30 diaspores of three tree species (10 diaspores of each species) placed on a plastic plate (8.5cm diameter) on the forest floor. Diaspores were collected in the study region from at least three ]]> Pera glabrata (Schott) Baill. , Hyeronima alchorneoides M. Allemão and Trema micrantha (L.) Blume. We used only diaspores collected on the same day in our experiments because stored diaspores or diaspores that had been refrigerated could suffer from desiccation and chilling injuries thus changing some of their characteristics and introducing bias (Theilade & Petri 2003). The plant species were selected because they were ]]> P. glabrata fruits consist of a dry unpalatable outer covering that splits when mature exposing three to four diaspores. The diaspores consist of brilliant black seeds (3mm diameter, 0.02g fresh weight; Passos & ]]> H. alchorneoides has roundish fruits (8mm diameter, 0.04g fresh weight; Flores 1993) consisting of a reddish fleshy pulp and one single seed. T. micrantha fruits are the smallest fruits used in the experiment (3mm diameter, 0.01g fresh weight; Silveira et al. 2003). The fruit consists of a green fleshy pulp that turns orange when mature and encase a single seed.

Observations at diaspore depots were made between 10:00 and 14:00. Each diaspore depot was checked after 15, 30, 45, 60, 75 and 90min. The species and the abundance of ants interacting with diaspores were recorded as well as their behaviour towards the diaspores. To determine whether the species richness and the diversity of ants interacting with diaspores increases during secondary forest succession, we applied a Poisson generalized ]]> H) (Krebs 1989), the diversity and evenness of ants were tested with a Gaussian generalized linear model (GLM).

The behaviour of ants interacting ]]>

Diaspore removal experiment: Rates of diaspore removal by ants in different successional stages were ]]> Fagopyrum tataricum (L.) Gaertn.). Seed fragments ranged from 1-4mm in diameter and had a mean dry mass of 12mg±1 SE (n=50). We used relatively small seed sizes because the removal of small diaspores is not constrained by the size of the ant but large diaspores tend to be removed only by larger ants (Pfeiffer et al. ]]> et al. 1991, Christianini & Galetti 2007) we used diaspores that are not native to the study region. Diaspores of native species were not used due to the large amount of diaspores needed in order to replicate the experiment across all sites and successional stages and because native diaspores were not available during two seasons of the year (summer and winter). In preliminary diaspore removal trials we confirmed that seed fragments of Tartary buckwheat were attractive to ]]>

Plates were covered with a wire cage (15cm x 15cm x 15cm, 1cm mesh size) to exclude vertebrates but allowing ants to access the diaspores. Cages were secured to the ground with wire anchors. We placed a transparent plastic cover over each plate to prevent the diaspores from being washed away by rain. Sampling ]]>

Diaspore removal rates were analyzed with a two-factor nested ANOVA. The main factor in this analysis was “successional stage” (fixed factor; levels: 9-11yr, 15-20yr, 40-55yr, >100yr) with three “sites” (random factor) nested within each level of the main factor and 20 replicated observations for each combination of “successional stage” and “site”. We tested for a ]]>

Results
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Ants interacting with diaspores: We found ants interacting with diaspores at 56 of 60 diaspore depots. Ants discovered diaspores rapidly and in the majority of cases we observed interactions within 15min. after exposure of diaspores. We recorded 22 ant species from seven genera and four subfamilies interacting with diaspores at depots (Table 1). Species richness of ants did not differ ]]>

The diversity and evenness of ants interacting with diaspores did not differ across the successional ]]> H=0.97(±0.02 SE), in 15-20yr secondary forests H’=1.36 (±0.2 SE) and E_H=0.95(±0.01 SE), in 40-55yr secondary forests H’=1.53(±0.2 SE) and E_H=0.93(±0.01 SE) and H’=1.13(±0.3 SE) and E_H=0.91(±0.03 SE) in old growth forests (n=3 for each mean).
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In all successional stages “seed cleaning” was the most frequent behaviour of ants interacting with diaspores. Nevertheless, the proportion of seed depots where we observed ants removing diaspores increased from 19% in the youngest successional stages to 38% in the oldest successional stages (Fig. 1). This difference in the frequency of ant behaviour towards diaspores was significant (Fisher’s Exact test, p=0.049). ]]>

Diaspore removal rates: Diaspore removal rates in the 12 study sites varied from 22%-61% depending on successional stage. In general, removal rates increased with an increase in age of successional stage (Fig. 2; Table 2). Average diaspore removal rates in old growth forests (45%) were higher than in 40-55yr, 15-20yr and 9-11yr forests (33%; 26% and 25%, respectively). Diaspore removal in old growth forest was 1.8 times higher than in the 9-11yr forest.


Discussion

Animal-diaspore interactions play an important role in the dynamics of tropical forests and their ]]>

Species richness and diversity of ants interacting with diaspores was similar in all successional stages of forests. This contrasts to the reduced richness and diversity of the entire ground foraging ant fauna in secondary forests of the Atlantic forest in Southern Brazil (Bihn et al. 2008, 2010). Ant species ]]> et al. 2010). Many ant species we found interacting with diaspores were relatively common in the study region (JH Bihn, unpublished results), especially species of Pheidole which accounted for the majority of ant-diaspore interactions in our and other studies in neotropical forests (Pizo et al. 1998, Pizo & ]]>

The behaviour of ants towards diaspores changed along the gradient of forest succession. In all stages of forest succession removal of the fleshy part of the diaspore in situ was the most common behaviour but the proportion of diaspores entirely removed increased from early to late successional stages. Both ]]> et al. 2007) but seeds remain available for other guilds of seed predator, e.g. rodents, marsupials and birds. Diaspore removal often leads to seed predation but a small number of seeds are left intact and are transported to protected microsites with favourable conditions for germination (Levey & Byrne 1993, Pizo 2008). Because we did not track the fate of diaspores we cannot infer about the ]]>

Diaspore removal rates were lower in young secondary than in old-growth forests and gradually increased with the age of secondary forests. Studies on invertebrate diaspore removal in different successional stages of tropical forests are few and report contradictory results. Notman & Gorchov (2001) found ]]> et al. 2005, Zelikova & Breed 2008). However, removal rates are not directly comparable among these investigations because each study uses a different set of diaspore species in the experiments and it has been demonstrated that removal rates of diaspores depend on diaspores identity (Notman & Gorchov 2001, Pizo & Oliveira 2001).
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What are the implications of the observed changes of the behaviour of ants towards diaspores and the increased diaspore removal rates during forest regeneration? The most likely fate of removed diaspore is predation. However, various studies have documented that ants transport undamaged diaspores to safe and favourable microsites for germination (Leyey & Byrne 1993, Pizo 2008). Although this outcome of ant-diaspore interactions might be rare, it might still be important for the recruitment of plant ]]> et al. 1998, Passos & Oliveira 2003). Lower removal rates in young secondary forests could potentially increase sibling competition among seedlings and thus have negative effects on the recruitment of plant populations, slowing down the regeneration of these forests. Only careful tracking of diaspore fate, dispersal distance and germination success can illuminate the benefits and costs for the recruitment of the involved ]]>

Acknowledgments

]]> This study was financially supported by Brazilian Research Council (CNPq) (Solobioma Project, 690148/01-1), the German Federal Ministry of Education and Research (BMBF project number 01LB0201), and the Fundação O Boticário de Proteção à Natureza. We thank the support of the SPVS for allowing us to work at Cachoeira Nature Reserve and their staff for field work assistance. Márcia C. M. Marques received a productivity grant ]]>

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*Correspondencia a: Victor P. Zwiener: Society for Wildlife Research and Environmental Education (SPVS). Rua Isaias Bevilacqua, 999, 80430-040, Curitiba, Paraná, Brazil; vzwiener@gmail.com
Victor P. Zwiener & Márcia C. M. Marques: Universidade Federal do Paraná, Setor de Ciências Biológicas, Departamento de Botânica, Caixa Postal 19.031, 81531-980 Curitiba, Paraná, Brazil; mmarques@ufpr.br
Jochen H. Bihn: Department of Ecology - Animal Ecology, Philipps-Universität Marburg, Karl-von-Frisch Straße 8, 35032 Marburg, Germany; jochen.bihn@gmail.com

1. Society for Wildlife Research and Environmental Education (SPVS). Rua Isaias Bevilacqua, 999, 80430-040, Curitiba, Paraná, Brazil; vzwiener@gmail.com
2. Universidade Federal do Paraná, Setor de Ciências Biológicas, Departamento de Botânica, Caixa Postal 19.031, 81531-980 Curitiba, Paraná, Brazil; mmarques@ufpr.br
3. Department of Ecology - Animal Ecology, Philipps-Universität Marburg, Karl-von-Frisch Straße 8, 35032 Marburg, Germany; jochen.bihn@gmail.com