Marco A. R. Mello

The Missing Part of Seed Dispersal Networks: Structure and Robustness of Bat-Fruit Interactions

Mutualistic networks are crucial to the maintenance of ecosystem services. Unfortunately, what we know about seed dispersal networks is based only on bird-fruit interactions. Therefore, we aimed at filling part of this gap by investigating bat-fruit networks. It is known from population studies that: (i) some bat species depend more on fruits than others, and (ii) that some specialized frugivorous bats prefer particular plant genera. We tested whether those preferences affected the structure and robustness of the whole network and the functional roles of species. Nine bat-fruit datasets from the literature were analyzed and all networks showed lower complementary specialization (H2u200a=u200a0.37±0.10, mean ± SD) and similar nestedness (NODFu200a=u200a0.56±0.12) than pollination networks. All networks were modular (Mu200a=u200a0.32±0.07), and had on average four cohesive subgroups (modules) of tightly connected bats and plants. The composition of those modules followed the genus-genus associations observed at population level (Artibeus-Ficus, Carollia-Piper, and Sturnira-Solanum), although a few of those plant genera were dispersed also by other bats. Bat-fruit networks showed high robustness to simulated cumulative removals of both bats (Ru200a=u200a0.55±0.10) and plants (Ru200a=u200a0.68±0.09). Primary frugivores interacted with a larger proportion of the plants available and also occupied more central positions; furthermore, their extinction caused larger changes in network structure. We conclude that bat-fruit networks are highly cohesive and robust mutualistic systems, in which redundancy is high within modules, although modules are complementary to each other. Dietary specialization seems to be an important structuring factor that affects the topology, the guild structure and functional roles in bat-fruit networks.

The modularity of seed dispersal: differences in structure and robustness between bat- and bird-fruit networks.

In networks of plant–animal mutualisms, different animal groups interact preferentially with different plants, thus forming distinct modules responsible for different parts of the service. However, what we currently know about seed dispersal networks is based only on birds. Therefore, we wished to fill this gap by studying bat–fruit networks and testing how they differ from bird–fruit networks. As dietary overlap of Neotropical bats and birds is low, they should form distinct mutualistic modules within local networks. Furthermore, since frugivory evolved only once among Neotropical bats, but several times independently among Neotropical birds, greater dietary overlap is expected among bats, and thus connectance and nestedness should be higher in bat–fruit networks. If bat–fruit networks have higher nestedness and connectance, they should be more robust to extinctions. We analyzed 1 mixed network of both bats and birds and 20 networks that consisted exclusively of either bats (11) or birds (9). As expected, the structure of the mixed network was both modular (Mxa0=xa00.45) and nested (NODFxa0=xa00.31); one module contained only birds and two only bats. In 20 datasets with only one disperser group, bat–fruit networks (NODFxa0=xa00.53xa0±xa00.09, Cxa0=xa00.30xa0±xa00.11) were more nested and had a higher connectance than bird–fruit networks (NODFxa0=xa00.42xa0±xa00.07, Cxa0=xa00.22xa0±xa00.09). Unexpectedly, robustness to extinction of animal species was higher in bird–fruit networks (Rxa0=xa00.60xa0±xa00.13) than in bat–fruit networks (Rxa0=xa00.54xa0±xa00.09), and differences were explained mainly by species richness. These findings suggest that a modular structure also occurs in seed dispersal networks, similar to pollination networks. The higher nestedness and connectance observed in bat–fruit networks compared with bird–fruit networks may be explained by the monophyletic evolution of frugivory in Neotropical bats, among which the diets of specialists seem to have evolved from the pool of fruits consumed by generalists.

Diet and Abundance of the Bat Sturnira lilium (Chiroptera) in a Brazilian Montane Atlantic Forest

Abstract We studied variations in diet and abundance of the bat Sturnira lilium (Chiroptera: Phyllostomidae) in a montane Atlantic Forest, in order to investigate if patterns in this habitat differ from those in the better-studied lowlands. The diet of S. lilium was assessed based on fecal samples, whereas possible variations in abundance were documented based on capture success. We also monitored and linked variability in air temperature to fruit production of Solanaceae, the main food of S. lilium. Bats fed exclusively on fruits, mostly on Solanaceae and occasionally on Piperaceae and Cecropiaceae. S. lilium was mostly absent in the area during the colder months, suggesting that they might migrate to lower and hence warmer elevations. Absence of the bats was not related to a distinct decline in availability of fruit of Solanaceae because fruit production was not related to temperature. We conclude that in tropical montane systems, abundance of some frugivorous bats might be affected more by air temperature than by food availability. Furthermore, we reinforce the idea that preserving elevational gradients is a crucial aspect for the conservation of migratory species.

Seasonal variation in the diet of the bat Carollia perspicillata (Chiroptera: Phyllostomidae) in an Atlantic Forest area in southeastern Brazil

Carollia perspicillata feeds primarily on plants of the family Piperaceae, as reported in the literature. Although this preference occurs throughout this species’ geographic range, in some situations they may eat other items. This study analyzed variations in the feeding habits of this bat species over an 18-month period. Although C. perspicillata consumed mostly Piper plants, they also ate other fruits (e.g. Cecropia and Solanum plants), and insects as well. Food choice followed a seasonal pattern, related to the availability of Piper plants. The seasonal absence of these fruits may have necessitated bats to eat alternative items.

Pollination networks of oil‐flowers: a tiny world within the smallest of all worlds

1. In the Neotropics, most plants depend on animals for pollination. Solitary bees are the most important vectors, and among them members of the tribe Centridini depend on oil from flowers (mainly Malpighiaceae) to feed their larvae. This specialized relationship within the smallest of all worlds (a whole pollination network) could result in a tiny world different from the whole system. This tiny world would have higher nestedness, shorter path lengths, lower modularity and higher resilience if compared with the whole pollination network. 2. In the present study, we contrasted a network of oil-flowers and their visitors from a Brazilian steppe (caatinga) to whole pollination networks from all over the world. 3. A network approach was used to measure network structure and, finally, to test fragility. The oil-flower network studied was more nested (NODF = 0.84, N = 0.96) than all of the whole pollination networks studied. Average path lengths in the two-mode network were shorter (one node, both for bee and plant one-mode network projections) and modularity was lower (M = 0.22 and four modules) than in all of the whole pollination networks. Extinctions had no or small effects on the network structure, with an average change in nestedness smaller than 2% in most of the cases studied; and only two species caused coextinctions. The higher the degree of the removed species, the stronger the effect and the higher the probability of a decrease in nestedness. 4. We conclude that the oil-flower subweb is more cohesive and resilient than whole pollination networks. Therefore, the Malpighiaceae have a robust pollination service in the Neotropics. Our findings reinforce the hypothesis that each ecological service is in fact a mosaic of different subservices with a hierarchical structure (webs within webs).

Movements of the bat Sturnira lilium and its role as a seed disperser of Solanaceae in the Brazilian Atlantic forest

Bats and birds carry out most of the seed dispersal in the Neotropics (Galindo-Gonzales et al . 2000), and are crucial for the dynamics and regeneration of tropical forests (Whittaker & Jones 1994). However, only a few details are known about the interactions in particular bat–fruit systems. Most frugivorous bats are highly mobile (Bernard & Fenton 2003), and do not harm seeds (Fleming & Sosa 1994), suggesting that they are legitimate and effective seed dispersers ( sensu Fleming & Sosa 1994).

Invasive Africanized honeybees change the structure of native pollination networks in Brazil

The Africanized honeybee Apis mellifera (AHB) is an invasive species spread over all Brazilian biomes, which has negative impacts on native bee populations, but whose impacts on native plants are still controversial. In order to understand how its impacts extend to the pollination service at the community level, we studied the AHB and its interactions in a multi-species context using network theory. We analyzed six pollination networks from the Brazilian Caatinga, a xeric biome where beekeeping is increasing very quickly. The AHB occupied a central position in all networks, as it was responsible for a large share of the interactions observed (14xa0±xa07xa0%) and bound together different modules. By simulating the removal of the AHB from each network, we observed no effects on connectance, but a strong decrease in nestedness (−23xa0±xa019xa0%) and an increase in modularity (8xa0±xa05xa0%). The robustness of networks to cumulative random extinctions was on average not affected. In summary, our evidence points out that the AHB induces significant changes in the structure of native pollination networks, mainly by making them more cohesive and monopolizing many interactions. Although the AHB did not affect network robustness, its net impact on the pollination service may be negative, because this invasive species is very generalistic and may not be an efficient pollinator for some native plants.

Flower-visiting guild associated with the Caatinga flora: trophic interaction networks formed by social bees and social wasps with plants.

We conducted a comparative analysis of bee-plant and wasp-plant interaction networks, aiming at the identification of similarities and differences between networks of flower-visiting groups with direct or indirect mutualism with plants. We measured for each network: number of social bees and social wasps, number of plants visited (P), degree of nestedness, number of observed (I) and possible interactions, connectance (C), and interaction density (D). The network formed by pooling together social bees and social wasps exhibited 25 species (12 bees and 13 wasps) and 49 visited plants, with a connectance of 15.34%. The wasp-plant network had higher connectance (C = 21.24) than the bee-plant network (C = 15.79). Both the social wasp-plant and the social bee-plant network were significantly nested, they presented structure more nested than all randomly generated matrices (n = 1 000). Both interaction networks have similar topologies and are nested, asymmetrical and modular structures.ZusammenfassungWir verglichen ein soziales BienenPflanzen Netzwerk (BPN) mit einem sozialen Wespen-Pflanzen Netzwerk (WPN) unter der Fragestellung, ob verschiedene Arten von Mutualismus mit demselben Partner zu unterschiedlichen Netzwerkstrukturen führen. Hierzu wurden soziale Bienen und Wespen in einem Sammelgebiet mit Caatinga-Vegetation in Bahia bei ihren Blütenbesuchen gefangen. Jedes zweiteilige Netzwerk wurde dann in Form einer R-Nachbarschaftsmatrize beschrieben. Wir beschrieben jedes Netzwerk in Hinblick auf Schachtelung (nestedness NODF und N), Modularität (M) und Bedeutung einzelner Spezies (Ij). Beide Netzwerke erwiesen sich als geschachtelt (Abb. 1). Wir untersuchten weiterhin, inwieweit die beiden Netzwerkmaße (NODF und N) die Schachtelung in entsprechenden Nullmodellmatrizen (mit n = 1000 Zufallswiederholungen) quantifizierten, wobei Präsenzen zufallsverteilt den jeweils einzelnen Zellen der Matrix zugeordnet wurden. Die aus unseren Daten gebildeten Bienen-Pflanzen- und Wespen-Pflanzen-Matrizen wiesen allesamt eine tiefere Schachtelung auf als die Zufallsmatrizen. Das WPN bildete 116 der 546 möglichen Interaktionen ab und zeigte eine Bindungsstärke von C = 21,24, während das BPN 72 der 456 möglichen Interaktionen aufwies, bei einer Konnektivität von C = 15,79. Sieben der blütenbesuchenden Spezies bildeten den Kernbereich des WPN und sechs Arten erwiesen sich als von besonderer Bedeutung für die Struktur des BPN. Die Topologie des BPN war stark von der Gegenwart von Apis mellifera beeinflusst, einer eingeführten Art, die als Generalist Interaktionen mit 33 der 38 Pflanzenarten einging. Das Gesamtnetzwerk (OFPN) wurde aus 25 blütenbesuchenden Arten und 49 besuchten Pflanzen gebildet und hatte eine Konnektivität von 15,34. Insgesamt konnten wir 188 von 1225 möglichen Interaktionen finden, wobei neun Arten für 78,19 % aller Verbindungen verantwortlich waren: Apis mellifera (33 Interaktionen), Polybia ignobilis (18), P. sericea (17), Polistes canadensis (17), P. paulista (15), Brachygastra lecheguana (13), Trigona spinipes (12), P. occidentalis (11) und Protonectarina sylveirae (11). Ein relativ hoher Anteil der Pflanzenarten (63,3 %, N = 31) wurde sowohl von sozialen Bienen als auch sozialen Wespen besucht. Unsere Analysen der Beziehungsnetzwerke zeigten einen klaren Unterschied hinsichtlich der Bedeutung einzelner Pflanzenarten als Nahrungsquelle für die jeweiligen blütenbesuchenden Gruppen (Abb. 2). Die Modularität des Gesamtnetzwerks aus beiden Gruppen war relativ gering (M = 0,07, P = 0,004), was auf eine Überlappung zwischen Bienen und Wespen in den Blütenbesuchen zurückzuführen ist. Wir fanden zudem eine höhere Nischengruppierung innerhalb der Bienen als innerhalb der Wespen. Trotz der Unterschiede im fakultativen Mutualismus zwischen Bienen-Pflanzen (direkter Mutualismus — Bestäubung) und WespenPflanzen (indirekter Mutualismus — Verteidigung) wiesen die beiden Beziehungsnetzwerke ähnliche Topologien auf, mit geschachtelten Mustern und asymmetrischen, modularen Strukturen.

A test of the effects of climate and fruiting of Piper species (Piperaceae) on reproductive patterns of the bat Carollia perspicillata (Phyllostomidae)

Bats of the genus Carollia feed mainly on plants of the genus Piper, dispersing their seeds in all localities where they occur together. Interactions among these bats, their food plants, and the climate were studied in an Atlantic Forest area in Southeastern Brazil. Path analysis was used to estimate the strength of direct and indirect effects through which variables determine the timing of bat reproduction. Temperature had a small direct influence, but a strong indirect one. Rainfall affected bat reproduction through indirect ways. Although the consumption of Piper fruits by bats did not have a significant influence, the timing of production of Piper fruits was a strong variable directly affecting bat reproduction. We therefore suggest that Piper plants and climate may play a keyrole in the timing of reproduction in C. perspicillata bats.

Hierarchical fruit selection by Neotropical leaf-nosed bats (Chiroptera: Phyllostomidae)

Abstract It is crucial to understand how Neotropical leaf-nosed bats select fruits, because their choices strongly affect the seed dispersal process, especially of pioneer plants. We tested the hypothesis of hierarchical fruit selection by phyllostomid bats at the levels of the bat genus and species by combining a literature database with field experiments. Considering our database for the whole Neotropics, Artibeus bats focus on Ficus (Moraceae) and Cecropia (Cecropiaceae), Carollia bats on Piper (Piperaceae), and Sturnira bats on Solanum (Solanaceae). Results from a field experiment in Brazil corroborated those preferences, because bats of those 3 genera selected 1st the fruits of their preferred plant genera, even when secondary fruits were offered in higher abundance. In another field experiment in Panama, we observed that 2 sympatric Carollia species, although focusing on the same plant genus, prefer different Piper species. Literature records for the whole range of the 2 Carollia species show that they have strongly nested diets. Our findings corroborate the hypothesis that frugivorous phyllostomids do not forage opportunistically, and, moreover, segregate their diets hierarchically at the genus and species levels. Resumo É crucial entender como morcegos filostomídeos neotropicais selecionam frutos, porque as escolhas deles influenciam fortemente o processo de dispersão de sementes, especialmente de plantas pioneiras. Testamos a hipótese de seleção hierárquica de frutos por morcegos filostomídeos nos níveis do gênero e espécie de morcegos, através de uma combinação de um banco de dados e experimentos de campo. Considerando o nosso banco de dados para toda a região Neotropical, morcegos Artibeus focam em Ficus (Moraceae) e Cecropia (Cecropiaceae), morcegos Carollia em Piper (Piperaceae) e morcegos Sturnira em Solanum (Solanaceae). Os resultados de um experimento de campo no Brasil corroboraram essas preferências, pois morcegos desses 3 gêneros selecionaram os frutos dos seus gêneros preferidos em primeiro lugar, até mesmo quando frutos secundários foram oferecidos em maior abundância. Em outro experimento de campo no Panamá, observamos que 2 espécies simpátridas de Carollia, apesar de focarem no mesmo gênero de plantas, preferem espécies de Piper diferentes. Registros da literatura para toda a área de distribuição geográfica dessas duas espécies de Carollia mostram que elas têm dietas fortemente aninhadas. Nossas descobertas corroboram a hipótese de que filostomídeos frugívoros não forrageiam de maneira oportunista e, além disso, segregam suas dietas hierarquicamente nos níveis do gênero e da espécie.