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 (H2' = 0.37±0.10, mean ± SD) and similar nestedness (NODF = 0.56±0.12) than pollination networks. All networks were modular (M = 0.32±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 (R = 0.55±0.10) and plants (R = 0.68±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.互惠共生网络（mutualistic networks）对生态系统服务的维持至关重要。遗憾的是，当前学界对种子扩散网络（seed dispersal networks）的认知仅基于鸟-果互作（bird-fruit interactions）研究。因此，本研究通过对蝙蝠-果互作网络（bat-fruit networks）展开调查，以期填补这一研究空白的一部分。已有种群研究表明：其一，部分蝙蝠物种相较于其他类群更依赖果实资源；其二，部分特化食果蝙蝠（frugivorous bats）偏好特定的植物属（plant genera）。本研究旨在验证这些取食偏好是否会影响整个网络的结构与鲁棒性（robustness），以及物种的功能角色。本研究分析了9篇已发表文献中的蝙蝠-果互作数据集，结果显示，相较于传粉网络，所有此类网络的互补特化（complementary specialization）程度更低（H2'=0.37±0.10，均值±标准差），且嵌套性（nestedness）水平相近（NODF=0.56±0.12，均值±标准差）。所有网络均呈现模块化结构（M=0.32±0.07，均值±标准差），平均包含4个由紧密互作的蝙蝠与植物类群构成的紧密连通子群（模块，modules）。这些模块的组成遵循种群水平上观测到的属间互作模式，即叶口蝠属（Artibeus）与榕属（Ficus）、长舌蝠属（Carollia）与胡椒属（Piper）以及短尾叶口蝠属（Sturnira）与茄属（Solanum）的互作关系，尽管部分此类植物属也可被其他蝙蝠类群传播种子。蝙蝠-果互作网络对模拟的蝙蝠与植物类群累积移除均表现出较高的鲁棒性：蝙蝠移除模拟的鲁棒性R=0.55±0.10，植物移除模拟的鲁棒性R=0.68±0.09。专性食果蝙蝠与更多比例的可利用植物类群发生互作，且在网络中占据更核心的位置；此外，专性食果蝙蝠的灭绝会引发网络结构发生更为显著的变化。本研究得出结论：蝙蝠-果互作网络是一类高度紧密连通且鲁棒性强的互惠共生系统，模块内部的功能冗余度较高，但不同模块之间存在互补性。食性特化似乎是影响蝙蝠-果互作网络拓扑结构、功能群（guild）结构与物种功能角色的重要构建因子。