Split between two worlds: automated sensing reveals links between above- and belowground social networks in a free-living mammal

Many animals socialize in two or more major ecological contexts. In nature, these contexts often involve one situation in which space is more constrained (e.g. shared refuges, sleeping cliffs, nests, dens or burrows) and another situation in which animal movements are relatively free (e.g. in open spaces lacking architectural constraints). Although it is widely recognized that an individual's characteristics may shape its social life, the extent to which architecture constrains social decisions within and between habitats remains poorly understood. Here we developed a novel, automated-monitoring system to study the effects of personality, life-history stage and sex on the social network structure of a facultatively social mammal, the California ground squirrel (Otospermophilus beecheyi) in two distinct contexts: aboveground where space is relatively open and belowground where it is relatively constrained by burrow architecture. Aboveground networks reflected affiliative social interactions whereas belowground networks reflected burrow associations. Network structure in one context (belowground), along with preferential juvenile–adult associations, predicted structure in a second context (aboveground). Network positions of individuals were generally consistent across years (within contexts) and between ecological contexts (within years), suggesting that individual personalities and behavioural syndromes, respectively, contribute to the social network structure of these free-living mammals. Direct ties (strength) tended to be stronger in belowground networks whereas more indirect paths (betweenness centrality) flowed through individuals in aboveground networks. Belowground, females fostered significantly more indirect paths than did males. Our findings have important potential implications for disease and information transmission, offering new insights into the multiple factors contributing to social structures across ecological contexts.

诸多动物会在两种及以上核心生态场景下开展社交活动。在自然环境中，这类场景通常包含两类：一类是空间更为受限的情境（例如共享庇护所、睡眠崖壁、巢穴、兽穴或洞穴），另一类则是动物活动相对自由的情境（例如不存在空间结构限制的开阔区域）。尽管学界已普遍认可个体特征会塑造其社交生活，但空间结构对生境内外社交决策的约束程度，目前仍未得到充分研究。本研究开发了一套新型自动化监测系统，用以探究个性、生活史阶段以及性别对兼性社会性哺乳动物——加利福尼亚地松鼠（Otospermophilus beecheyi）——社交网络结构的影响，实验设置了两类截然不同的场景：空间相对开阔的地上场景，以及受洞穴结构显著约束的地下场景。地上社交网络反映的是亲和性社交互动，而地下社交网络则对应洞穴社群关联。其中一类场景（地下）的网络结构，加上幼体-成体的优先关联模式，可预测另一类场景（地上）的网络结构。个体的网络位置通常在年度间（同一场景内）以及生态场景间（同一年度内）保持稳定，这表明个体个性与行为综合征分别推动了这些自由生活哺乳动物的社交网络结构形成。地下网络中的直接联结（强度）往往更强，而地上网络中则有更多间接路径（中介中心性）通过个体。在地下场景中，雌性个体所介导的间接路径数量显著多于雄性。本研究结果对疾病与信息传播具有重要的潜在启示，为探究不同生态场景下影响社交结构的多重因素提供了全新视角。