Urbanization drives partner switching and loss of mutualism in an ant-plant symbiosis

Mutualistic interactions between species underpin biodiversity and ecosystem function, but may be lost when partners respond differently to abiotic conditions. Except for a few prominent examples, effects of global anthropogenic change on mutualisms are poorly understood. Here we assess the effects of urbanization on a symbiosis in which the plant Cordia nodosa houses ants in hollow structures (domatia) in exchange for defense against herbivores. We expected to find that mutualist ants would be replaced in the city by heat-tolerant opportunists, leaving urban plants vulnerable to herbivory. In five protected forest sites and five urban forest fragments in southeast Perú, we recorded the identity and heat tolerance (CTmax) of ant residents of C. nodosa. We also assayed their plant-defensive behaviors and their effects on herbivory. We characterized the urban heat-island effect in ambient temperatures and within domatia. Forest plants housed a consistent ant community dominated by three specialized plant-ants, whereas urban plants housed a suite of ten opportunistic taxa that were, collectively, about 13 times less likely than forest ants to respond defensively to plant disturbance. In the forest, ant exclusion had the expected effect of increasing herbivory, but in urban sites, exclusion reduced herbivory. Despite poor ant defense in urban sites, we detected no difference in total standing herbivory, perhaps because herbivores themselves also declined in the city. Urban sites were warmer than forest sites (daily maxima in urban domatia averaged 1.6°C hotter), and the urban ant community as a whole was slightly more heat tolerant. These results illustrate a case of mutualism loss associated with anthropogenic disturbance. If urbanization is representative of increasing anthropogenic stressors more broadly, we might expect to see destabilization of myrmecophytic mutualisms in forest ecosystems in the future.

Methods
Methods are detailed in the main manuscript.

物种间的互利共生互作是支撑生物多样性与生态系统功能的核心基础，但当共生伙伴对非生物环境的响应存在差异时，这类互作关系可能发生衰退。除少数典型案例外，全球人为活动变化对互利共生系统的影响尚未得到充分认知。本研究聚焦城市化对一种共生关系的影响：植物破布木（*Cordia nodosa*）通过中空结构（蚁巢体，domatia）为蚂蚁提供栖息场所，以此换取蚂蚁对植食动物的防御服务。我们预期城市环境中的互利共生蚂蚁会被耐热机会主义类群取代，致使城市植物面临植食侵害的风险升高。
我们在秘鲁东南部的5个原生保护森林样地与5个城市森林片段中，记录了栖息于*Cordia nodosa*内的蚂蚁种类组成及其耐热临界温度（CTmax），同时测定了这些蚂蚁的植物防御行为及其对植食危害的影响，并表征了环境温度及蚁巢体内的城市热岛效应。
原生森林样地中的植物所栖息的蚂蚁群落结构稳定，优势类群为3种特化植食防御蚂蚁；而城市森林片段中的植物则栖息着由10个机会主义类群组成的蚂蚁群落，整体而言，这些城市蚂蚁对植物受干扰时做出防御响应的概率仅为森林蚂蚁的约1/13。
在原生森林样地中，排除蚂蚁会如预期般加剧植食危害；但在城市样地中，排除蚂蚁反而降低了植食危害。尽管城市样地中的蚂蚁防御能力不足，但我们未检测到总现存植食水平存在显著差异，这或许是因为城市环境中的植食动物种群自身也出现了衰减。
城市样地的温度显著高于原生森林样地（城市蚁巢体的日最高温平均高出1.6℃），且城市蚂蚁群落整体的耐热性略高于森林蚂蚁群落。上述结果证实了一例与人为干扰相关的互利共生系统衰退案例。若城市化可作为日益加剧的人为胁迫的典型代表，未来森林生态系统中的蚁植互利共生（myrmecophytic mutualisms）关系或出现稳定性下降的情况。
材料与方法
研究方法详见主文稿。