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.