Antbears and underground melons: A highly specialized seed dispersal mutualism mediated by scent

Societal Impact Statement Seed dispersal is critical for the establishment and persistence of populations of most plant species. We investigated the seed dispersal biology of an African melon, Cucumis humifructus , which is closely related to cultivated cucumbers and watermelons but differs in that it buries its fruits deep underground. The fruits are located by antbears using olfaction; the antbears consume the fruit pulp and the seeds germinate in their faeces. Cucumis humifructus has become very rare in some parts of Africa and is vulnerable on account of its annual lifecycle combined with its dependence on a declining mammal species for establishing each new generation. Summary Seed dispersal mutualisms between plants and animals are seldom specialized at the species level. We investigated the highly unusual case of the dispersal of seeds of a melon Cucumis humifructus by the antbear ( Orycteropus afer ), a myrmecophagous African mammal. This annual plant buries its fruits c. 20 cm underground, a depth from which seedling emergence is impossible. We asked why the fruits are buried and how they are located by animals. We investigated the seed dispersal system of C. humifructus in central Namibia using camera traps, seed germination experiments and analyses of animal faeces. Coupled gas chromatography and mass spectrometry (GCMS) was used to analyse the chemistry of fruit scent. Naturally‐buried C. humifructus fruits were excavated solely by antbears. Antbear faecal pellets often contained intact C. humifructus seeds. All of the C. humifructus plants that we examined originated in antbear pellets. Fruits placed experimentally above ground or buried shallowly were eaten by porcupines which act as seed predators as they destroy soft melon seeds with their chewing teeth. Fruits of C. humifructus emit scent with a chemical profile distinct from that of related melon species. We argue that deep burial of fruits is a strategy that C. humifructus uses to escape from mammalian seed predators, particularly porcupines. This study highlights the potential role of escape from antagonistic interactions in the evolution of specialized seed dispersal mutualisms.