Plant structural defences against browsing birds: a legacy of New Zealand's extinct moas

Browsing by large vertebrates has been a major force in the evolution of terrestrial plants but Holocene extinctions of the browsers have left a legacy of broken biotic partnerships. Ratite birds were the largest herbivores in several regions, such as the moas of New Zealand. Many woody plants there have a distinct form of branching, described as "divaricate", with thin, wide angled, branches intertwining to form a tangled canopy. Divaricate branching has been interpreted as a form of protection against climate extremes or as an anachronistic defense against the extinct moas. Here we report the first experimental evidence that many of these plants are defended against extant ratite browsers. In feeding experiments on two tree species with different (heteroblastic) juvenile and adult branch morphology, emus and ostriches obtained adequate feeding rates from adult shoots but sub-maintenance feeding rates from juvenile shoots with the ratite-resistant traits. Divaricate juvenile shoots suffered 30-70% less biomass removal to the birds than adult shoots. Ratites browse by a distinctive clamping and tugging action. Structural defence traits that exploit the limitations of this feeding mode include narrow, strong, elastic branches that resist being torn off, wide branching angle ("divaricate") that makes shoots difficult to swallow, and small, widely spaced leaves. This novel plant architectural defence has developed in at least 20% of the native woody flora of New Zealand, including 10 heteroblastic tree species that exhibit the ratite-resistant strategy until they reach ca 3 metres height. It is also a major axis of variation amongst homoblastic woody shrub species. The defences are useless against mammalian browsers that shear shoots, contributing to marked decreases in the abundances of ratite-resistant species in New Zealand after the introduction of mammals.