Bird pollinators, seed storage and cockatoo granivores explain large woody fruits as best seed defense in Hakea
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Nutrient-impoverished soils with severe summer drought and frequent fire typify many Mediterranean-type regions of the world. Such conditions limit seed production and restrict opportunities for seedling recruitment making protection from granivores paramount. Our focus was on Hakea, a genus of shrubs widespread in southwestern Australia, whose nutritious seeds are targeted by strong-billed cockatoos. We assessed 56 Hakea species for cockatoo damage in 150 populations spread over 900 km in relation to traits expected to deter avian granivory: dense spiny foliage; large, woody fruits; fruit crypsis via leaf mimicry and shielding; low seed stores; and fruit clustering. We tested hypothesises centred on optimal seed defenses in relation to (a) pollination syndrome (bird vs insect), (b) fire regeneration strategy (killed vs resprouting) and (c) on-plant seed storage (transient vs prolonged).Twenty species in 50 populations showed substantial seed loss from cockatoo granivory. No subregional trends in granivore damage or protective traits were detected, though species in drier, hotter areas were spinier. Species lacking spiny foliage around the fruits (usually bird-pollinated) had much larger (4-5 times) fruits than those with spiny leaves and cryptic fruits (insect-pollinated). Species with woody fruits weighing >1 g were rarely attacked, unlike those with spiny foliage and small cryptic fruits. Fire-killed species were just as resistant to granivores as resprouters but with much greater seed stores. Strongly serotinous species with prolonged seed storage were rarely attacked, with an order of magnitude larger fruits but no difference in seed store compared with weakly/non-serotinous species. Overall, the five traits examined could be ranked in success at preventing seed loss from large woody fruits (most effective), fruit clustering, low seed stores, spinescence, to crypsis (least effective). We conclude that the evolution of large woody fruits is contingent on pollinator type (dictates flower/fruit location, thus apparency to granivores), level of serotiny (response to poor soils and fire that requires prolonged seed defense) and presence of a formidable granivore (that promotes strong defense).
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