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Recently W.D. Hamilton and colleagues proposed a provocative new theory to explain the adaptive significance of autumnal leaf colours. They suggested that these colours were signals produced by the trees to warn potential insect herbivores of their defensive ability and tested this theory by an analysis of data on aphid species richness on different tree species. Here we argue that the principal assumptions of their theory do not match current knowledge of plant pigment biochemistry and aphid ecology. We therefore present further adaptive explanations for autumn leaf colours and suggest alternative reasons for the reported relationship between tree leaf colour and aphid species richness.

Under many environmental conditions, plants are exposed to levels of sunlight in excess of those required for photosynthesis. Then, a regulated increase in the rate of nonradiative dissipation of excess excitation energy in the thylakoid membrane correlates with the conversion of the carotenoid violaxanthin into zeaxanthin and provides protection from the damaging effects of excessive irradiation. The hypothesis that these carotenoids specifically control the oligomerization of the light harvesting complexes of photosystem II was tested by investigating the effects of violaxanthin and zeaxanthin on the behavior of the major complex, LHCIIb, on sucrose gradients; it was found that zeaxanthin stimulated the formation of LHCIIb aggregates with reduced chlorophyll fluorescence yield whereas violaxanthin caused the inhibition of such aggregation and an elevation of fluorescence. Measurements of 77 K fluorescence indicated that zeaxanthin was not exerting an additional direct quenching of chlorophyll fluorescence. These effects can explain the physiological control of the light harvesting system by the xanthophyll cycle.

Abstract