Phenological Adaptations in Fleshy Vertebrate-Dispersed Fruits of Temperate Plants

Abstract

The timing of fruit ripening is an important feature of fleshy-fruited vertebrate-dispersed plants in temperate regions. The dominating dispersal agents are birds, of which the majority are migratory. Many of these birds use fleshy fruits as a source of food to build reserves before and during migration, for which reason many plants ripen their fleshy fruits at a time that coincides with the peak of bird abundance in the autumn (Snow and Snow 1988, Debussche and Isenmann 1992, Noma and Yumoto 1997). However, there is variation in this pattern. At an individual species level, variation in fruit ripening may not follow bird abundance patterns (French 1992, Fuentes 1992, Willson and Whelan 1993). Furthermore, many plants produce fleshy fruits before or after the autumn assembly of migrating birds (Eriksson and Ehrlen 1991, White and Stiles 1992). There are at least four possible explanations for such phenological deviations. First, non-migrating birds, or stationary mammals, may be the most important seed dispersers for some species (Eriksson 1994, Traveset and Willson 1997), relaxing the need for a specific timing of fruit ripening. Second, competition among plants for disperser-attraction may have resulted in different strategies of fruit phenology (Thompson and Willson 1979, Stiles 1980, Stapanian 1982). Early maturing fleshy fruits may primarily attract birds that seek quick energy while the birds still rear their young. Fruits ripening late, i.e. after the birds have migrated, instead attract stationary animals during autumn and winter by providing persistent sources of reserve food. This kind of reasoning leads to predictions of phonological trends in nutritional content of fruit pulp: carbohydrate content would decrease during the season whereas lipids and proteins would increase. Moreover, based on considerations of plant recruitment, Stapanian (1982) suggested that species with early ripening fruits would benefit from having many small seeds instead of few large seeds. The reason is that small seeds are more likely to possess delayed germination, disperse in time, which is suitable for plants that due to dispersal by still territorial birds do not reach far from the mother plant. Third, the phenology of fruiting may be constrained by the timing of flowering, and the subsequent time needed for seed development (Primack 1987). A final explanation for a lack of clear phenological patterns of fruit maturation is that these traits may not be amenable to adaptive explanations at all due to phylogenetic inertia (Herrera 1986, Kochmer and Handel 1986, Bremer and Eriksson 1992, Jordano 1995). According to this view, the traits possessed by many extant fleshy fruits evolved under circumstances no longer prevailing, in some genera as far back as during the early Tertiary. Empirical studies aimed at scrutinizing hypotheses on the relationship between fruit traits and phenology have produced conflicting results. The predicted trends in nutritional content have gained limited support from some studies (Herrera 1982, Johnson et al. 1985, Debussche et al. 1987) but not from others (Piper 1986, Eriksson and Ehrlen 1991). For seasonal trends in structural fruit traits there is generally no support (Herrera 1982, Eriksson and Ehrlen 1991), apart from a trend of increasing seed size found by Piper (1986). A conclusion that presently seems most reasonable is that phylogenetic constraints have a strong impact on fleshy fruit traits, limiting the scope for finding close connections between the traits and features of the present-day environments (Herrera 1995, Jordano 1995). However, no study has explicitly examined structural and nutritional features of fleshy fruits in relation to phenology, with use of a method that accounts for phylogenetic relationships among species. If nutritional and structural fruit traits are generally lineage-specific, a cross-species comparison of these traits in relation to phonology may fail to detect any trends because the lineage-effects confound the effects of phenology.