Fruits of Viburnum opulus (highbush cranberry, guelder rose) ripen in the fall and remain uneaten throughout the winter months. To investigate the fruiting strategy of this plant, I described the natural history of fruit removal from V. opulus shrubs in central New York and investigated nutritional mechanisms for the phenology of fruit removal by its principal disperser. Viburnum opulus fruit crops were often completely consumed in April and May, almost exclusively by Cedar Waxwings (Bombycilla cedrorum). Sugar solute concentration of V. opulus fruit pulp increased over the winter season through dehydration. When wild Cedar Waxwings were presented with early-season (removed and frozen in December) and remnant late-season (April) fruits, they strongly preferred early-season fruits. This result demonstrated that springtime consumption of V. opulus fruits by Cedar Waxwings is not caused by chemical changes in the fruit pulp during the winter months that enhance fruit palatability.
Cedar Waxwings often fed intermittently on the male catkins of eastern cottonwoods (Populus deltoides) when eating V. opulus fruits. Feeding experiments with captive waxwings showed that birds lost body mass on either V. opulus fruits or P. deltoides catkins alone, but maintained or gained body mass when offered both foods simultaneously. The combined diet provided Cedar Waxwings with nutritionally sufficient amounts of energy from fruit sugars and protein from pollen. Two chemical characteristics of V. opulus fruits were implicated in creating a short-term demand for supplemental protein: an especially low nitrogen/carbohydrate ratio and secondary compounds. The pulp of V. opulus fruits contains secondary compounds that make this fruit very acidic, presenting consumers with the challenge of maintaining acid/base homeostasis. Elevated nitrogen losses by waxwings eating only V. opulus fruits were consistent with the hypothesis that birds catabolized protein to produce bicarbonate as an acid buffer. Secondary compounds may play a central role in the evolution of plant fruiting syndromes because of their dual effects on microbes, mediating persistence of fruits in the environment, and palatability of fruits to seed dispersers, presumably because they exact a protein cost from consumers.
These results showed that nutritional interactions of seasonally ephemeral food items can determine temporal patterns of fruit consumption. The well-defended fruits of V. opulus are eaten when more palatable fruits no longer remain and when a complementary protein source becomes available. This fruiting strategy can result in wholesale seed dispersal. The restricted nature of the mutualism between waxwings and V. opulus appears to be a result of the extraordinary persistence of these fruits and the unique dietary habits of waxwings. Viburnum opulus fruits remain uneaten until the spring months, when waxwings are scavenging remnant crops of sugary fruits and most other avian frugivores have switched to animal foods.