Nutritional Interactions and Fruit Removal: Cedar Waxwing Consumption of Viburnum opulus Fruits in Spring

Abstract

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 earlyseason 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.

Birds and guelder rose Viburnum opulus: selective consumption and dispersal via regurgitation of small-sized fruits and seeds

“…However, sometimes part of the guelder rose crop is left in winter and the fruits are consumed at the beginning of spring (Witmer 2001;Hernández 2008a), or not consumed and dry up on the shrubs, where they remain for many months (Englund 1993;pers. obs.).…”

“…Frugivorous birds show little preference for guelder rose fruits due to their low palatability and nutritional value, as the pulp is very acid and poor in proteins and lipids (Sorensen 1983;Herrera 1987;Jones and Wheelwright 1987;Witmer 2001;Kollmann and Grubb 2002). Their sugar content increases during winter but does not appear to enhance their palatability (Jones and Wheelwright 1987;Witmer 2001).…”

“…They are persistent fruits highly resistant to the damage caused by frost and are hardly ever attacked by pathogens or insects (Jones and Wheelwright 1987;Englund 1993;Kollmann and Grubb 2002). Thus, guelder rose dispersal is dependant on periods of time when more preferred food (other fruits or invertebrates) is not available or becomes scarce, usually when winter has already set-in, and seed-dispersing birds consume them in larger amounts; many fruits are often consumed by granivorous birds and climbing rodents which destroy the seeds, or dry up on the plant during spring and are not eaten (Jones and Wheelwright 1987;Snow and Snow 1988;Englund 1993;Witmer 2001;Kollmann and Grubb 2002;Hernández 2008a). Therefore it is expected that if larger fruits are negatively selected by disperser birds they will probably remain on the plants longer and be less useful in terms of dispersal, resulting in effective selection of smaller fruits and seeds.…”

“…Their sugar content increases during winter but does not appear to enhance their palatability (Jones and Wheelwright 1987;Witmer 2001). They are persistent fruits highly resistant to the damage caused by frost and are hardly ever attacked by pathogens or insects (Jones and Wheelwright 1987;Englund 1993;Kollmann and Grubb 2002).…”

Fruit removal by climbing rodents in guelder rose: Comparison with birds and differences between inner and outer racemes

“…With respect to frugivorous birds, it is well known that they reject guelder rose fruits because their pulp is very acid and poor in proteins and lipids, and consequently have low palatability and nutritional value (Sorensen 1983;Herrera 1987;Jones and Wheelwright 1987;Witmer 2001;Kollmann and Grubb 2002). So guelder rose dispersal depends on periods of time when other preferred food is not available or is scarce, usually when winter has already started, and frugivorous birds consume them in larger quantities (Jones and Wheelwright 1987;Witmer 2001;Kollmann and Grubb 2002).…”