Changes in interactions between juniper and mistletoe mediated by shared avian frugivores: parasitism to potential mutualism

Abstract

Although mistletoe is typically viewed as a parasite of juniper in a two-way interaction, its role may become neutral or even mutualistic when their common avian seed dispersing agents are considered as a three-way interaction. In the study area, wintering avian frugivores forage on both one-seed juniper (Juniperus monosperma) berries and on the fruit of its associated mistletoe (Phoradendron juniperinum). Three major findings emerged from our studies that support a three-way interaction and the hypothesis of conditional interactions. First, mistletoes provide a stable resource for shared avian seed dispersers; junipers do not. Whereas juniper berry production varied 10- to 15-fold over the 3 years of our study, mistletoe fruit abundance did not vary significantly. Second, the abundance of avian seed dispersal agents, such as Townsend's solitaires (Myadestes townsendi), is strongly tied to the abundance of juniper berries in mast years and mistletoe fruits in all years. In fact, the best overall predictor of their common avian seed dispersal agents was the abundance of mistletoe; stands with mistletoe attracted up to 3 times more avian frugivores than stands with little or no mistletoe. Thus, mistletoe berries can serve as the main attractor for birds that disperse juniper berries. Third, in agreement with the hypothesis that mistletoe can benefit junipers by attracting and supporting greater populations of avian seed dispersal agents, the number of juniper seedlings was more than 2-fold greater in stands with high mistletoe density compared with stands that had little or no mistletoe. Results suggest that the occurrence of a three-way interaction, in the presence of environmental variation (in this case, annual variation in juniper berry crops), may change the ecological roles of associated species. A conceptual model is presented to illustrate how the role of mistletoe may range from parasitic to mutualistic, while the role of avian seed dispersers may conversely range from mutualistic to parasitic, the latter by acting as vectors for the spread of mistletoe.

Distribution, frequency and host patterns of European mistletoe (Viscum album subsp. album) in the major city of Lodz, Poland

“…This favors the spread of seeds from infected hosts over noninfected hosts during years when susceptible trees have not produced an abundance of fruits. It has been suggested that when the seeds of infected trees are also spread by mistletoe vectors and this is correlated with greater tree regeneration, the relationship between the mistletoe and host tree approaches mutualism (Van Ommeren & Whitham 2002).…”

Connecting Resource Tracking by Frugivores to Temporal Variation in Seed Dispersal Networks

“…When the mistletoe Phoradendron juniperinum was fruiting, removal of fruit from its host, Juniperus monosperma, was enhanced (van Ommeren and Whitham, 2002). Gleditsch and Carlo (2010) experimentally demonstrated increased fruit removal of Solanum americanum in areas that had higher shrub densities of Lonicera mackii and L. morrowii.…”

Mistletoes: Pathology, Systematics, Ecology, and Management

“…This favors the spread of seeds from infected hosts over noninfected hosts during years when susceptible trees have not produced an abundance of fruits. It has been suggested that when the seeds of infected trees are also spread by mistletoe vectors and this is correlated with greater tree regeneration, the relationship between the mistletoe and host tree approaches mutualism (213). Recent studies have also suggested other intriguing hypotheses regarding the interactions among host morphology, bird behavior, and mistletoe dispersal in South America (133,139).…”

“…For dioecious tree species, bird visitation may be biased in favor of fruiting plants, thereby influencing overall mistletoe distribution (39). Furthermore, the consistent availability of mistletoe fruits can attract birds which also feed on the host's fruits (213). This favors the spread of seeds from infected hosts over noninfected hosts during years when susceptible trees have not produced an abundance of fruits.…”

“…Mistletoes may influence the relationship of mycorrhizal fungi and their hosts by stressing the host to the point that mycorrhizal fungi populations in the roots of severely infected trees are decreased (44,70,145). Mistletoes are patchily distributed and generally most abundant on the largest host trees or shrubs at the local scale, which may have impacts on population structure of host trees in a forest (11,39,167,197,213).…”