Fruit Removal Rates Research Articles

Disentangling the drivers of reduced long-distance seed dispersal by birds in an experimentally fragmented landscape

Seed dispersal is a crucial component of plant population dynamics. Human landscape modifications, such as habitat destruction and fragmentation, can alter the abundance of fruiting plants and animal dispersers, foraging rates, vector movement, and the composition of the disperser community, all of which can singly or in concert affect seed dispersal. Here, we quantify and tease apart the effects of landscape configuration, namely, fragmentation of primary forest and the composition of the surrounding forest matrix, on individual components of seed dispersal of Heliconia acuminata, an Amazonian understory herb. First we identified the effects of landscape configuration on the abundance of fruiting plants and six bird disperser species. Although highly variable in space and time, densities of fruiting plants were similar in continuous forest and fragments. However, the two largest-bodied avian dispersers were less common or absent in small fragments. Second, we determined whether fragmentation affected foraging rates. Fruit removal rates were similar and very high across the landscape, suggesting that Heliconia fruits are a key resource for small frugivores in this landscape. Third, we used radiotelemetry and statistical models to quantify how landscape configuration influences vector movement patterns. Bird dispersers flew farther and faster, and perched longer in primary relative to secondary forests. One species also altered its movement direction in response to habitat boundaries between primary and secondary forests. Finally, we parameterized a simulation model linking data on fruit density and disperser abundance and behavior with empirical estimates of seed retention times to generate seed dispersal patterns in two hypothetical landscapes. Despite clear changes in bird movement in response to landscape configuration, our simulations demonstrate that these differences had negligible effects on dispersal distances. However, small fragments had reduced densities of Turdus albicollis, the largest-bodied disperser and the only one to both regurgitate and defecate seeds. This change in Turdus abundance acted together with lower numbers of fruiting plants in small fragments to decrease the probability of long-distance dispersal events from small patches. These findings emphasize the importance of foraging style for seed dispersal and highlight the primacy of habitat size relative to spatial configuration in preserving biotic interactions.

Spatial–temporal distribution of ornithochorous seeds from an Elaeagnus umbellata community dominating a riparian habitat

AbstractThe dispersal efficiency and potential distribution of ornithochorous seeds of Elaeagnus umbellata in a riparian habitat were evaluated to clarify this species' establishment site in relation to the disturbance regime of the floodplain. Fruit removal by avian frugivores was monitored using fruit bags, and the spatial distribution of excreted seeds was quantified by seed traps set randomly on a gravel bar as an isolated seed source in the Yoshino River throughout an autumn fruiting season. Although more than 45% of the fruits remained on the twigs in the fruit bags, almost all fruits on the control twigs without fruit bags were exploited by the beginning of January. The fruit removal rate and seed dispersal distance were positively correlated with an increase in wintering bird species and their abundance. Intact bird‐dispersed seeds of E. umbellata were trapped within a 400‐m range and damaged seeds were limited to traps set within 50 m from the seed source. Frugivore behavior, such as feces excretion on rocks near water drinking sites and perching on surrounding woodland, greatly influenced the spatial and temporal dispersal pattern of the seed rain. In the present study, the avian frugivores showed upstream seed dispersal; thus, in years with stochastic autumnal floods, secondary dispersal via hydrochory downstream may be facilitated. The intensive seed dispersal in E. umbellata indicates that the present distribution of parent trees in the restricted elevation range of the gravel bars is the result of survival through disturbance, rather than seed dispersal limitation.

Revealing secondary seed removers: results from camera trapping

AbstractThis paper reports the results of the first study on secondary seed removal of seeds dispersed by Sykes’ monkeys (Cercopithecus albogularis) using camera traps in Africa. Patterns of primary seed dispersal are often superimposed by secondary conveyance, emphasising the need to study these secondary processes carefully. As the agents and mechanisms of seed dispersal are often concealed, being carried out by cryptic or nocturnal animals in dense vegetation, camera trapping was deemed a viable means to investigate secondary removal of seeds disseminated by C. albogularis in the Western Soutpansberg, South Africa. Camera traps were established at preferred feeding trees of the focal Sykes’ monkey group to identify animal species that remove seeds and fruits spat and dropped to the forest floor and seed removal observations were carried out. This method proved to be effective in identifying seed removers and also allowed to get indications about the quantities of seeds removed. Ten animal species were recorded visiting the trees, of which eight were observed removing seeds and fruits. Overall seed and fruit removal rates were high, indicating that the foraging behaviour of C. albogularis attracts many terrestrial frugivores.

Fleshy Fruit Removal and Nutritional Composition of Winter-Fruiting Plants: A Comparison of Non-Native Invasive and Native Species

Invasive, non-native plants threaten forest ecosystems by reducing native plant species richness and potentially altering ecosystem processes. Seed dispersal is critical for successful invasion and range expansion by non-native plants; dispersal is likely to be enhanced if they can successfully compete with native plants for disperser services. Fruit production by non-native plants during winter (or dormant season), when native fruits and arthropods are scarce, might enhance chances of fruit consumption and seed dispersal by vertebrates. We compared the proportion and rate of fruit removal among five invasive, non-native and two native plant species that retain fruit during winter to test whether non-native fruits are readily removed and their seeds dispersed by vertebrates-even where native fruit is available. We also assessed whether the nutritional content of fruit pulp affects fruit removal rates, and collected bird droppings from fecal traps to examine species and rates of seed dispersal. Most (83% to 93%) fruit was removed from all species except native Smilax rotundifolia L. (55%). Most (92%) seeds collected from bird droppings were from non-native plants (six species); only 8% were from native plants (four species). Mean fruit survival time (across species) was positively correlated with total sugar and negatively correlated with lipid. Total fruit consumed was not correlated with nutrient content. Our results indicate most fruits of tested winter-fruiting, non-native invasive plants are removed, and their seeds are dispersed. In the southern Appalachian Mountains, only a few native plant species, notably greenbriar (Smilax spp.), American holly (Ilex opaca Alton), and sumac (Rhus spp.) retain abundant, ripe fruit during winter months, and these species tend to be patchy in their distribution. Therefore, winter fruit availability by non-native invasive plants offers an important opportunity for dispersal and range expansion, and is likely key in their successful invasion of ecosystems.

Effects of forest age on fruit composition and removal in tropical bird-dispersed understorey trees

Abstract:Little is known about how land-use changes affect interspecific interactions such as fruit–frugivore mutualisms. Forest age could affect both fruit sugar concentrations via differences in light availability or disperser abundance, and fruit removal rates via differences in bird and plant community composition. We examined how these two factors are affected by forest age in a Costa Rican rain forest. We compared seven young-secondary forest species, seven old-growth forest species, andMiconia nervosagrowing in both forests. We measured sugar concentrations in fruits and manipulated the location of paired fruiting branches, measuring subsequent fruit removal. Sugar concentration means were on average 2.1 percentage points higher in young-secondary forest species than in old-growth forest species, but did not differ amongMiconia nervosafruits from the two forests. Fruit removal rates were higher in young-secondary forest for 86% of young-secondary forest species, 71% of old-growth forest species, and on average for both young-secondary and old-growth forestMiconia nervosaindividuals. Higher sugar concentrations in young-secondary forest plants could reflect stronger competition for dispersers, while experimental fruit removal results suggests the opposite patterns of competition; fruits are more likely to be removed by dispersers in young-secondary forest independent of fruit nutrient concentration.

Petals may act as a reward: myrmecochory in shrubby Darwinia species of south‐eastern Australia

AbstractThe removal rates of fruits (the diaspore) were assessed in exclusion experiments in three shrubby species of Darwinia, endemic to the Sydney Basin of south‐eastern Australia. There was a clear pattern of fruit removal in just a few days by small species of ants from the genera Iridomyrmex, Crematogaster and Pheidole. When only ants had access to fruits an average of 41% of fruits were removed, whereas when only vertebrates had access an average of 13% of fruits were removed. There was some variation in the number of fruits removed both between species and within species across study sites or annual seed crops. When ants had access to seeds this variation in removal amounted to 10–80% over 1–4 days. Uniquely in Darwinia, it is the old petals (which remain attached to the fruit) that are attractive to the ants, rather than a specific lipid body. This likely represents a case of successful ecological fitting by Darwinia to take advantage of the widespread presence of myrmecochory in the Australian flora.

Inequalities in fruit‐removal and seed dispersal: consequences of bird behaviour, neighbourhood density and landscape aggregation

Summary Frugivores disperse the seeds of the majority of woody plant species world‐wide. Thus, insights on how frugivores influence the dispersal of plants and the variability of this process are crucial for understanding plant population dynamics in a rapidly changing world. We used a spatially explicit, stochastic, individual‐based model that simulates fruit‐removal and seed dispersal by birds to assess bird density, landscape and neighbourhood effects on the inequalities of within‐population fruit‐removal rates and seed dispersal. We also compared model predictions with spatially‐explicit field data. In our simulations, bird density had a strong effect on the distribution of fruit‐removal rates creating large inequalities among plants. Also, for equal bird densities, inequalities increased with the landscape level aggregation of plants. Fruit removal increased with increasing plant neighbourhood density although there was a tendency to decline at the highest densities. Neighbourhood density also changed average dispersal distances, but with shorter distances at higher densities. Plants with few neighbours not only had longer distance dispersal but also a larger variance in seed rain across distances than plants with ten or more neighbours. These relationships between neighbourhood density and fruit removal and dispersal distance were scale‐dependent with a peak in correlations at 150‐m radius. Similar to model predictions, field data shows an inverse relationship between dispersal distances (inferred from bird movements) and fruiting neighbourhood density. Also, fruit‐removal rates observed in the field show large numbers of plants receiving little or zero fruit‐removal. Fruit‐removal rate distributions were statistically indistinguishable between the simulation and field data. But, distributions were strikingly different from two alternative models that lacked spatial effects. Synthesis. Our model and field data show that as fruiting plants become aggregated, inequalities in fruit‐removal rates increase and seed dispersal distance decreases. Both of these processes could help create and maintain plant aggregation and affect genetic structuring. The model also predicts that small‐scale neighbourhood effects can be controlled by large‐scale processes such as overall frugivore abundance and landscape‐level plant aggregation. Most importantly, both simulations and field data shows an interaction between plant spatial pattern and bird foraging, which results in neighbourhood‐specific dispersal and rates of fruit removal.

Effects of Local Disturbance of Tropical Forests on Frugivores and Seed Removal of a Small‐Seeded Afrotropical Tree

Small-scale, local disturbance of tropical forests, for example from selective logging, is widespread, but its effects on biodiversity and ecosystem function have rarely been studied. In 3 East African tropical rainforests, we investigated the effect of different levels of local forest disturbance on the frugivore community and on tree visitation and fruit removal rates of the small-seeded tree Celtis durandii. We quantified birds and primates in little and heavily disturbed sites, distinguishing between forest specialists, forest generalists, and forest visitors. We quantified frugivorous tree visitors and seed removal rates of C. durandii trees in the same sites. Forest disturbance reduced the species richness and density of the frugivore community and of forest specialists. Frugivorous species and individuals visiting the study trees were reduced significantly, which led to a marginally significant decline in fruit removal by all frugivores and a significant reduction in removal by forest specialists. Reduction in fruit removal by forest specialists was not compensated for by increases in removal by forest generalists or visitors. Results did not differ among the 3 rainforests, which suggests they were consistent at a regional scale. So local forest disturbance led to a loss of frugivores and their seed removal services. This suggests that large-seeded tree species and trees with small fruits are losing seed dispersers. Thus, local forest disturbance appears to have a more general negative impact on frugivores and their seed dispersal services than anticipated previously.

Does attraction to frugivores or defense against pathogens shape fruit pulp composition?

Fruit traits evolve in response to an evolutionary triad between plants, seed dispersers, and antagonists that consume fruits but do not disperse seeds. The defense trade-off hypothesis predicts that the composition of nutrients and of secondary compounds in fruit pulp is shaped by a trade-off between defense against antagonists and attraction to seed dispersers. The removal rate model of this hypothesis predicts a negative relationship between nutrients and secondary compounds, whereas the toxin-titration model predicts a positive relationship. To test these alternative models, we evaluated whether the contents of nutrients and secondary compounds can be used to predict fruit removal by mutualists and pathogens in 14 bird-dispersed plants on a subtropical island in São Paulo state, southeastern Brazil. We selected eight to ten individuals of each species and prevented fruit removal by covering four branches with a net and left fruits on four other branches available to both, vertebrate fruit consumers and pathogens. The persistence of ripe fruits was drastically different among species for bagged and open fruits, and all fruit species persisted longer when protected against seed dispersers. We found that those fruits that are quickly removed by vertebrates are nutrient-rich, but although the attack rate of pathogens is also high, these fruits have low contents of quantitative defenses such as tannins and phenols. Thus, we suggest that the fruit removal rate by seed dispersers is the primary factor selecting the levels of fruit defense. Likewise, nutrient-poor fruits have low removal of seed dispersers and low probability of attack by pathogens. These species retain ripe fruits in an intact condition for a prolonged period because they are highly defended by secondary compounds, which reduce overall attractiveness. However, this strategy might be advantageous for plants that depend on rare or unreliable dispersers.

Mistletoe fruit‐colour polymorphism and differential success in a habitat mosaic

Abstract Polymorphisms in fruit colour are common in nature, but mechanistic explanations for the factor(s) responsible for their maintenance are for the most part lacking. Past studies have focused on frugivore colour preferences and fruit removal rates, but until recently there has been no evidence that these factors are responsible for the maintenance of the polymorphisms. For other types of genetic polymorphisms, habitat heterogeneity has been shown to play a role in their maintenance. Here we test the habitat heterogeneity hypothesis for a polymorphic New Zealand mistletoe. We show that red‐fruited and orange‐fruited morphs of the mistletoe Alepis flavida (Hook. F) Tiegh. (Loranthaceae) differ in their growth, mortality and flowering on forest edges and in forest interior. Red‐fruited morphs, which are preferred by dispersers, grew, survived and flowered as well as orange‐fruited morphs on edges, whereas orange‐fruited morphs had much greater growth, survival, and flowering than red‐fruited morphs in the forest interior. This is the first evidence that habitat‐specific differences in growth and survival may contribute to maintaining fruit‐colour polymorphisms.

Dispersal of Canarium euphyllum (Burseraceae), a large-seeded tree species, in a moist evergreen forest in Thailand

We investigated the dispersal of a large-seeded tree species, Canarium euphyllum (Burseraceae), in the moist evergreen forests of the Khao Yai National Park in Thailand. By combining direct observations of fruit consumption in tree canopies (543 h) and the camera-trapping observations of fallen fruit consumption on the forest floor (175 camera-days), we identified the frugivore assemblage that foraged on the fruits of C. euphyllum and assessed their role in seed dispersal and seed predation. In the canopy, our results showed that seeds were dispersed by a limited set of frugivores, one pigeon and four hornbill species, and predated by two species of squirrel. On the forest floor, seven mammal species consumed fallen fruits. A combination of high rates of fruit removal and short visiting times of mountain imperial pigeons (Ducula badia) and hornbills (Buceros bicornis, Aceros undulatus, Anorrhinus austeni and Anthracoceros albirostris) led us to conclude that these large frugivorous birds provide effective seed dispersal for this tree species, in terms of quantity. These frugivorous species often have low tolerance to negative human impacts and loss of these dispersers would have severe deleterious consequences for the successful regeneration of C. euphyllum.

Reproductive biology of theIlexspecies (Aquifoliaceae) in Hong Kong, China

Fourteen wild species of shrubs and trees in the dioecious genus Ilex occur in Hong Kong (22°N, 114°E). All species flowered and formed fruits once each year. Sex ratios at flowering were male biased in all but one large population studied and, in most cases, this bias could not be explained by earlier flowering in males or higher female mortality. Apis cerana accounted for >87% of flower visits in all species and there was a significant positive relationship across species between the number of visits per flower per hour and the estimated mean number of flowers on a plant. The large green fruits of Ilex chapaensis Merr. were consumed only by masked palm civets, Paguma larvata, while the red or black fruits of other species were consumed by birds. The rate of fruit removal across species was positively related to sugar content and negatively related to phenolic and saponin contents. The mean number of pyrenes per fruit was 4.0–6.2 and the mean percentage of pyrenes containing seeds was 49%–90%. Most embryos were immature (heart shaped) at fruit maturity, but <50% of embryos developed further in some species. Floral investment was 0.93–5.84 times higher in male plants, but total reproductive investment was 0.62–8.3 higher in females.

Lantana camara and the fruit- and seed-damaging fly, Ophiomyia lantanae (Agromyzidae): Seed predator, recruitment promoter or dispersal disrupter?

Abstract The seed damaging fly, Ophiomyia lantanae is a widespread agent that infests the fruits and seeds of Lantana camara . Its effectiveness in reducing seed dispersal or seedling recruitment has not been comprehensively tested. We determined the effects of O. lantanae damage on fruit removal rates of L. camara in a field study. We also investigated recruitment responses (seed germination in growth cabinets and seedling emergence in pot trials) of two common L. camara biotypes, pink and pink-edged red (PER) to O. lantanae damage. We found that fewer damaged fruits were removed than undamaged fruits, suggesting that frugivores select against damaged fruit. In all recruitment experiments, the responses to damage were biotype dependent. In germination experiments, these differential responses were primarily due to significantly reduced germination of damaged PER seeds. Seedling emergence from pots of the PER biotype was also lower in damaged seeds (27.5%) than undamaged seeds (56.1%). In contrast, emergence increased with seed damage in the pink biotype, from 28.2 to 41.1%. O. lantanae damage significantly reduced seed mass only in the smaller seeded PER biotype. In the larger seeded pink biotype, it may have promoted seedling emergence by interfering with dormancy mechanisms. We also examined in situ seed banks at L. camara populations prior to peak seed production. Mean viable seed densities ranged from 78.6 to 402.8 seeds m −2 . Of these, non-dormant seeds comprised 24.6 to 98.2 seeds m −2 , suggesting that recruitment is unlikely to be seed limited. We conclude that while O. lantanae influences recruitment and dispersal processes, the magnitude of the responses measured are unlikely to greatly influence plant densities in south-east Queensland infestations.

INTERSPECIFIC NEIGHBORS CHANGE SEED DISPERSAL PATTERN OF AN AVIAN-DISPERSED PLANT

Ecologists increasingly recognize that plant–plant facilitation can influence plant community structure. However, seed dispersal facilitation among plant neighbors that share seed dispersal agents has received little study. Seed dispersal facilitation among neighboring plants can be defined as an increase in the number, distances, and/or places reached by a plant's seeds that is due to the presence of co-fruiting-plant neighbors with which it shares frugivore seed dispersers. I experimentally tested the potential for seed dispersal facilitation and competition among co-fruiting-plant neighbors using Solanum americanum and Cestrum diurnum, two plant species that co-occur in open habitats of Puerto Rico and whose seeds are dispersed by the same bird species. I constructed S. americanum neighborhoods with and without C. diurnum (i.e., mixed and non-mixed) while controlling plant ripe-fruit crop and surrounding fruiting landscape in six replicate fields. I quantified seed dispersal using a grid of seed-collecting trays bearing bird perches placed at four distance classes from experimental plant neighborhoods. I found no difference in the quantity or rate of fruit removal between mixed and non-mixed neighborhoods. However, there were significantly more bird droppings with seeds collected from mixed neighborhoods than from monospecific S. americanum neighborhoods. Although the quantity of seed dispersal was no different among treatments, S. americanum seeds were distributed into more “packaging units” and reached more sampling trays when neighbored by C. diurnum. This was explained by the higher number of frugivores that visited mixed neighborhoods compared to Solanum-only neighborhoods, and by an associated increase in agonistic interactions in mixed neighborhoods. Therefore, the seed dispersal pattern of S. americanum was facilitated by the presence of fruiting C. diurnum neighbors. This study provides the first experimental evidence that seed dispersal kernels of endozoochorous plants are context dependent and not entirely a property of individual plant or disperser species.

Influence of between-year variation in the density of Rhus trichocarpa fruits on the removal of fruit by birds

The fruiting phenology and fruit removal patterns of Rhus trichocarpa Miq. (Anacardiaceae) were investigated in a warm-temperate secondary forest in Japan. Mature fruits of this species are dispersed by birds. Effects of fruit display size and canopy openness on fruit removal were investigated in years with different fruit densities (i.e., masting and non-masting years). Moreover, effects of increased canopy openness during winter on fruit removal were also investigated. Seasonal patterns of fruit removal were quite different between masting and non- masting years. In the non-mast year, fruits were removed by birds soon after maturation in the summer. In contrast, in the mast year, fruits were removed gradually by birds from summer to winter. Moreover, the rate of fruit removal was greater for trees with a larger display size in the non-mast year, whereas that was greater for trees with greater canopy openness in the mast year. Canopy openness increased in winter, and fruit removal in winter was enhanced in trees with a more open canopy only in the non-mast year. These observations strongly suggest that avian dispersers became satiated in the mast year, whereas fruit removal was enhanced in the non-mast year. In the mast year, although many fruits were not dispersed until winter, they were neither depredated nor rotten, and the long period of fruit removal by birds may have enhanced fruit dispersal. The large abundance of seedlings and saplings of this species in Japanese secondary forests suggests that this fruiting strategy is beneficial.

Is there limiting similarity in the phenology of fleshy fruits?

AbstractQuestion:Is there evidence for limiting similarity in the timing of fruit production by a bird‐dispersed plant community? Is the rate of fruit removal in each plant species inversely related to fruit availability in other species? Can simple measurements of fruit phenologies (i.e. temporal changes in fruit availability) obscure important fruit attributes that influence their removal by birds?Location:Vancouver Island, British Columbia, Canada.Methods:Periods of fruit availability were measured in ten woody angiosperm species for two years. In the second year, the fate of individual fruits was quantified to disentangle dates of fruit maturation, removal and mortality from measurements of availability.Results:Null model analyses of fruit availability distributions showed no evidence for limiting similarity. However, fruit removal rates of most plant species were correlated with their relative abundance in the community, indicating fruits were removed more rapidly when other fruits were less abundant. Species with similar periods of fruit availability often had different dates of fruit maturation, rates of fruit removal and fruit persistence times, indicating fruit availability measurements can obscure important bird‐fruit interactions.Conclusions:Competition for dispersers appears to occur. However, it has not resulted in limiting similarity in fruit availability distributions. A likely explanation for this discrepancy is that fruit availability distributions often confound several important fruit attributes that can independently influence fruit removal by birds.

Is there limiting similarity in the phenology of fleshy fruits?

Abstract Question: Is there evidence for limiting similarity in the timing of fruit production by a bird-dispersed plant community? Is the rate of fruit removal in each plant species inversely related to fruit availability in other species? Can simple measurements of fruit phenologies (i.e. temporal changes in fruit availability) obscure important fruit attributes that influence their removal by birds? Location: Vancouver Island, British Columbia, Canada. Methods: Periods of fruit availability were measured in ten woody angiosperm species for two years. In the second year, the fate of individual fruits was quantified to disentangle dates of fruit maturation, removal and mortality from measurements of availability. Results: Null model analyses of fruit availability distributions showed no evidence for limiting similarity. However, fruit removal rates of most plant species were correlated with their relative abundance in the community, indicating fruits were removed more rapidly when other fruits were less ...

Modeling seed dispersal in a variable environment: a case study of the fleshy-fruited savanna shrub Grewia flava

In ecology much attention has been paid towards seed dispersal of fleshy-fruited plants, however, knowledge is lacking about the long-term demographic consequences of variation in dispersal distance and fruit removal rate, particularly given the natural variability of the environment the organism lives in. In this study we used a spatially explicit, two-level stochastic computer model to simulate population dynamics of a fleshy-fruited shrub living in the sub-canopy of solitary savanna trees. On the landscape level we implemented three realistic scenarios of savanna landscape dynamics for a period of 500 years with equal inter-annual mean of environmental variables. The first scenario is representative of a relatively constant environment with normal variability in precipitation, constant tree density and random tree recruitment pattern. The second and third scenarios represent positive auto-correlated, cyclic patterns with alternating phases of tree cover increase and decrease corresponding with favorable and unfavorable rain phases. Our simulation experiments show that when fruit removal rate is extremely low, population persistence is enhanced under relatively constant rain conditions, while alternating rain phases of the cyclic scenarios lead to a significant population decrease. This result confirms previous findings that periodically fluctuating environments may increase local extinction risk. However, when dispersal distance is a limiting factor (whilst removal rate was sufficiently high), tree clumps typically forming in wet phases of both cyclic scenarios compensated for the negative effect of low dispersal distances, while the constant scenario with random tree pattern and larger inter-tree distances resulted in a significant population decline.

Cold temperature increases winter fruit removal rate of a bird-dispersed shrub

We tested the hypothesis that winter removal rates of fruits of wax myrtle, Myrica cerifera, are higher in colder winters. Over a 9-year period, we monitored M. cerifera fruit crops in 13 0.1-ha study plots in South Carolina, U.S.A. Peak ripeness occurred in November, whereas peak removal occurred in the coldest months, December and January. Mean time to fruit removal within study plots was positively correlated with mean winter temperatures, thereby supporting our hypothesis. This result, combined with the generally low availability of winter arthropods, suggests that fruit abundance may play a role in determining winter survivorship and distribution of permanent resident and short-distance migrant birds. From the plant's perspective, it demonstrates inter-annual variation in the temporal component of seed dispersal, with possible consequences for post-dispersal seed and seedling ecology.

INFLUENCES OF ANIMAL POLLINATION AND SEED DISPERSAL ON WINTER FLOWERING IN A TEMPERATE MISTLETOE

The evolution of flowering time can be influenced directly by pollinators and indirectly by seed dispersers. In temperate latitudes, interactions with climate, especially temperature, may affect both plants and their animal mutualists. Winter-flowering plants allow assessment of biotic influences on the evolution of flowering time because temperature is unlikely to select directly for this uncommon reproductive behavior. In northwestern Patagonia, the hemiparasitic mistletoe Tristerix corymbosus flowers from early fall, through the cool winter, to late spring. This species is pollinated by the hummingbird Sephanoides galeritus, and its seeds are dispersed by the marsupial Dromiciops australis. In two populations during two years, I analyzed seasonal variation in pollination, fruit production, and fruit removal. Hummingbird visitation was lowest in winter and late spring, and flowers opening during those periods showed reduced pollination and fruit set, partly due to pollinator limitation, compared to flowers that opened during fall or early spring. Fruits that ripened during summer (January–March) had a higher chance of being removed than fruits ripening during either spring or fall, due to their overlap with the period of maximum disperser activity. Timing of flower opening was strongly associated with fruit maturation time and with fruit removal rates. Thus, even though flowers that opened during winter exhibited only moderate fruit production, their fruits benefited from high fruit removal and seed dispersal in mid to late summer. These results suggest that the activity period of this plant's disperser, in combination with a lack of strong pollination constraints, probably governed the evolution of flowering phenology in this mistletoe. However, the proximate influence of temperature on flower and fruit development may prevent a fine-tuned match between flowering phenology and the period of maximum mutualist activity.