Evolutionary Implications of Fruit-Processing Limitations in Cedar Waxwings

Levey, Douglas J.; Grajal, Alejandro

doi:10.1086/285210

Cited by 109 publications

(96 citation statements)

References 71 publications

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“…Fruits are generally considered to be a food resource high in bulk (Herrera 1987), and bulk overloads the gut thereby reducing ingestion rate. Rapid seed processing may clear the gut and thus allow an increased ingestion rate (Levey & Grajal 1991;Levey 1992). Waxwings fed two types of artificial fruit (agar-based sugar solution as pulp and plastic beads as seeds) with equal seed loads but with different seed sizes consumed significantly more of the larger-seeded fruits.…”

Section: Discussionmentioning

confidence: 99%

“…Waxwings fed two types of artificial fruit (agar-based sugar solution as pulp and plastic beads as seeds) with equal seed loads but with different seed sizes consumed significantly more of the larger-seeded fruits. Because large seeds were defecated more quickly than small seeds, the increase in fruit consumption indicated that waxwings were process rate limited (Levey & Grajal 1991). Levey (1992) reported that freely feeding manakins took natural and artificial fruits very quickly after regurgitation.…”

Section: Discussionmentioning

confidence: 99%

“…Seed size affects SRT, which is important for fruiting plants as it affects survival into the next generation. A number of studies have examined SRT in relation to seed size for various plant species (Sorensen 1984;Johnson et al 1985;Levey 1987;Levey & Grajal 1991).…”

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Relationship between seed retention time in bird's gut and fruit characteristics

Fukui

2003

Ornithol. Sci.

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Mutual interactions between birds and plants species have been emphasized in a range of studies of endozoochory, during which frugivorous birds consume fruit and subsequently disperse plant seeds (Snow 1971;Herrera 1985Herrera , 1995Jordano 1995). There are, however, various conflicts between fruiting plants and frugivorous birds, for example, fruit pulp production is costly for plants, but provides frugivores with energy (Sorensen 1984;Fukui 1996). Fruiting plants and frugivorous birds are also in conflict over seed retention time (SRT), which is defined here as: the time from ingesting a fruit to the time when its seed(s) are eliminated, corresponding to the time spent passing through the bird's digestive system.Several studies have suggested that seed dispersal distance is a function of SRT, however, small seeds tend to be dispersed further (Hoppes 1988;Murray et al. 1994), indicating a relationship between seed size and SRT. Small seeds tend to remain in the gut longer than large seeds. Furthermore, long SRT in the avian gut apparently enhances seed germination (Barnea et al. 1991). Seeds ingested by blackbirds Turdus merula usually had a higher germination rate than those ingested by bulbuls Pycnonotus xanthopygos. This differential rate in germination has been explained by longer SRT in blackbirds than in bulbuls. Longer SRT may increase abrasion of the seed coat by the avian digestive system and thus improve germination rate. SRT represents part of the handling cost of food for birds. Ingested seeds also represent a cost to frugivorous birds because the seeds displace gut volume that could otherwise be filled with digestible fruit pulp. Furthermore, the seed mass in- Abstract Seed retention time (SRT) of 16 fruit species in the guts of the Browneared Bulbul (Hypsipetes amaurotis), a major fruit consumer in central Japan, was studied to examine the relationship between SRT and fruit characteristics, i.e. fruit size, seed size, seed weight, and water content. Caged bulbuls were videotaped after feeding on fruits, and the time of defecation of each seed was recorded. Most seeds were always defecated in fecal pellets, with the exception of Aucuba japonica (the largest of the seeds studied), a seed of which was regurgitated on one occasion. Bulbuls defecate large seeds more rapidly than small seeds. The SRT of the last defecated seed, mean SRT, and standard deviation of SRT were significantly negatively correlated with seed size, fruit size, and seed weight, while SRT of the first defecated seed and water content were not correlated with any of the fruit characteristics examined. This suggests that Brown-eared Bulbuls are somehow able selectively to eliminate bulky seeds from the gut rapidly in order to overcome digestive limitations. If birds would prefer fruit species with large seeds that they can regurgitate and with short seed retention times in the gut, the results suggest that large seeds have the advantage of quantity of seed dispersed. Small seeds retained in the gut for longer have the advantage of b...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Relationship between seed retention time in bird's gut and fruit characteristics

Fukui

2003

Ornithol. Sci.

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“…SI ranges between 0 and 1; with low values indicating a high frequency of pecking and high values suggesting a high frequency of swallowing. This index suffers a possible shortcoming as some bird species usually regurgitate large seeds (Herrera 1984a;Sorensen 1984;Johnson et al 1985;Levey 1986;Worthington 1989;Levey & Grajal 1991). Birds species that regurgitate will show a smaller SI than species that do not.…”

Section: Frequency Of Fruit Sizes and Pecking Behaviour In The Fieldmentioning

confidence: 99%

“…This feeding behaviour provides additional advantages for birds as they do not carry the ballast of the seed and most of their gut volume can be used for processing digestible material (Sorensen 1984;Levey 1986Levey , 1987Worthington 1989;Levey & Grajal 1991).…”

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Fruit size in wild olives: implications for avian seed dispersal

et al. 1997

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1. The response of frugivorous birds to an enlargement of fruit size, and the consequences for both birds and plants, are analysed for the interaction between avian seed dispersers and olives (Olea europaea). 2. The enlargement of fruit size promotes a shift in frugivorous birds’ feeding behaviour, from swallowing fruits whole to pecking pieces of pulp. The relative frequency of olive consumption using each feeding behaviour was assessed by combining field data on frequency of appearance of olive pulp and seeds with data from laboratory trials. 3. Sardinian Warblers (Sylvia melanocephala) and European Robins (Erithacus rubecula) were mainly peckers both on cultivated and wild olives. Blackcaps (Sylvia atricapilla) consumed wild olives mainly by swallowing but consumed cultivated olives (larger than the wild ones) primarily by pecking. Song Thrushes (Turdus philomelos) were primarily swallowers of both types of fruits. 4. Laboratory trials with Song Thrushes, Blackcaps and European Robins showed that: (a) all were able to peck fruits; (b) fruit size determined a shift from swallowing to pecking, as pecking frequency increased with the enlargement of the fruit size; (c) all the species had an increased fruit handling failure rate when trying to swallow increasingly large fruits; and (d) from the birds’ perspective, small shifts in fruit size may have important consequences on fruit profitability. 5. Pecking on olives turns the mutualistic fruit–frugivore interaction into a fruit‐pulp predator interaction, thus arising a conflict between the plant and frugivorous birds. 6. This study shows that heavy dependence on fruit is not always simply related to seed dispersal. The same frugivorous bird species can act as a seed disperser or a pulp predator for the same plant species. The threshold between these roles is highly influenced by the ratio gape size/fruit size.

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Seed handling in chimpanzees (Pan troglodytes) and redtail monkeys (Cercopithecus ascanius): Implications for understanding hominoid and cercopithecine fruit-processing strategies and seed dispersal

Lambert

1999

Am. J. Phys. Anthropol.

144

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Primates are confronted with an array of constraints in feeding on fruit, including the removal of adhesive, energy-rich pulp from seeds. In this paper, I discuss how primates meet this challenge and present data on the fruit-processing and seed-handling behavior of chimpanzees and redtail monkeys in Kibale National Park, Uganda. These data are then related to these species' services as seed dispersers. Particular attention was paid to the methods by which primates removed pulp from seeds, the density of seed clumps that they deposited (by spitting, dropping, or defecating) to the forest floor, and the distance seeds were moved from parent trees. Distance and density differences in chimpanzee and redtail seed dispersal resulted from distinct fruit-processing and seed-handling methods. It was observed, in general, that redtail monkeys engaged in fine oral processing and were seed spitters: most seeds were dispersed in close proximity to parent trees (84% of spat seeds < 10 m of parent tree), and deposited singly (100% seeds spat singly). In contrast, chimpanzees were coarse fruit processors and seed swallowers: seeds were defecated in denser clumps (e.g., a mean of 149 large seeds/dung sample and hundreds of small seeds/dung sample), far from parent trees. I evaluate the factors that shape patterns of fruit processing in hominoids and cercopithecines, and argue that the observed seed handling differences can be attributed to differences in digestive retention times, oral anatomy, and alternative mechanisms by which to avoid the cost of seed ballast.

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Evolutionary Implications of Fruit-Processing Limitations in Cedar Waxwings

Cited by 109 publications

References 71 publications

Relationship between seed retention time in bird's gut and fruit characteristics

Relationship between seed retention time in bird's gut and fruit characteristics

Fruit size in wild olives: implications for avian seed dispersal

Seed handling in chimpanzees (Pan troglodytes) and redtail monkeys (Cercopithecus ascanius): Implications for understanding hominoid and cercopithecine fruit-processing strategies and seed dispersal

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