Bombycilla Cedrorum Research Articles

Seed Dispersal of the Mistletoe Psittacanthus schiedeanus by Birds in Central Veracruz, Mexico1

Mistletoes are hemiparasitic plants that frequently depend on frugivores for seed dispersal; yet their seed dispersal ecology is still poorly known. The mistletoe Psittacanthus schiedeanus (Loranthaceae) was studied for a five-month period in cloud forest remnants in central Veracruz, Mexico, to determine its seed dispersal ecology. We hypothesized that dispersal ecology of this mistletoe species is directly affected by the fruit-eating bird abundance, and asked if this species is following the high-investment strategy as suggested by Godschalk (1983). To evaluate this, we determined the morphological and nutritional characteristics of mistletoe fruit, the availability of ripe fruits along the mistletoe fruiting phenology, and the abundance of fruit-eating birds. Because P. schiedeanus is dispersed by generalist rather than specialist birds, we asked if this mistletoe species is ripening fruits during the fruit scarcity time (with highest possibilities of being consumed and dispersed by birds). We compared P. schiedeanus ripe fruit production to the cloud forest tree leaf fall and fruit production. Psittacanthus schiedeanus matures its nutritious fruits from November to April, with a peak of abundance in January and February. We found a synchrony between the abundance of P. schiedeanus ripe fruits and the abundance of Gray Silky-flycatchers (Ptilogonys cinereus) and Social Flycatchers (Myiozetetes similis); however, this was not the case with Cedar Waxwings (Bombycilla cedrorum), although these birds play an important role in the mistletoe dispersal. The fruiting pattern of P. schiedeanus, together with the fact that it is an important food resource for generalist rather than specialist frugivorous birds, suggest that this mistletoe is using the nutrient investment strategy to attract dispersers during a time of fruit scarcity.

A Simple Method for Tracking Vertebrate-Dispersed Seeds

Tracking vertebrate-dispersed seeds from parent plant to deposition site remains a primary obstacle to understanding the ecological and evolutionary consequences of seed dispersal. We evaluate a new and simple technique for tracking seeds. Fluorescent microspheres (15 μm diameter) are applied to fruits and later recovered in fecal material associated with the fruits’ seeds. Trials with captive Cedar Waxwings (Bombycilla cedrorum) demonstrated that (1) percentage recovery of microspheres is high, (2) all defecations containing seeds also contain microspheres, (3) relatively few microspheres are recovered in defecations not containing seeds, and (4) presence of microspheres on fruits does not affect fruit choice. Field trials with five species of fruits demonstrated that, after ∼30 d under full sun and high temperatures, photodegradation limits one’s ability to detect microspheres. The field trials also showed that an anti-transpirant applied with the microspheres allows them to adhere to fruits without deterring fruit consumption or damaging fruits and that microspheres can be found in fecal samples of wild birds. Our technique is likely to be applicable to any study in which it is necessary to link fecal material with a particular source of food or an individual animal.

A SIMPLE METHOD FOR TRACKING VERTEBRATE-DISPERSED SEEDS

Tracking vertebrate-dispersed seeds from parent plant to deposition site remains a primary obstacle to understanding the ecological and evolutionary consequences of seed dispersal. We evaluate a new and simple technique for tracking seeds. Fluorescent microspheres (15 μm diameter) are applied to fruits and later recovered in fecal material associated with the fruits’ seeds. Trials with captive Cedar Waxwings (Bombycilla cedrorum) demonstrated that (1) percentage recovery of microspheres is high, (2) all defecations containing seeds also contain microspheres, (3) relatively few microspheres are recovered in defecations not containing seeds, and (4) presence of microspheres on fruits does not affect fruit choice. Field trials with five species of fruits demonstrated that, after ∼30 d under full sun and high temperatures, photodegradation limits one’s ability to detect microspheres. The field trials also showed that an anti-transpirant applied with the microspheres allows them to adhere to fruits without det...

The Cyanogenic Glycoside Amygdalin Does Not Deter Consumption of Ripe Fruit by Cedar Waxwings

Cyanogenic glycosides are common secondary compounds in ripe fruits that are dispersed by birds. These substances are toxic to some mammals. We examined the repellent effect of amygdalin, a cyanogenic glycoside, on Cedar Waxwings (Bombycilla cedrorum). Amygdalin did not reduce food ingestion in Cedar Waxwings, even at relatively high concentrations. In addition, these birds did not exhibit preference for amygdalin-free over amygdalin-containing fruit. Cedar Waxwings given artificial food that contained four times the amount of amygdalin found in some wild fruits ingested the equivalent of 5.5 times the oral lethal dose for rats in 4 h without exhibiting any external signs of toxicity. Amygdalin ingestion appeared to have a negative effect on nitrogen retention and food assimilation. However, when nitrogen retention and food assimilation were recalculated assuming that all amygdalin ingested was excreted intact, these negative effects disappeared. The presence of large amounts of unhydrolyzed amygdalin in the excreta of waxwings fed on amygdalin-laced food confirmed our conjecture that amygdalin was excreted intact. We hypothesize that in Cedar Waxwings, amygdalin is absorbed in the intestine but is not hydrolyzed by endogenous enzymes and thus is excreted intact in urine. The apparent lack of repellent effects of amygdalin in Cedar Waxwings suggest that toxicity data for rats and humans may be a poor predictor for the deterrent effect of fruit secondary compounds on frugivorous birds. Many hypotheses that have been posed to explain the presence of secondary compounds in ripe fruit assume that these substances have repellent/ toxic effects on avian seed dispersers. For some compounds, such as amygdalin and other cyanogenic glycosides, this assumption may not be valid.

Do Avian Frugivores Absorb Fruit Sugars Inefficiently? How Dietary Nutrient Concentration Can Affect Coefficients of Digestive Efficiency

Fruit-eating birds are thought to inefficiently digest and/or assimilate nutrients from fruits. Contradicting this established premise, I found that Cedar Waxwings Bombycilla cedrorum and three thrush species absorbed fruit sugars efficiently, comparable to levels of sugar assimilation shown by nectar-feeding birds. Relatively low sugar digestive efficiencies by birds eating Lonicera morowii fruit could be explained by the especially low sugar solute concentration of this fruit's pulp. Sugar digestive efficiency is a proportional measure of sugar extraction from ingested sugar solutions. When most ingested water is excreted with unabsorbed sugars, digestive efficiency will decline as fruit sugar concentration decreases if sugars are reduced to relatively constant, minimum concentrations in excreted water. Under this circumstance, fecal nutrient concentration may be more appropriate for comparisons of how well animals utilize nutrients from foods that differ in their concentrations of dissolved or dispersed nutrients. Efficient absorption of fruit sugars by Cedar Waxwings and thrushes contradicts the premise that sugary, bird-dispersed fruits challenge the digestive systems of avian frugivores so that nutrient utilization is impaired. Because simple sugars (glucose and fructose) are readily assimilated, digestive processing of sugary fruits is more rapid than processing of foods containing complex nutrients. Thus, fruits represent accessible, energy-rich foods from which nutrients are efficiently absorbed by avian frugivores.

Frugivorous birds, host selection and the mistletoe Psittacanthus schiedeanus, in central Veracruz, Mexico

Frugivorous birds play an important role in parasitic mistletoe transmission among host species. The foraging behaviour and host selection of Psittacanthus schiedeanus mistletoe fruit-eating birds was studied in cloud forest remnants in Central Veracruz, México. Cedar waxwings, Bombycilla cedrorum, gray silky-flycatchers, Ptilogonys cinereus, and social flycatchers, Myiozetetes similis, eating ripe whole mistletoe fruits and defecating or regurgitating the seeds were observed. That variation in host species selection by frugivorous birds had a direct effect on mistletoe dispersion was hypothesized. To test whether mistletoe host species are visited in proportion to their abundance (total number of trees), or infested-tree abundance (total number of infested trees), or abundance of mistletoes (total number of individual mistletoe plants in each host species), the number of trees, infested trees and individual mistletoe plants were recorded. Tree abundance, infested-tree abundance and mistletoe abundance were different among host species. Frequency of birds' visits to host species varied depending on the tree, infested-tree, or mistletoe abundance. Liquidambar styraciflua was the most abundant host species with the highest number of infested trees and individual mistletoe plants, but Persea americana and Crataegus mexicana host species had the highest number of individual mistletoe plants in each tree. Our data suggest that L. styraciflua was the most selected host species by the three frugivorous birds. Host selection by birds is one behavioural factor in explaining differences in prevalence among host species, and variation in infection levels among individuals of one host species.RESUMEN. Las aves frugívoras juegan un importante papel en la transmisión de muérdagos parásitos hacia sus árboles hospederos. La conducta de forrajeo y selección de hospedero de aves consumidoras de frutos del muérdago Psittacanthus schiedeanus fueron estudiados en remanentes de bosque mesófilo de montaña del Centro de Veracruz, México. Bombycilla cedrorum, Ptilogonys cinereus and Myiozetetes similis fueron observados consumiendo frutos maduros enteros y defecando o regurgitando las semillas. Hipotetizamos que la variación en la selección de la especie hospedera por las aves frugívoras tiene un efecto directo en la dispersión del muérdago. Para probar si las especies de árboles hospederos son visitadas en proporción a su abundancia (número total de árboles), o la abundancia de hospederos infectados (número de árboles infectados) o la abundancia de muérdagos (número total de plantas individuales de muérdago en una sola especie de árbol); el número de árboles, árboles infestados y plantas de muérdago fueron registradas. La abundancia de árboles, de árboles infestados y de plantas de muérdago fue diferente entre las especies de árboles estudiadas. La frecuencia de visitas de las aves a las especies hospederas varió de acuerdo a la abundancia de árboles, de árboles infestados y de plantas de muérdago. Liquidambar styraciflua fue la especie hospedera más abundante con el mayor número de árboles infestados y abundancia de muérdagos, pero las especies Persea americana y Crataegus mexicana presentaron el mayor número de plantas de múerdago por árbol. Nuestros datos sugieren que L. styraciflua fue la especie hospedera más seleccionada por las aves frugívoras. La selección de hospederos por las aves es uno de los factores conductuales que explican las diferencias en prevalencia entre especies de hospedero, y la variación en los niveles de infestación entre individuos de una de las especies de hospedero.

Test, rejection, and reformulation of a chemical reactor-based model of gut function in a fruit-eating bird.

We explored modulation of retention time in cedar waxwings (Bombycilla cedrorum) by feeding them diets varying in hexose concentration. Our goals were to (1) test three predictions of a chemical reactor-based model of how guts might respond optimally to diet shifts; (2) determine whether modulation of retention time can occur quickly, thereby facilitating rapid changes in diet; (3) tease apart the relative influence of ingestion rate and nutrient concentration on retention time; and (4) examine the degree of axial mixing in the intestine and its relationship with retention time. The model's predictions were rejected: mean retention time did not decrease, ingestion rate did not increase, and glucose assimilation efficiency did not decrease with increased hexose concentration of the diet. Instead, birds displayed maximal intake rate at intermediate sugar concentration, and mouth to cloaca mean retention times increased with hexose concentration. Significant modulation of retention time occurred quickly, within 3 h of exposure to a different diet. Birds did equally well in terms of total energy assimilated on diets differing 3.3-fold in hexose concentration (from 500 mmol/L to 1660 mmol/L) but showed reduced intake when fed food with low hexose concentration (110 mmol/L). Far more variation in retention time was explained by direct effects of ingestion rate than by direct effects of hexose concentration. Finally, a gut dispersion index that measured degree of axial mixing was positively correlated with mean retention time, indicating that higher retention times are accompanied by increased axial mixing. We propose a modification of the assumptions of the original model. The resulting "osmotic constraint" model better captures the interaction between feeding rate and digestive function in fruit-eating birds.

Farmland birds in southern Ontario: field use, activity patterns and vulnerability to pesticide use

The use of cropfields by birds is largely unknown in southern Canada and consequently the risk incurred by pesticide use on bird populations cannot be adequately characterised. The activity patterns and relative interior to edge use of bird species were examined for four crops in southern Ontario to assess the susceptibility of different species to pesticide use. Altogether 138 species were identified in the four crops over the 2 year period but only 25 species were recorded during 50% of visits in at least 1 month: 14 in corn ( Zea mays L.), 16 in soybean ( Glycine max L. Merr.), 14 in apple ( Malus spp.) orchards and eight in vineyards ( Vitis spp.). Territorial behaviour was an important activity for several species from May through July in the four crops. Nesting was confirmed in May, June and July for most species, with the exception of American Goldfinch Carduelis tristis, Chipping Sparrow Spizella passerina and Cedar Waxwing Bombycilla cedrorum which nested in August/September. Foraging was the most important activity for most species in all months (7/10 species in May, 6/8 species in June, 4/8 species in July, 5/8 August/September). Few fledgling young were observed. Most species used field edges consistently more often than expected in corn and soybean fields, according to the edge/interior ratio, Yellow Warbler Dendroica petechia being the exception. In apple orchards, relatively few species differentiated between edge and interior. Based on their frequency of occurrence (>50%), behaviour and temporal coincidence with pesticide applications, 13 species were considered most at risk: Killdeer Charadrius vociferus, Horned Lark Eremophila alpestris, American Crow Corvus brachyrhynchos, American Robin Turdus migratorius, European Starling Sturnus vulgaris, Chipping Sparrow, Vesper Sparrow Pooecetes gramineus, Savannah Sparrow Passerculus sandwichensis, Song Sparrow Melospiza melodia, Red-winged Blackbird Agelaius phoeniceus, Common Grackle Quiscalus quiscala, Brown-headed Cowbird Molothrus ater and Barn Swallow Hirundo rustica. The latter species, because of its foraging habit, is less likely to be exposed to pesticides. This study was important to identify focal species that can be used for detailed investigations on exposure to pesticides.

Digestive adjustments in cedar waxwings to high feeding rate

Birds may dramatically increase their food intake during migratory periods or during winter. We tested the hypotheses that when birds are hyperphagic, (a) their digesta retention time and extraction efficiency will not change compared with that of birds feeding at reduced rates, (b) their total capacity for breakdown and absorption of nutrients will increase, and (c) the mechanism responsible for the increase in total capacity will be an increase in amount of intestine rather than an increase in intestinal tissue-specific enzyme activity or nutrient transporter activity. We measured gut anatomy, retention time of digesta, enzyme hydrolysis rates, nutrient absorption rates, and digestive efficiency in individual cedar waxwings (Bombycilla cedrorum) acclimated to –20°C or +21°C. Compared with cedar waxwings held at +21°C, waxwings acclimated to –20°C more than tripled their daily food intake. Mass of digestive organs increased by 22–53%, but rates of enzyme activity and nutrient uptake per unit of small intestine did not change significantly. Retention time of digesta declined slightly, and there was a small decrease in digestive efficiency. As predicted, the main adjustment to increased energy requirements and food intake was an increase in gut length, mass, and volume which largely compensated for increased digesta flow at high intake rates. However, we detected a small reduction in retention time and digestive efficiency in waxwings with high intakes which suggests that these waxwings may be unable to further increase their gut size (i.e., that the increase in gut size was maximal). If adjustments involving gut size require weeks of acclimation time, migration patterns and the pace of migration in birds could be influenced by time required for preparation of the gut. J. Exp. Zool. 283:394–407, 1999. © 1999 Wiley-Liss, Inc.

Ecological and evolutionary implications of energy and protein requirements of avian frugivores eating sugary diets.

To assess how the high-sugar/low-protein content of fruit diets affects digestive function and nutrition of frugivorous birds, I compared intake, passage rate, sugar utilization, protein requirements, and mass changes of cedar waxwings (Bombycilla cedrorum), American robins (Turdus migratorius), and wood thrushes (Hylocichla mustelina) fed synthetic diets simulating the range of sugar (6.6%, 12.4%, and 22.0% solutes) and protein (4.5%, 3.0%, and 1.5% of dry matter) content of bird-dispersed fruits. The dietary emphasis on sugary fruits by cedar waxwings suggests the potential for digestive and physiological specializations to this food type. All birds increased volumetric food intake and passage rates as sugar concentration declined. Birds completely (22.0%-12.4% sugar solute concentration) or incompletely (12.4%-6.6% sugar solute concentration) compensated for dietary dilution. Cedar waxwings consumed each diet at higher rates than did thrushes, as they do when eating sugary fruits, demonstrating that interspecific differences in ingestion rates of sugary fruits are a consequence of nutrient composition, rather than seed bulk or secondary compounds of fruits. Passage rate was not responsible for interspecific differences in short-term food intake rate, implicating gut morphology as the key functional feature limiting intake. Most sugary fruits are nutritionally deficient in apparent protein for thrushes but are nutritionally adequate in protein for cedar waxwings because of this species' relatively high intake rates and low protein requirements. The digestive systems of frugivorous birds respond flexibly to dietary sugar concentration, but protein content of fruits can present a nutritional limitation, potentially influencing the proportions of fruit and animal foods in birds' diets.

Contrasting digestive strategies of fruit‐eating birds

1. Sugary fruits dominate the annual diet of Cedar Waxwings (Bombycilla cedrorum), whereas lipid‐rich foods dominate the diets of frugivorous thrushes. Nutrient utilization and preferences of Cedar Waxwings and thrushes fed sugary and lipid‐rich natural fruits were assessed to ascertain the potential for nutrient‐based specializations that could explain diet selection in nature. 2. Compared allometrically, Cedar Waxwings showed higher rates of sugar assimilation from sugary fruits than did thrushes, by virtue of higher intake rates, and achieved the highest energy assimilation rates when eating a sugary fruit. A trade‐off to this digestive strategy appears to be less efficient utilization of lipids when eating exclusively lipid‐rich fruits. 3. Thrushes digested lipids more efficiently than Cedar Waxwings as a function of intake rate or estimated retention time, and thrushes achieved the highest energy assimilation rates when eating a lipid‐rich fruit. Specialization to a diet rich in lipids appears to limit the rate at which sugary fruits can be processed. 4. Within each bird species, sugar digestive efficiencies were high and were not reduced at higher intake rates. Lipids were consumed at lower rates than sugars, and lipid digestive efficiencies declined with increasing intake rates. Frugivorous birds modulated digestive processing of fruits according to the time needed for efficient digestion and/or absorption of sugars and lipids, respectively. 5. Rate of nitrogen intake, not sugar assimilation, positively influenced body mass changes of birds. Sugary fruits appear nutritionally rich in energy, but limited in protein for avian frugivores. Relatively high intake rates and low protein requirements of Cedar Waxwings suggest that specialization to sugary, low‐protein diets involves traits that facilitate acquisition and conservation of protein/amino acids. 6. Cedar Waxwings and thrushes show digestive specialization to the utilization of sugars and lipids, respectively, as dominant dietary nutrients. These traits explain patterns of food selection by these birds in the laboratory and in nature. Variation in the value of particular fruit nutrients to different birds renders the dietary descriptor of ‘frugivore’ ambiguous in a nutritional context.

CONTROL OF GUT RETENTION TIME BY SECONDARY METABOLITES IN RIPESOLANUMFRUITS

We tested whether compounds in ripe Solanum americanum fruits affect gut retention time of S. americanum seeds in Cedar Waxwings (Bombycilla cedrorum). Glycoalkaloids were of special interest because they commonly occur in ripe Solanum fruits and are associated with diarrhea in humans. Also, we determined the influence of gut retention time and the presence/absence of two glycoalkaloids, α-solasonine and α-solamargine, on germination of S. americanum seeds. In one trial, we measured seed retention times of 10 waxwings fed three types of artificial fruits, Control (containing no secondary metabolites), Low Concentration (containing low concentrations of α-solasonine and α-solamargine, matching those in ripe S. americanum fruit), and Extract (containing an ethanol extract of ripe S. americanum fruits, with many unidentified secondary metabolites). Seeds in Low Concentration fruits were not defecated more quickly than those in Control fruits, but seeds in Extract fruits were. Thus, ripe S. americanum fruits contain a chemical or chemicals with a laxative effect. Also, seeds from Control fruits were deposited in more defecations and at lower densities in each defecation than those from Extract fruits. In a second trial, we compared retention times of seeds in control fruits and in fruits with high concentrations of glycoalkaloids, typical in ripe fruits of other Solanum species. These high concentrations had a significant constipative effect on seed passage. Percentage germination and mean germination time of defecated seeds were not influenced by mean retention time in waxwing guts. However, proportionately fewer seeds germinated from Low Concentration fruits than from Control fruits. These results suggest that plants have more control over seed processing by frugivores than generally acknowledged. Secondary metabolites in ripe fruits can increase or decrease retention time and thereby influence seed deposition patterns (e.g., number of defecations with seeds, number of seeds per defecation, and presumably, dispersal distance).

Influence of Seed Processing by Frugivorous Birds on Germination Success of Three North American Shrubs

Abstract Coevolutionary models of the interactions between fruiting plants and avian seed dispersers have been influenced by the assumption that regurgitation and defecation of seeds have diffferent effects on seed coats, and consequently seed germination. We evaluated how the manner of seed processing affects seed germination by feeding fruits of three bird-dispersed shrubs, spicebush (Lindera benzoin), chokecherry (Prunus virginiana), and arrowwood (Viburnum dentatum), to captive cedar waxwings (Bombycilla cedrorum) and thrushes (Turdus migratorius, Hylocichla mustelina, Catharus guttatus and C. minimus). Cedar waxwings defecate all seeds, whereas thrushes regurgitate most seeds. For all three shrub species and all five bird species, there were no differences in germination success between seeds manually cleaned of pulp, and cleaned, bird-passed seeds, regardless of whether seeds were regurgitated or defecated. However, seeds of Lindera and Prunus that were defecated by cedar waxwings and planted with f...

A Glycoalkaloid in Ripe Fruit Deters Consumption by Cedar Waxwings

--Many ripe fruits contain chemicals that presumably protect them against attacks by frugivores that do not disperse seeds. These secondary metabolites may be generally toxic, representing an evolutionary compromise between defense from pathogens and attraction of seed dispersers (the General Toxicity hypothesis). Alternatively, they may be nontoxic to seed dispersers and simultaneously to vertebrate frugivores that do not disperse seeds (the Directed Toxicity hypothesis). To tease apart these hypotheses, we tested whether consumption of artificial fruit agar by captive Cedar Waxwings (Bombycilla cedrorum) was reduced by the presence of c•-solamargine, a glycoalkaloid common in solanaceous fruits. We recorded consumption of three artificial fruit types differing in c•solamargine concentration and a control fruit that lacked c•-solamargine. Waxwings were strongly and equally deterred by all concentrations of c•-solamargine. These concentrations, 0.1, 0.2, and 0.3% wet mass, are commonly found in some Solanum fruits. In a second trial, we addressed another hypothesis, the Nutrient-Toxin Titration hypothesis, which predicts that the deterrent effects of c•-solamargine can be overridden by highly nutritious fruit pulp. We offered waxwings three types of artificial fruits that varied in nutrient concentration but not in c•-solamargine concentration. Nutrient content had no effect on consumption when c•-solamargine was present. In summary, our results are inconsistent with both the Directed Toxicity and the Nutrient-Toxin Titration hypotheses. Received 24 June 1996, accepted 27 August 1997. BIRDS ARE PRIMARY CONSUMERS of fruits and dispersers of seeds. At one interface of this mutualistic interaction is the match between the nutritional requirements of birds and the chemical content of fruits (Martinez del Rio and Restrepo 1993). Nutrients of particular interest to researchers have been lipids, proteins, and carbohydrates (Martinez del Rio et al. 1989, Worthington 1989, Karasov and Levey 1990, Levey and Grajal 1991, Place and Stiles 1991, Witmer 1994, Afik and Karasov 1995). Largely overlooked are secondary metabolites, which promise to yield new insights for studies of fruit-frugivore interactions, as they have for studies of plant-herbivore interactions (Cipollini and Levey 1997b). For example, some secondary metabolites in ripe fruit pulp are paradoxical because they appear to deter fruit consumption-and hence seed dispersal--by seed-dispersing birds (Herrera 1982, Cipollini and Levey 1997c). How can their presence be explained in the context of mutualism? Here, we use Cedar Waxwings (Bombycilla cedrorum) to test two • E-mail: dlevey@zoo.ufl.edu 2 Present address: Department of Biology, 430 Berry College, Rome, Georgia, 30149, USA sets of hypotheses, formally proposed by Cipollini and Levey (1997c), that address the evolutionary significance of fruit secondary metabolites. The Directed Toxicity hypothesis tates that secondary metabolites in ripe fruit are to vertebrate frugivores that do not disperse seeds but are not to those that disperse seeds (Janzen 1975). This hypothesis gains credence from observations that seed-dispersing birds consume a wide range of toxic fruit (Martin et al. 1951, Kear 1968, Heiser 1969, Herrera 1982, Jordano 1987) and appear to be broadly tolerant of naturally occurring toxins (Herrera 1985). Alternatively, the General Toxicity hypothesis posits that secondary metabolites are repellent o all frugivores, regardless of how they treat seeds (Cipollini and Levey 1997c). This hypothesis is bolstered by studies concluding that variation in behavior and morphology among frugivores cannot account for variation in fruit traits (Herrera 1992, Jordano 1995, Tamboia et al. 1996). The Nutrient-Toxin Titration and Removal Rate hypotheses focus on interspecific variation among plants and the possible interactions of nutrient content, secondary chemistry, mi-

Do Seeds Hinder Digestive Processing of Fruit Pulp? Implications for Plant/Frugivore Mutualisms

The seeds of bird-dispersed fruits could impose significant costs on frugi- vores if seed bulk reduces the effective capacity of the gut and, hence, reduces the rate of nutrient intake. This has led to the notion that avian frugivores pass food through their di- gestive tracts rapidly to minimize the effects of seeds on nutrient acquisition. Consequently, avian frugivores are thought to utilize fruit sugars inefficiently, because this permits higher intake and sugar-assimilation rates from a supposedly energy-dilute food. I evaluated the influence of seed bulk on intake and absorption of sugars from chokecherry fruits (Prunus virginiana) by Cedar Waxwings (Bombycilla cedrorum), American Robins (Turdus migratorius ), Wood Thrushes (Hylocichla mustelina), Gray-cheeked Thrushes (Catharus minimus), and Her- mit Thrushes (Catharus guttatus). I compared Cedar Waxwings with thrushes to determine if they differed in how seed bulk affects digestion of fruit. Cedar Waxwings have higher mass-specific intake rates of sugary fruits than do thrushes; because waxwings defecate all seeds, whereas thrushes regurgitate many seeds, the difference in intake of sugary fruits between waxwings and thrushes may result from ingestion/fruit-processing limitations as- sociated with mode of seed processing. For all species, seeds did not reduce rates of intake and sugar absorption from chokecherry fruit pulp. All birds assimilated sugars from choke- cherry fruits efficiently, and digestive processing of seeds did not reduce sugar absorption. Rates of fruit processing were closely tied to rates of sugar absorption, rather than to the physical composition of the diet. My results suggest that current models of digestive func- tion in avian frugivores are seriously flawed. Because differences in intake rates of sugary fruits between waxwings and thrushes were independent of the presence of seeds, these differences were not due to different modes of seed processing. Received 13 January 1997,

Test of a digestion optimization model: effects of costs of feeding on digestive parameters.

We tested predictions of a chemical reactor model of digestion by manipulating the short-term costs of feeding and then measuring the effect on digestive parameters. We compared residence time of digesta and extraction efficiency of glucose in cold-acclimated waxwings (Bombycilla cedrorum) feeding ad lib. and in birds whose costs of feeding were increased through the addition of intervals of time when they received no food. Such a feeding schedule simulated the ecological situation in which a frugivorous bird like a waxwing encounters food in patches and experiences nonfeeding periods as it searches for new preferred food patches. None of the results were consistent with the predictions of the optimal digestion model: extraction efficiency was independent of costs of feeding, and residence times did not increase as costs of feeding increased. This empirical evidence on the passage of digesta in waxwings suggests that movement of digesta in the guts of birds is much more complex than movement of material in an ideal chemical reactor. Tests of the optimal digestion model have involved manipulating food quality or the costs of feeding, and the conclusions are similar: compensatory modulation of retention time or digesta mixing and not rate of hydrolysis and absorption seem most important in maintaining the remarkably constant digestive efficiency.

Comparative Analysis of Habitat Selection, Nest Site and Nest Success by Cedar Waxwings (Bombycilla cedrorum) and Eastern Kingbirds (Tyrannus tyrannus)

-We compared nest success, habitat use and nest site selection of cedar waxwings (Bombycilla cedrorum) and eastern kingbirds (Tyrannus tyrannus) breeding in the same locations over a 3-yr period to determine if nest success differed between species, or with habitat or nest sites. Nest success was lower in waxwings in all 3 yr (3-yr average: 18% vs. 55%). Both species preferred hawthorns (Crataegus) as nest trees, but in neither species was nest success higher when nests were placed in hawthorns. Nest success did, however, vary with habitat structure: successful kingbirds nests were usually located in the most open habitat (i.e., lowest canopy cover and surrounded by the fewest trees), whereas failed waxwing nests were located in habitats with the densest vegetation. Habitats of failed kingbird and successful waxwing nests were intermediate and similar. Nest sites were very similar, except that waxwing nests were much more concealed in the nest tree's vegetation. However, neither cover nor other nest site variables differed between failed and successful nests within either species. A discriminant function analysis that used mainly habitat variables correctly classified 68% of failed waxwing and 64% of successful kingbird nests, but less than 50% of failed kingbird and successful waxwing nests. Thus, kingbirds and waxwings overlap extensively in habitat use and nest sites, but kingbirds prefer more open habitats, presumably because it allows them to detect predators and defend their nests. Waxwings prefer habitats with denser vegetation, presumably because they rely upon inconspicuous behavior to avoid nest predators. Failed kingbird nests were in waxwing-like habitats, suggesting a link between nest sites, habitats and parental behavior. We believe that the characteristic aggressive nest defense of kingbirds was the major reason for their higher nesting success.

Consequences of an Alien Shrub on the Plumage Coloration and Ecology of Cedar Waxwings

-Cedar Waxwings (Bombycilla cedrorum) with orange (instead of the normal yellow) tail bands have appeared in eastern North America in the last 35 years. Biochemical studies have implicated a dietary cause (Hudon and Brush 1989), specifically the fruits of Lonicera morrowii (Brush 1990), for this novel color variant. I show that rectrices replaced while Cedar Waxwings are feeding on L. morrowii fruits develop orange tips. Rectrices replaced subsequent to switching the diet of molting waxwings from L. morrowii fruits to dog chow were yellow, showing close temporal correspondence between dietary input of rhodoxanthin and the coloration of growing feathers. In the Ithaca vicinity, fruits of L. morrowii are eaten by wild Cedar Waxwings from June until mid-October. The extended pattern of availability and consumption of Lonicera in this region appears to explain my unique observations of adult Cedar Waxwings growing orange tails during the fall months. Cedar Waxwings maintained body condition and molted while on an extended diet of L. morrowii fruits (36 days for two birds and 64 days for two others). Three birds initiated tail molt while on this diet, including one that molted all of its flight feathers. These results emphasize the nutritional specialization of Cedar Waxwings to a diet of sugary, low-protein fruits, and show that molt occurs in an apparently normal manner when birds are eating a low-protein fruit diet. Received 30 September 1994, accepted 15 April 1995. CEDAR WAXWINGS (Bombycilla cedrorum) normally have a yellow terminal band on their tails. Within the past 35 years, Cedar Waxwings with orange tail bands have appeared in the northeastern United States and southeastern I Present address: Department of Zoology and Physiology, University of Wyoming, Laramie, Wyoming 82071, USA. E-mail: waxwing@uwyo.edu Canada (Yunick 1970, Hudon and Brush 1989, Pittaway 1991, Mulvihill et al. 1992). Carotenoid pigments (i.e. xanthophylls) cause the yellow tail bands of Cedar Waxwings (Hudon and Brush 1989), as well as the red tips of their secondaries (Brush and Allen 1963). The coloration of the novel orange-tipped rectrices of Cedar Waxwings is caused by the inclusion of a red carotenoid pigment (rhodoxanthin) in the FRONTISPIECE. Tail colors of Cedar Waxwings. Bird in upper left (Bird 1) was fed only Lonicera fruits during tail molt. Bird in upper right (Bird 2) was switched from Lonicera fruits to chow diet midway through tail molt. Bird in lower left is wild bird with orange tail band (Cornell University Vertebrate Collection [CVC] no. 30194; juvenile male, 9 November 1961, Chemung Co., New York). Bird in lower right is wild bird with normal yellow tail band (CVC no. 14422, adult male, 1 June 1942, Tompkins Co., New York).

Annual Diet of Cedar Waxwings Based on U.S. Biological Survey Records (1885-1950) Compared to Diet of American Robins: Contrasts in Dietary Patterns and Natural History

The diet of Cedar Waxwings (Bombycilla cedrorum) is described using records of gut contents collected by the U.S. Biological Survey. Cedar Waxwings eat more fruit than most other Temperate Zone birds, including one of the most frugivorous thrushes, the American Robin (Turdus migratorius; 84 vs. 57% fruit in their annual diets, respectively). Cedar Waxwings are almost exclusively frugivorous in the winter and early spring. During the spring period of fruit scarcity, flowers comprise a large portion of the diet of waxwings (44% of May diet). Cedar Waxwings eat aerial and vegetation-borne animal prey, whereas American Robins eat vegetation-borne and terrestrial prey. The fruits eaten by Cedar Waxwings are characterized by high sugar and low lipid content. American Robins, like other North Amer- ican thrushes, eat sugary and lipid-rich fruits, suggesting contrasting digestive strategies in waxwings and thrushes. This perspective is reinforced by the correspondence between these birds' diets, the timing of breeding in relation to availability of preferred foods, and flocking patterns. Received 24 February 1995, accepted 25 August 1995. ECOLOGISTS OFTEN equate caloric content of foods with nutritive value without considering the specific nutrient composition of foods and the digestive characteristics of consumers (e.g. Martin 1985). Such assessments assume that an- imals are similar in the ways that they process and assimilate foods and that digestion of var- ious nutrients does not vary among species. This perspective has probably resulted from the his- torical importance of energy in ecological the- ory (Elton 1927, Lindeman 1942, Schoener 1971, Krebs 1978, McKey 1975). Although knowledge of caloric content of foods can be informative in systems where animals have comparable di- gestive characteristics and foods are chemically similar (Pyke 1980), this approach ignores cru- cial information in comparisons between ani- mals with different digestive systems eating chemically diverse diets. Detailed comparisons of dietary habits can identify specializations to particular foods and corresponding limitations imposed by such adaptations (e.g. Walsberg

Evaluation of a methyl anthranilate formulation for reducing bird damage to blueberries

We evaluated the bird repellency of ReJeX-iT ® AG-36 which contains the active ingredient methyl anthranilate (MA). In a 14-day field trial in Michigan, MA applied at 16.1 kg ha −1 did not reduce bird damage overall, but did appear to offer some protection from 3 to 10 days post-treatment. After 10 days, however, bird damage more than doubled. In Florida, we applied MA at a rate of 32 kg ha −1 and then presented the fruit to individually caged cedar waxwings ( Bombycilla cedrorum). Berry consumption did not differ between treatment and control groups, but consumption of berries 72 h post-spray exceeded that of 24 h post-spray.