TY - JOUR
AU1 - Pryor, Gregory, S.
AU2 - Levey, Douglas, J.
AU3 - Dierenfeld, Ellen, S.
AU4 - Bosque,, C.
AB - Abstract For those few bird species that are exclusively frugivorous, the low protein content of fruits is likely a major nutritional constraint. Physiological mechanisms that allow strict frugivory remain enigmatic, but reduced protein requirements may suffice. We investigated protein requirements of Pesquet's Parrot (Psittrichas fulgidus), a highly specialized, obligate frugivore. Three isocaloric, fruit-based diets of varying protein content (6.1, 3.3, and 2.6% dry mass crude protein) were used in feeding trials lasting three to five days per diet. A minimum dietary protein requirement of 3.2% dry mass was estimated from balance trials. Endogenous nitrogen losses were 0.05 gN kg−0.75 day−1 and nitrogen equilibrium occurred at 0.32 gN kg−0.75 day−1. Those values are extremely low compared to those of granivorous and omnivorous bird species, but higher than those of nectarivorous species. In terms of nitrogen losses and requirements, Pesquet's Parrot most closely parallels the highly frugivorous Cedar Waxwing (Bombycilla cedrorum). Thus, reduced protein requirements appear to play an important physiological role in ability of highly frugivorous birds to subsist on fruit diets. Although fruits provide a rich source of easily assimilated carbohydrates, they are notoriously low in protein (Morton 1973, White 1974, Berthold 1976, Mattson 1980, Snow 1981, Thomas 1984, Jordano 1992). Furthermore, nonprotein nitrogen (N) in the form of free amino acids and secondary metabolites is common in fruit (Herrera 1982, Cipollini and Levey 1997) and is not discriminated from protein N in traditional Kjeldahl analysis (Izhaki 1993). Thus, true protein content of fruit is likely even lower than most published estimates. Given the low protein content of fruits, it is not surprising that very few species of birds can subsist on a diet of exclusively fruits (Berthold 1976, Snow 1981, Holthuijzen and Adkisson 1984, Bairlein 1987, Izhaki and Safriel 1989). Although the physiological mechanisms that allow some birds to be strictly frugivorous are not fully understood, proposed mechanisms include high ingestion rates (Sorensen 1984, Bairlein 1987, Izhaki and Safriel 1989, Karasov and Levey 1990, Levey and Grajal 1991, Levey and Duke 1992, Levey and Karasov 1992), short gut retention times (Herrera 1984, Martinez del Rio et al. 1989, Levey and Grajal 1991, Levey and Duke 1992, Levey and Karasov 1994), and low protein requirements (Witmer 1998, Witmer and Van Soest 1998). We investigated protein requirements of an obligate frugivorous bird, Pesquet's Parrot (Psittrichas fulgidus). In particular, we examined two related physiological responses (i.e. endogenous N losses, which represent N lost via urine and feces; and N equilibrium, which occurs when N intake equals N excretion) of that obligate frugivore to the low protein content of fruits. Pesquet's Parrot is a highly specialized, obligate frugivore that feeds only on a few species of figs (Forshaw and Cooper 1989, Mack and Wright 1998). This threatened species is endemic to the highland rainforests of New Guinea and has a featherless face and elongate beak, which are thought to be adaptations for preventing head feathers from matting when it feeds on the sticky interior of large, ripe figs (Homberger 1980, Forshaw and Cooper 1989). In captivity, Pesquet's Parrots are best maintained and can breed when fed a low protein diet comprising almost entirely fruit (De Jager 1976, Homberger 1980, Thursland and Paul 1987, Low 1990, 1991; Sweeney 1999). Thus, we predicted that Pesquet's Parrot would have a low dietary protein requirement (i.e. low endogenous N losses and low N equilibrium), relative to omnivorous and granivorous species. Because Pesquet's Parrot evolved from a granivorous ancestor and is distantly related to other obligately frugivorous birds (Thompson 1899, Dyck 1976, Homberger 1980, 1991, Van Dongen and De Boer 1984, Forshaw and Cooper 1989, Courtney 1997), it provides an opportunity to explore physiological adaptations to frugivory in a lineage largely independent of previously examined lineages. Methods Feeding trials were conducted from 15–30 May 1997 at the Wildlife Conservation Society's Wildlife Survival Center, located on St. Catherines Island, Georgia. Three adult, nonmolting Pesquet's Parrots with a mean (±SD) initial body mass of 757 ± 58 g were used. Prior to the start of trials, birds were moved from large, outdoor enclosures to three indoor cages (∼1 m3) and acclimated for 10 days. All cages were disinfected with chlorhexidine before use, and food bowls were disinfected with a bleach solution before each use. Temperature remained constant at 25°C and a natural photoperiod (via skylights) was supplemented with daytime fluorescent lighting (12 L:12 D). The maintenance diet (Diet 1 in Table 1) was fed during the acclimation period and between feeding trials. Water was available ad libitum, and birds were in the same room during all phases of the study. Table 1. Composition of the fruit-based diets used in Pesquet's Parrot feeding trials Open in new tab Table 1. Composition of the fruit-based diets used in Pesquet's Parrot feeding trials Open in new tab Three isocaloric diets (calculated Gross Energy = 0.91 kcal g−1 wet mass [wm]; 3.78 kcal g−1 dry mass [dm]) of varying crude protein (CP) content (6.1, 3.3, and 2.6% dm CP; Table 1) were fed as a homogenized slurry to the birds. Those protein levels approximate the range reported for wild figs (range = 2.1 to 8.8% dm CP: Janzen 1979, Thomas 1984, Wrangham et al. 1993). The sequence and duration of feeding trials was 6.1% (5 days), 2.6% (4 days), and 3.3% (3 days) CP, respectively, with two days of maintenance diet (6.1% CP) between trials. Dietary amino acid levels for 18 amino acids were determined with an automatic amino acid analyzer and an external standard. That was necessary because a deficiency of a single essential amino acid can result in increased N equilibrium, and thus an increased protein requirement (Maynard et al. 1979, Klasing 1998). Conversely, an excess of nonessential amino acids can cause increased endogenous N losses. Amino-acid profiles of diets used in this study were similar but differed from a high quality granivorous bird diet (Table 2). That was not considered problematic because parrots had been maintained for years and reproduced on a diet similar to Diet 1 (Tables 1, 2) and appeared healthy. Table 2. Amino acid composition (percentage of total protein) of experimental diets. Dashes indicate undetectable levels of amino acids Open in new tab Table 2. Amino acid composition (percentage of total protein) of experimental diets. Dashes indicate undetectable levels of amino acids Open in new tab Feeding times occurred at 0630, 1200, and 1600 EST, and food was removed for the night at 2100. Diets were prepared daily because they were fruit-based and spoiled quickly. To test for evaporative water loss, a control bowl of food was placed in the same room as the caged birds daily and its mass monitored. Because water loss from food was not detectable during any of the feeding trials, no corrections were made for evaporation. Samples of the diet were collected daily for N analysis. Uneaten food was collected at each feeding and weighed to determine intake. Excreta collections were made from plastic sheets on the cage floors at each feeding and when food was removed for the night. Because potential loss of gaseous N from the alkaline excreta (pH 8.0) was a concern (Brice and Grau 1991), excreta were frozen immediately after collection to minimize N loss via ammonia volatilization (Manoukas et al. 1964, Blem 1968, Dawson and Herd 1983). Body mass was monitored during feeding trials. Birds were weighed before first feeding each day, when amount of food in their digestive tracts was minimal. We were concerned that frequent weighings would stress the birds because they are rarely handled. Thus, to weigh a bird, a pan balance fitted with a perch was placed in the cage. After the bird moved onto the perch, its body mass was recorded and the balance removed. The birds became accustomed to that routine after a few days and did not appear stressed. Dry mass of diet and excreta samples was determined by freeze drying, and N content of dried samples was determined by standard Kjeldahl technique (Association of Official Analytical Chemists 1984). Instead of using the standard nitrogen-to-protein conversion factor of 6.25, which is based on animal tissue (Maynard et al. 1979), we used a conversion factor of 4.05 to calculate CP. That was necessary because fruits have lower conversion factors than animal tissues (Izhaki 1993, Conklin-Brittain et al. 1999). The 4.05 conversion factor is based on 27 species of wild fruits (Izhaki 1993). To compare feed intake and excreta among birds and diets, ANOVA were used with Scheffe's post-hoc tests. Intake and excreta values were scaled to metabolic body mass (kg0.75) for interspecific comparisons (Robbins 1993). To detect changes in body mass of birds among feeding trials, percentage change in body mass was calculated and arcsin transformed (Sokal and Rohlf 1981). ANOVA with Scheffe's post-hoc tests were then used to compare changes in body mass among diets. To calculate endogenous N losses and N equilibrium, N excretion was plotted against N intake (“N balance plot;” Robbins 1993, Murphy 1993). Nitrogen excretion included urinary and fecal components, because they are mixed together in the cloaca of birds before excretion and cannot be adequately separated (Robbins 1993). From the N balance plot, endogenous N losses and N equilibrium were determined (Robbins 1993, Murphy 1993); minimum endogenous N losses (i.e. theoretical N excretion on a protein-free diet) are indicated by the y-intercept, and N equilibrium occurs where N intake equals N excretion. To compare N balance plots among individuals, ANCOVA were used. Once N equilibrium was determined, CP requirements for maintenance of body mass were calculated for each bird by regressing percentage CP in the diet against N intake; the point at which percentage CP = N intake at N equilibrium provided estimated minimum protein requirement for maintenance (Brice and Grau 1991, Murphy 1993, Robbins 1993). All statistical analyses were conducted with SPSS v.7.5 software (SPSS Inc., Chicago, Illinois), with alpha set at 0.05. Results and discussion Dry mass intake remained constant among birds (F = 3.20, df = 2 and 6, P = 0.11) and among diets (F = 1.77, df = 2 and 6, P = 0.25; Fig. 1). The birds did not compensate for low dietary protein content by increasing consumption, as apparently occurs in some frugivorous birds and bats (Thomas 1984, Izhaki and Safriel 1989). Body masses remained constant throughout all feeding trials (F = 0.49, df = 2 and 6, P = 0.64; Fig. 2), indicating no net catabolism or anabolism occurred. All birds exhibited similar N balance, as indicated by similar slopes (F = 0.10, df = 2 and 3, P = 0.91) and y-intercepts (F = 0.87, df = 2 and 5, P = 0.47; Fig. 3). Endogenous N losses were 0.05 gN kg−0.75 day−1 and N equilibrium occurred at 0.32 gN kg−0.75 day−1. Based on regression analysis and N equilibrium, a diet containing 3.2% dm CP (using a 4.05 nitrogen-to-protein conversion factor) would meet the minimal requirements for maintenance in Pesquet's Parrot. Fig. 1. Open in new tabDownload slide Mean mass-specific, dry mass intake of Pesquet's Parrots fed diets varying in protein content. Dietary protein calculated as %N (analyzed) × 4.05 (after Izhaki 1993). Error bars represent standard deviations. Matching letters indicate similar means (p > 0.05) Fig. 1. Open in new tabDownload slide Mean mass-specific, dry mass intake of Pesquet's Parrots fed diets varying in protein content. Dietary protein calculated as %N (analyzed) × 4.05 (after Izhaki 1993). Error bars represent standard deviations. Matching letters indicate similar means (p > 0.05) Fig. 2. Open in new tabDownload slide Mean changes in body masses of Pesquet's Parrots among experimental feeding trials. Dietary protein calculated as %N (analyzed) × 4.05 (after Izhaki 1993). Error bars represent standard deviations. Matching letters indicate similar means (P > 0.05) Fig. 2. Open in new tabDownload slide Mean changes in body masses of Pesquet's Parrots among experimental feeding trials. Dietary protein calculated as %N (analyzed) × 4.05 (after Izhaki 1993). Error bars represent standard deviations. Matching letters indicate similar means (P > 0.05) Fig. 3. Open in new tabDownload slide Nitrogen balance among Pesquet's Parrots, represented by the solid line, where Y = 0.86X + 0.05 (R2 = 0.96; n = 9). Data for different birds are indicated by different symbols. Values below the dashed line (Y = X) indicate net N anabolism, whereas values above this line indicate net N catabolism Fig. 3. Open in new tabDownload slide Nitrogen balance among Pesquet's Parrots, represented by the solid line, where Y = 0.86X + 0.05 (R2 = 0.96; n = 9). Data for different birds are indicated by different symbols. Values below the dashed line (Y = X) indicate net N anabolism, whereas values above this line indicate net N catabolism Estimating protein requirements for maintenance in birds is complicated by several factors, including variability in nutrient digestion and absorption (Karasov and Diamond 1983, Karasov et al. 1987, Levey and Karasov 1989), changes in visceral morphology (Drobney 1984, Walsberg and Thompson 1990, Klasing 1998), and ability of birds to adjust to insufficient or excessive dietary protein (Bairlein 1987, Murphy 1993). The presence of nonprotein N and interference by secondary metabolites are often ignored, as are unexplained N losses (Hegsted 1976, Young 1986, Izhaki and Safriel 1989, Mack 1990, Sedinger 1990, Izhaki 1993). Unmeasured N losses, for example from sloughed skin and feathers (King and Murphy 1990) or from drying fecal samples in an oven (Manoukas et al. 1964, Dawson and Herd 1983), result in an underestimate of minimum N requirements, because calculated N equilibrium would actually represent N deficit. Such errors may explain discrepancies observed between the calculated amount of dietary N needed for N equilibrium and observed amount needed for long term maintenance of body mass and positive N balance in several bird species (Hegsted 1976, Brice and Grau 1991, Murphy 1993). For example, Brice and Grau (1991) estimated that only 0.4% CP was necessary for positive N balance in Costa's Hummingbird, but observed that 1.5% CP was necessary to maintain body mass. Likewise, Murphy (1993) determined that White-crowned Sparrows required 8.7% CP for positive N balance, 5.3% CP for N equilibrium, and 7.3% CP for maintenance of body mass. Because of those inconsistencies, as well as various conversion factors used to calculate CP from measured N levels, it is more meaningful to compare endogenous N losses and N equilibrium among species. Endogenous N losses and N equilibrium in Pesquet's Parrots are extremely low compared to granivorous and omnivorous birds, but are similar to nectarivorous and other frugivorous birds (Table 3). Frugivorous and nectarivorous birds (n = 5 spp. pooled) have lower endogenous N losses (t = 5.9, p = 0.0002) and lower N equilibrium (t = 3.8, p = 0.005) than granivorous and omnivorous birds (n = 6 spp. pooled). In terms of endogenous N losses and N equilibrium, Pesquet's Parrot is most similar to another highly frugivorous bird, the Cedar Waxwing (Witmer 1998). Table 3. Comparison of crude protein (CP) requirements, nitrogen (N) losses, and N equilibrium of birds reported in the literature. Nitrogen losses represent endogenous N losses (urinary and fecal N). Data arranged in decreasing order of crude protein requirements. Dashes indicate no data available Open in new tab Table 3. Comparison of crude protein (CP) requirements, nitrogen (N) losses, and N equilibrium of birds reported in the literature. Nitrogen losses represent endogenous N losses (urinary and fecal N). Data arranged in decreasing order of crude protein requirements. Dashes indicate no data available Open in new tab Because gut volume is thought to limit rates of nutrient assimilation from bulky, nutritionally dilute fruit (Worthington 1989, Levey and Grajal 1991, Levey and Duke 1992, Klasing 1998, but see Witmer 1999), a larger gut volume would allow higher net rates of nutrient absorption in frugivores. Indeed, in some highly specialized frugivores, intestines are so completely packed with food that ingestion cannot occur until defecation makes more space available (Levey and Duke 1992, Klasing 1998). In frugivorous Cedar Waxwings and Phainopeplas (Phainopepla nitens), a relatively wide intestinal diameter results in high feed intake, which is associated with high rates of nutrient absorption (Walsberg 1975, Witmer 1998, Witmer and Van Soest 1998). Pesquet's Parrots also have wide intestines (Guntert 1981) and high feed intake (one fourth of their total body mass per day [wm]; this study). Furthermore, rapid nutrient absorption likely occurs in those parrots because their short intestines have extremely long microvilli throughout the entire intestinal tract and cloaca (Guntert 1981). Those modifications of the digestive tract are consistent with very low protein requirements in Pesquet's Parrots. Besides modifications of the digestive tract, some frugivores may obtain additional dietary protein from insects or seeds in fruits they ingest. Because Pesquet's Parrots feed exclusively on figs, their protein intake might be supplemented by fig wasps and seeds. However, we doubt that fig wasps contribute significantly to dietary protein levels. Even if those birds completely digest fig wasps, amount of additional protein contributed by wasps would be <3% of their total protein requirement (based on data from Herbst 1986). Obtaining protein from fig seeds is also unlikely because Pesquet's Parrot seems incapable of digesting seeds, due to a poorly developed, weak, and narrow gizzard (Guntert 1981). When small seeds are offered in their diet, the seeds are avoided, discarded, or swallowed intact (Homberger 1980, this study). During this study, small grape seeds passed undamaged through those parrots' digestive tracts. If small fig seeds also pass intact, Pesquet's Parrots could be seed dispersers of the figs on which they specialize. Because seeds and insects likely provide little protein in the diet of this unusual parrot, low protein requirements (i.e. reduced N equilibrium and endogenous N losses) appear to play an important physiological role in the ability of Pesquet's Parrot to subsist on a fruit diet. Acknowledgments This study was funded by the Wildlife Conservation Society. Laboratory analytical training was provided by M. Fitzpatrick. We thank the staff at the Wildlife Conservation Society's Wildlife Survival Center on St. Catherines Island for assistance in diet preparation, cage construction, and handling of Pesquet's Parrots. This manuscript was improved by the valuable suggestions of L. Gannes and two anonymous reviewers. Literature Cited Association of Official Analytical Chemists. 1984 . Official Methods of Analysis of the Association of Official Analytical Chemists. 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TI - Protein Requirements of a Specialized Frugivore, Pesquet's Parrot (Psittrichas fulgidus)
JF - Auk: Ornithological Advances
DO - 10.1093/auk/118.4.1080
DA - 2001-10-01
UR - https://www.deepdyve.com/lp/oxford-university-press/protein-requirements-of-a-specialized-frugivore-pesquet-s-parrot-RsCRzAUrYA
SP - 1080
VL - 118
IS - 4
DP - DeepDyve
ER -