Protein requirements of a specialized frugivore, Pesquet's Parrot (Psittrichas fulgidus)

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^sup -0.75^ day ^sup -1^ and nitrogen equilibrium occurred at 0.32 gN kg ^sup 0.75^ day^sup -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 m^sup 3^) 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 deg 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.