Print version ISSN 0716-078X
Rev. chil. hist. nat. vol.73 n.3 Santiago Sept. 2000
Energetics and nutritional ecology of small herbivorous birds
Ecología energética y nutricional en aves herbívoras pequeñas
Herbivory is a rare strategy in birds. Only 3% of extant birds exploit plant material as an energy source. Both plant chemical composition and bird constraints associated to flight and digestion may explain why herbivory is so scarce in small endotherms such as birds. Here we tackle the question of how herbivorous birds meet energy/nutrient requirements when feeding on extremely poor diets. We focus on Phytotoma rara (Phytotomidae), possibly the smallest herbivorous bird. From our mini-review we conclude that several features such as the fast passage rates, an effective physical breakdown of cell walls, and constant and high activities of digestive enzymes make available the highly nutritious cell contents to the small herbivore, without the energy costs of anatomical structures for bacterial fermentation or slow passage rates. These are possible crucial adaptations in the evolution of herbivory in small birds.
Key words: herbivory, bird, body mass, digestion, foraging, energetics.
La herbivoría en aves es una estrategia poco común. Solo el 3% de las aves actuales consumen plantas como fuente de energía. Tanto la composición química de las plantas como las restricciones asociadas al vuelo y digestión en aves pueden explicar el reducido número de pequeños endotermos, como las aves, que son herbívoros. Nuestro objetivo es explicar como las aves herbívoras satisfacen sus requerimientos nutricionales y energéticos cuando consumen dietas extremadamente pobres. Para lo cual nos centramos en Phytotoma rara (Phytotomidae), posiblemente el ave herbívora más pequeña. Phytotoma rara presenta numerosas características, como el rápido tiempo de transito, un efectivo rompimiento de la pared celular, y la alta y constante actividad de las enzimas digestivas, que le permiten disponer de nutrientes y energía celulares, sin los costos energéticos asociados al desarrollo de estructuras anatómicas de fermentación bacteriana o lentos tiempos de transito. Estos son posiblemente adaptaciones cruciales en la evolución de la herbivoría en aves pequeñas.
Palabras clave: herbivoría, aves, tamaño corporal, forrajeo, digestión, energética.
Herbivory is a rare strategy in birds. Only 3% of extant birds (c.a., 300 of 9600 species) exploit plants material as an energy source (Morton 1978, Grajal 1991). Because cell walls of plants (i.e. dietary fiber) and secondary compounds are a barrier to the extraction of soluble nutrients from the cell and are difficult to digest (Hume 1989), thus affecting overall digestibility and rates of energy metabolism and allocation (Van Soest 1982), fiber and secondary metabolites should influence food selection and energy nutritional budget of herbivores.
Both, plant chemical composition and bird constraints associated to flight (Norberg 1996) and digestion (Sibly 1981) may explain why herbivory is so scarce in small endotherms such as birds (Foley & Cork 1992). Most herbivorous birds are larger than 1 kg (Dunning 1993). Only a few species with body lower than 100 g are totally or partially herbivores. Small endotherms have similar relative digestive-tract size, but higher relative metabolic rate and faster gut turnover time than large ones (Bozinovic 1995). Batzli (1985) hypothesized that those physiological and allometric digestive-metabolic constraints force small vertebrates to select food with low fiber contents. However, Foley & Cork (1992) analyzed the extent to which small herbivorous endotherms can bend these allometric constraints. They suggested that some species of small endotherms compensate for low quality diets (high fibrous diets) by a combination of digestive mechanisms that include: rapid turnover time of fibrous food, changes in gut capacity and increased nutrient uptake by the small intestine (see Sibly 1981, Gross et al. 1985, Karasov 1986, Green & Millar 1987, Bozinovic et al. 1988, Karasov & Diamond 1988, Hammond & Wunder 1991, Derting & Bogue 1993).
Ecological factors, such as climate and food habits appear to be the most important features in determining energy expenditure at both intra and interspecific levels (McNab 1986, 1988a, 1988b). Food quality, and digestive physiology affect the rate of energy metabolism (Batzli 1985), setting a limit to the energy budget of organism (Weiner 1992). Moreover, in theory small endotherms should show decreased energy expenditures and increased gut turnover time in comparison with large ones. This is because metabolic rate scales with body mass to the 0.75 power (Kleiber 1961, Peters 1983, Calder 1984), whereas gut capacity scales isometrically with body mass (Parra 1978, Batzli 1985, Hume 1989). Consequently the turnover of gut contents should scale as the ratio of gut contents and metabolic rate, namely to body mass to the 0.25 power. This relationship predicts that smaller vertebrates have higher metabolic rate, preferred high-energy food and retain food in the digestive tract for a shorter time than larger ones (Demment & Van Soest 1985, Foley & Cork 1992). Here we tackle the question of how herbivorous birds meet energy/nutrient requirements when feeding on extremely poor diets. We focus on Phytotoma rara (Phytotomidae), possibly the smallest herbivorous bird.
FORAGING, DIGESTION AND ENERGETICS
As mentioned, few species of birds consume exclusively plant material. Most species of herbivores also fed on insects, fruits or seeds (Karasov 1990). Herbivores are selective foragers, several studies confirm that they select plant material according to age and chemical plant composition (Short et al. 1974). Birds are especially selective due to the high-energy requirement of flight and the need to reduce the weight of digestive organs and their contents. These birds consume preferentially parts of plants that are relatively high in protein and low in fiber, such as rhizomes, buds, flowers, very young leaves, and young grasses. Consequently, mature leaves, stems and grass are rejected. For example, Gill (1995) documented that several Anseriformes assimilated nearly 60 to 70% of energy of young plants, but only 30-40% of mature foliage. Canvasbacks (Aythya valisineria) exhibited a very high energy assimilation (79%) on tubers, a plant with a 16% of fiber (Takekawa 1987). The cursorial Spruce Grouse (Falcipennis canadensis) which fed on high fibrous old spruce leaves, assimilated only 30% of the food energy (Pendargast & Boag 1974). Also, secondary compounds as alkaloids, glycosides, toxic amino acids, and mycotoxins, affect food selection of herbivorous birds. These compounds limit intake and digestibility (Akin 1989, Jakubas et al.1995). Guglielmo et al. (1996) experimentally observed a 24% reduction in energy assimilation in Ruffed Grouse (Bonasa umbellus) when consuming plant material with naturally high secondary metabolites as coniferyl benzoate. Detoxification cost probably determined a preference for low secondary metabolites plants.
Several properties of gastrointestinal tract (GI) anatomy and physiology affect the ability of herbivorous birds to extract nutrients from the food. These are: a) structural complexity and surface area of the GI tract, b) motility and their effect in transit time of digesta, c) capacity of GI tract for chemical breaking down and/or fermenting macromolecules, and d) capacity of the GI to absorb the resultant product (Karasov & Hume 1997). For example, De Golier et al. (1999) studied the morphological patterns of the caeca in 21 orders of birds. These authors observed that a well-developed caeca occur principally in herbivorous or omnivorous birds as Ratites, Anseriformes, Galliformes, Gruiformes, Cuculiformes, Strigiformes, Caprimulgiformes and Trogoniformes. Functionally, the caeca is associated with an increase in the digestive efficiency of plant material through selective filling with highly fermentable smaller particles and liquid, while most of the largely undigested cell wall is excreted (Duke 1989, McLelland 1979, Karasov 1990). Bacterial fermentation in the caeca, increases nitrogen recycling, nutrient absorption, the uses of urinary nitrogen for microbial growth and energy for microbial volatile fatty acid production (VFA) (Gasaway 1976a, Gasaway 1976b, Gasaway et at. 1976, Skadhauge 1976, Björnhag 1989, Clench & Mathias 1995). In fact, the largest birds species, as Ostriches (Struthio camelus), and Rheas (Rhea americana, Pterocnemia pennata) (38-80 kg, Karasov 1990) are herbivorous-omnivorous, and are principally cursorial with large digestive organs and hindgut fermentative chambers (Fig. 1a) (Noble 1991).
|Fig. 1. Gastrointestinal tract of a) Darwin' s Rhea, b) Hoatzin. c) Goose', and d) Rufous-tailed Plantcutters. Letters means e = esophagus, p = proventriculus. c = crop. 9 = gizzard. si = small intestine. ca = caeca. |
Tracto digestivo de a) Ñandú. b) Hoatzin c) Ganso. y d) Rara. Letras significan e =esófago. p = proventrículo,c = estómago muscular, g = esto mago glandular, si = intestino delgado, ca = ciegos.
Common in mammals but very unusual in birds, is foregut fermentation, where the fiber is fermented in pregastric chambers (Fig 1b). In mammals, this digestive method allows detoxification of plant secondary compounds (Barry & Blaney 1987), and microbial synthesis of essential amino acids and vitamins (Van Soest 1982). The only herbivorous bird with demonstrated foregut fermentation is the Hoatzin (Opisthocomus hoatzin), a 700 g bird (Dominguez-Bello et al. 1993, Grajal et al. 1989, Grajal 1991, 1995a, 1995b,). The gastrointestinal design of the Hoatzin corresponds to an alloenzymatic-autoenzymatic system (see Penry & Jumards 1986, 1987), with a large muscular crop divided in two chambers and a posterior esophagus (Fig. 1b) where fermentation occurs. A long small intestine allows autoenzymatic digestion in this species (Grajal 1995a). Caeca are short but low pH levels and the presence of VFAs indicate the occurrence of fermentation. Other birds with possible foregut fermentation are the Kakapo (Strigops habroptilus) and the New Zealand pigeon (Hemiphaga novaeseelandiae); their diets are omnivorous including plant material and some fruits and animals (Best & Powlesland 1985, Cloud et al. 1986). All these birds exhibit a poor flight ability and lower levels of energy expenditures (Grajal 1991).
The presence of fermentation chambers is not the unique design for autoenzymatic process, because larger birds can retain the digesta for a longer time than smaller birds (Karasov 1990). In fact, the Emu (Droamius novaehollandiae, a 30 k bird), apparently digests an important amount of fiber (35% approx.) without special mechanisms, however the major fermentation site is at the distal section of the small intestine (Herd & Dawson 1984, Noble 1991). In parallel, a low energy and protein requirement (Dawson & Herd 1983) and a primitive coprophagy were recorded in this species (Del Hoyo et al. 1992).
On the other hand, the feeding strategy of the aquatic plant eaters such as ducks and geese (Anatidae), coots and gallinules (Rallidae), and grouses (Tetraonidae) with medium size of body mass (mean ± SE) = 1,300 ± 400 g, ranged from 300 to 9,000 g (De Golier et al. 1999, Del Hoyo et al. 1994, Dunning 1993), is characterized by a fast passage rate of digesta and a high food intake (Björnhag & Sperber 1977, Burton et al. 1978, Buchbaum et al. 1986, Dawson et al. 1989). Their gastrointestinal tract is represented by enzymatic and muscular stomachs and a long small intestine with a caeca partially developed (Fig. 1c). This design allows acid degradation of hemicellulose at the stomach and a partial and selective microbial fermentation at the intestine and caeca (Marriot & Forbes 1970, Moss 1983, Buchsbaum et al. 1986, Kehoe et al. 1988) The fiber digestion and volatile acids production represents approximately one-third of the assimilated energy in the Australian wood duck (Chenonetta jubata, Dawson et al. 1989), this proportion is equivalent to foregut fermentation in the Hoatzin (Grajal et al. 1989). The difference with the Hoatzin is that this feeding behavior and digestive design do not constrain the birds flying capacity.
In small birds (body mass < 100 g) a folivory frugivory strategy (sensu Gragal 1991) was observed in few passerines species such as Saltatoridae (Bosque et al.1999), Colidae (Bartholomew & Trost 1970, Prinzinger et al. 1981), and Phytotomidae (Ziswiler & Farner 1972, López-Calleja & Bozinovic 1999). Apparently, birds in this group do not present morphological specialization in their digestive system, representing the typical frugivorous-like design. Nevertheless, for example Phytotoma rara (Phytotomidae), the most austral distributed species (Fjeldsä & Krabbe 1990), fed exclusively on herbage during autumn and winter, and incorporated fruits only during spring and summer (López-Calleja & Bozinovic 1999). The digestive morphology of P. rara is frugivorous-like, with a small stomach and short and gross intestine (Fig. 1d).
Herbivorous birds exhibit lower basal metabolic rate (BMR) than expected based on body mass (Kendeigh et al. 1977, McNab 1988a, Daan et al.1990, Grajal 1991, Hinds et al. 1993). McNab (1986, 1988a, b) proposed that the scaling of BMR to body mass is sensitive to ecological factors in vertebrates, such as dietary habits. Species that exploit food with low energy and high fiber content, and/or high cost of digestion as herbivores, appear to have low mass-independent rates of energy expenditure. In fact, plant material imposes a restriction in energy flux, the fiber proportion causes the lowest coefficient of energy assimilated of all avian food types (Karasov 1990), the presence of plant secondary metabolites and their toxins reduce intake rate in herbivorous birds (Jakubas et al. 1993), and moreover, a fraction of the energy assimilated is used in the detoxification process (Guglielmo et al. 1996). Figure 2 shows 25 records of BMR of herbivorous birds, expressed as proportion of expected value for their body mass. Herbivorous species exhibit lower BMR (mean ± SD = 84.2 ±14.2 %), but with a high variability (Fig. 2). Strict herbivores, such as the folivorous Sage grouse (Centrocercus urophasianus) and the Hoatzin (O. hoatzin) exhibit much lower metabolic rate than expected (Vehrencamp et al. 1989, Grajal 1991). Parallely, partial herbivores such as Anseriformes and Ratites, do not present a clear pattern (Fig. 2). Flight capacity (muscle mass), and distribution (cold vs. tropical habitat) may explain some of the data scatter. Researching flight capacity, McNab (1988a) postulated that the lower values of BMR of mammalian herbivores is a consequence of reduced muscle mass together with sedentary habits for mammals herbivores. This author predicted that in birds, requirements associated with flight would prevent lower values of BMR. We compared observed to expected BMR considering flight capacity and did not observe any tendency (Flight:c2 = 0.78, P >0.05, n = 17; and Non-flight: c2 = 0.84, P >0.05, n = 8). In this sense, Rezende et al. (pers. comm.) documented a similar to expected BMR for the herbivorous passerine P. rara (2.47 ± 0.06 mlO2/gh), and Bosque et al. (1999) observed a low metabolic rate for two small passerine folivorous (Saltator coerulescens, 1.49 ± 0.04 mlO2/gh and Saltator orenocensis, 1.72 ± 0.06 mlO2/gh). Weathers (1979) proposed that species range of distribution and specifically, climate affect BMR. In the tropic species present lower BMR than in temperate areas. Recently, Rezende et al. (pers. comm.) evaluated the climatic effect over BMR in herbivorous birds. They observed that birds from temperate areas tend to have higher BMR while tropical birds lower values. Then, distributional limits appears as an important variable to explain herbivores BMR variability, where few small herbivorous bird (> 100 g) are present in cold temperate areas.
| Fig. 2. Re1ationship between BMR observed/BMR expected (%) and body mass for 25 herbivores birds from the 1iterature. Birds are taxonomica11y grouped, and co1ors mean good flying capacity (grey symbo1s) and weak flying capacity (white symbo1s). For estimation of expected BMR, Ashoff & Poh1 ( 1970) equations for passerine and non-passerine were used. |
Relación entre la razón de BMR observado/ BMR esperado (%) y masa corporal para 25 aves herbívoras obtenidos de la literatura. Los registros se agruparon taxonómicamente, donde los colores representan aves voladoras (grises) y malas voladoras (blancos). Para la estimación del BMR esperado se usaron las ecuaciones de Ashoff & Pohl ( 1970) para paserinos y no-paserinos.
Now, we tackle the question ¿How herbivorous birds can meet their requirements when feeding poor diets?
Phytotoma rara: a small avian herbivore
The three members of the South American Phytotomidae are one of the smallest passerine herbivores (Ziswiler & Farner 1972). Of these three, the Rufous-tailed Plantcutter (P. rara) has the southern-most distribution, from Vallenar (28°34S, 70°45W) to Chiloé (42°25S, 73°46W), Chile (Goodall et al. 1946). Phytotoma rara inhabits forests and scrub-lands, as well as crop fields and orchards (Araya & Millie 1986). In the field an exclusively herbivorous diet was documented during autumn and winter, consuming preferentially young monocotyledon leaves than dicotyledons. During spring and summer, their diet included fruits and a low proportion of insects. In a preference trial, P. rara significantly preferred lettuce compared to soy shoots or oat leaves, did not exhibit a clear preference between leaves and fruits, and rejected insects (López-Calleja & Bozinovic 1999). Both, in natural and experimental conditions, P. rara preferred monocotyledons over dicotyledons and young over mature plants, probably because monocotyledons present few tannins in comparison with dicotyledons (Bernays et al.1989), and young plants contain more protein and low fiber proportion (Mauseth 1995). Surprisingly, the Rufous-tailed Plantcutter presents one of the highest mass-independent values of BMR observed among avian herbivore (see Fig. 2). Nevertheless, the daily energy expenditure (DEE) of P. rara is lower (1.5 x BMR, López-Calleja 1999) than the average observed for birds (4 to 5 x BMR, Drent & Daan 1980, Daan et al. 1990, Bryant & Tatner 1991). This value is consistent with their sedentary foraging strategy observed in the field (López-Calleja & Bozinovic 1999). Probably, the digestive adaptations (morphological, physiological and biochemical; see López-Calleja & Bozinovic 1999, Meynard et al. 1999) of P. rara allows to increase the energy/nutrient extraction efficiency of poor food, being enough to maintain their values of metabolic expenditure.
On the other hand, when comparing feeding rates (FR, g day-1) with the expected values based on the allometric equation for passerines reported by Nagy (1987), where FR = 0.398 bm0.850 (bm in g), we observed that FR with lettuce diet was 143% more than that expected, and with a mixed diet (lettuce plus fruits) FR was in the expected value (Lopez-Calleja & Bozinovic 1999). Paralelly, mean retention time (MRT, Warner 1981) is nearly 50% lower than the expected value based on body mass (Fig. 3a). The short retention time and high FR are typical in herbivorous birds as well as ducks and geese (Karasov 1990, see above), but ducks and geese present partial fermentation with VFA production. Nevertheless, P. rara has a higher MEC in comparison to birds that fed on herbage or grasses (0.26 to 0.40, n = 16, Karasov 1990), and similar with birds that fed bulbs and rhizomes (0.38 to 0.74, n = 4, Karasov 1990) (Fig. 3b). How P. rara present a similar MEC as birds that fed on high energetic plant material without any fiber utilization as fermentation cameras?
| Fig. 3. a) Mean Retention Time records for birds and records for P. rara consuming mixed (lettuce + fruit) and lettuce alone diets. b) Frequency range of Metabolizable Energy Coefficient (MEC*) values observed in avian herbivorous feeding studies and the new record for P. rara. |
a) Tiempo medio de retención (MRT) para aves herbívoras. más registros en P. rara consumiendo dieta mixta de lechuga y fruta conio de lechuga sola. b) Rango de valores de coeficiente de energía metabolizable (MEC*) observados en diferentes estudios de alimentación en aves herbívoras. más el nuevo registro para P. rara.
The Rufous-tailed Plantcutter exhibits other digestive characteristics to maintain their high MEC, such as:1) A teeth-like structures of horny palate and the lower beak (Ziswiler & Farner 1972), a special morphology of the jaw articulation, a horny spines on the dorsal surface of the tongue, clamp like tongue, and a rough layer covering the narrow lumen at the muscular stomachs (Girod 1998). These structures permit the bird to macerate cell wall prior to digestion. Other herbivorous birds such as the Australian passerine Tooth-billed Bowerbird (Sceropoetes dentirostris) and several Anatidae present similar beak modification (Klasing 1998). 2) A muscular stomach and a highly folded intestinal mucosa with long microvilly. The esophagus and glandular stomach are long and flexible and the muscular stomach (crop) is bigger than expected (Fig. 1d, Table 1). Probably the size of esophagus and crop are associated with a bulky diet during winter, and are used as food reservoir as happens in other bird species (Klasing 1998). The small intestine is shorter (length) and thicker (diameter) than expected for body mass (Ricklefs 1996). The intestinal mucosa is highly folded, with long microvilly through all the small intestine (Martínez del Rio, com. pers.). We suspect that this intestinal design allows a rapid transit time of the fibrous meal fraction, and the highly folded mucosa facilitate the retention and absorption of the small particles previously macerated. The liver is bigger than the expected for its body mass (Table 1). Probably this is associated with detoxification of plants secondary compounds (Schmidt-Nielsen 1990, Brody 1994). Finally, 3) In many species of birds the activity of digestive enzymes decreases distally along the small intestine (Martínez del Río 1990, Martínez del Río et al. 1995). According to the optimization design hypothesis, a decrease in the concentration of substrates along the gut axis should be matched by a decrease activity of enzymes which will reduces the expensive cost of maintenance of non-utilized membrane-bound protein (Hume 1998). Interestingly P. rara present constant activities of sucrase, maltase and aminopeptidase-N along the intestine, and only in the final section do enzyme activities change significantly (Meynard et al. 1999). Moreover, sucrase and maltase present enzymes activities higher than those previously reported in other passerines of similar body size (Fig. 4, Martínez del Río et al. 1995, Afik & Karasov 1995, Sabat et al. 1998, Caviedes-Vidal et al. in press, Sabat 2000). Probably both, a high and constant enzyme activity, allow P. rara to exploit a diluted food resource and to maintain a higher overall extraction efficiency when feeding on plants.
| Fig. 4. Total enzymes activities of sucrase, maltase and aminopeptidase-N from s ix passerines birds previously reported compared with P. rara values. |
Actividad enzimática total de sacarosa, maltosa y aminopeptidasa-N en seis aves paserinas previamente reportadas comparadas con datos de P. rara.
In conclusion, P. rara exhibits several morphological and physiological digestive mechanisms that allow it to cope with an herbivorous diet. Theoretically, the observed short retention time should result in lower efficiency of energy/matter extraction due to reduced digesta exposure to digestive processing (Karasov 1996), but the behavioral, morphological and physiological adaptation associated with food manipulation, intake and processing plays an important role in the observed digestibility. Then, the fast passage rates and effective physical breakdown of cell walls permits the highly nutritious cell contents to be available to the small herbivore, without the high energy costs of anatomical structures for bacterial fermentation or slow passage rates. These are possibly crucial adaptations in the evolution of the herbivorous diet in the small plantcutters.
CONCLUSIONS AND FUTURE DIRECTIONS
A feeding behavior and, consequently, a pattern of energy use and expenditure, could be greatly influenced by anatomical, physiological and biochemical constraints of the digestive system. Nevertheless, foraging processes and digestibility not only depend on digestive strategies and design, but also on the food type itself. Theoretically, the combination of organismal events, including structural features, the biochemical and physiological components of energy intake, and the thermodynamic efficiency of energy/matter transformations are under natural selection. An adaptive landscape that includes mechanisms and processes of energy, matter, nutrients and water intake and digestion under specific biotic and abiotic environmental conditions, appear as the results of natural selection.
We reviewed here that contrary to previous ideas, some species of birds often include fibrous plant tissues as a major dietary item doubtless because they are able to obtain a considerable fraction of energy from fiber to satisfy their energy requirements for maintenance. In short, because of the physiological and behavioral compensatory mechanisms for exploitation of low diet quality exhibited by the small herbivorous birds, extremely high fiber diets may be enough to satisfy their energy cost. Obviously additional studies are needed to elucidate the connections between energetics, nutrition and life history. This task will only come with a shift in attitude concerning the place of testing ecophysiological hypothesis in avian biology. Individuals engaged in ornithology should open, or continue, more conceptual dialogues with colleagues who are engaged in other facets, not necessarily taxonomically related, of functional ecology including behavioral, biophysical and physiological ecology.
This paper resulted from our participation of the symposium on avian physiology organized by Francisco Bozinovic and Carlos Martínez del Rio at the VI-Neotropical Ornithological Congress (Mexico). Previous versions of this paper benefited from the critical comments of Bill Karasov and P. Sabat. M. V. López-Calleja grateful the organization committees assistance fellowship. This paper was partially supported by Fondecyt 2970002 of M. V. López-Calleja, and 1980959 of F. Bozinovic.
(Managed by F. Bozinovic)
AFIK D & WH KARASOV (1995) The tradeoffs between digestion rate and efficiency in the Yellow-rumpled Warblers, and its ecological implications. Ecology 76: 2247-2257. [ Links ]
AKIN de (1989) Histological and physical factors affecting digestivility of forages. Agronomy Journal 81: 17-25. [ Links ]
ARAYA B & G MILLIE (1986) Guía de campo de las aves de Chile. Editorial Universitaria, Santiago. 300 pp. [ Links ]
ASCHOFF J & H POHL (1970) Rhythmic variation in energy metabolism. Federation Proceeding 29: 1541-1552. [ Links ]
BARTHOLOMEW GA & CH TROST (1970) Temperature regulation in the Speckled Mousebird Colius striatus. Condor 72: 141-146. [ Links ]
BARRY TN & BLANEY BJ (1987) Secondary compounds of forages. In: Hacker JB & Ternouth JH (eds) The Nutrition of Herbivores: 137-171. Academic Press, New York. [ Links ]
BERNAYS EA, G COOPER DRIVER & M BILGENER (1989) Herbivores and plant tannins. Advances in Ecological Research: 19: 263-302. [ Links ]
BEST H & R Powlesland (1985) Kakapo. John McIndoe Ltda & NZ Wildlife Service, Dunedin, New Zealand. 33pp. [ Links ]
BJÖRNHAG G (1989) Transport of water and food particles through the avian ceca and colon. Journal of Experimental Zoology, supplement 3:32-37. [ Links ]
BJÖRNHAG G & IS SPERBER (1977) Transport of various food components though the digestive tract of turkeys, geese and guineafowl. Sweden Journal of Agricultural Research 7: 57-66. [ Links ]
BOSQUE C, MA PACHECO & RB SIEGEL (1999) Maintenance energy costs of two partially folivorous tropical passerines. Auk 116: 246-252. [ Links ]
BOZINOVIC F (1995) Nutritional energetics and digestive responses of an herbivorous rodent (Octodon degus) to different levels of dietary fiber. Journal of Mammalogy 76:627-637. [ Links ]
BOZINOVIC F, C VELOSO & M ROSENMANN (1988) Cambios del tracto digestivo de Abrothrix andinus (Cricetidae): efecto de la calidad de dieta y requerimientos de energía. Revista Chilena de Historia Natural 61: 245-251. [ Links ]
BUCHSBAUM R, J WILSON & I VALIELA (1986) Digestibility of plant constituents by Canada Geese and Atlantic Branta. Ecology 67: 386-393. [ Links ]
BURTON BA, RJ Hudson & DD BRAGG (1978) Efficience of utilization of bulrush rhizomes by Lesser Snow Geese. Journal of Wildlife Management 43: 728-735. [ Links ]
BRODY T (1994) Nutritional biochemestry. Academic Press, Boston. 658 pp. [ Links ]
BRYANT DM & P TATNER (1991) Intraspecies variation in avian energy expenditure: correlates and constrains. Ibis 133: 236-245. [ Links ]
CALDER WA (1984) Size, function, and life history. Harvard University Press, Cambridge, MA. 431 pp. [ Links ]
CAVIEDES-VIDAL E, C AFIK, C MARTINEZ DEL RIO & WH KARASOV (in press). Dietary modulation of intestinal enzymes of the house sparrow (Passer domesticus): testing an adaptative hypothesis. Comparative Biochemistry and Physiology. [ Links ]
CLENCH M & JR MATHIAS (1995) The avian cecum: a review. Willson Bulletin 107: 93-121. [ Links ]
CLOUD MN, PD GAZE, JR HAY & BJ KARL (1986) Habitat use and spring movements of New Zealand Pigeons at lake Rotoroa, Nelson Lakes National Park. Notornis 33:37-44. [ Links ]
DAAN S, D MASMAN & A GROENEWOLD (1990) Avian basal metabolic rates: their association with body composition and energy expenditure in nature. American Journal of Physiology 259: R233-R340. [ Links ]
DAWSON TJ & RM HERD (1983) Digestion in Emu, Dromaius novaehollandiae: low energy and nitrogen requirements of this large ratite bird. Comparative Biochemestry and Physiology 75A: 41-45. [ Links ]
DAWSON TJ, AB JOHNS & AM BEAL (1989) Digestion in the Australian Wood Duck (Chenonetta jubata): a small avian herbivore showing selective digestion of the hemicellulose component of fiber. Physiological Zoology 62: 522-540. [ Links ]
DE GOLIER TF, SA MAHONEY & GE DUKE (1999) Relationships of avian cecal lengths to food habits, taxonomic position, and intestinal lengths. Condor 101: 622-634. [ Links ]
DEL HOYO J, A ELLIOT & J SARGATAT, eds (1994) Handbook of the Birds of the World: New world vultures to guineafowl. Lynx Editions, Barcelona. Vol. 2: 638 pp. [ Links ]
DEMMENT MW & PJ VAN SOEST (1985) A nutritional explanation for body-size patterns of rumiant and nonrumiant herbivores. American Naturalist 125: 641-672. [ Links ]
Derting TL & BA Bogue (1993) Responses of the gut to moderate energy demands in a small herbivore (Microtus pennsylvanicus). Journal of Mammalogy 74: 59-68. [ Links ]
DOMINGUEZ-BELLO MG, M LOVERA, P SUAREZ & F MICHELANGELI (1993) Microbial digestive symbionts of the crop of the hoatzin (Opisthocomus hoatzin): an avian foregut fermenter. Physiological Zoology 66: 374-383. [ Links ]
DRENT RH & S DAAN (1980) The prudent parent: energetic adjustment in avian breeding. Ardea 68:225-252. [ Links ]
DUKE GE (1989) Gastrointestinal motility and its regulation. Poultry Science 61:1245-1256. [ Links ]
DUNNING JB (1993) Handbook of avian body masses. CRC Press Inc., Boca Raton. 371 pp. [ Links ]
FJELDSÄ J & N KRABBE (1990) Birds of the high Andes. Zoological Museum, University of Copenhagen & Apollo Books, Svendborg. 876 pp. [ Links ]
FOLEY WJ & SJ CORK (1992) Use of fibrous diets by small herbivores: how far can the rules be "bent"? Trends in Ecology and Evolution 7: 159-162. [ Links ]
GASAWAY WC (1976a) Seasonal variation in diet, volatile fatty acid production and size of the cecum of Rock Ptarmigan. Comparative Biochemistry and Physiology 53A: 109-114. [ Links ]
GASAWAY WC (1976b) Volatile fatty acids and metabolizable energy derived from cecal fermentation in the Willow Ptarmigan. Comparative Biochemistry and Physiology 53A: 115-121. [ Links ]
GASAWAY WC, RG WHITE & DF HOLLEMAN (1976) Digestion of dry matter and absorption of water in the intestine and cecum of the Rock Ptarmigan. Condor 78: 77-84. [ Links ]
GILL FB (1995) Ornithology . 2nd edition, WH Freeman & CO, New York. 766 pp. [ Links ]
GIROD S (1998) Folivorie als extreme Ernährungsspezialisation beim Chilenischen Pflanzenmähder Phytotoma rara Mol. (Aves). Doctoral dissertation, Universität Zürich, Zürich. 87 pp. [ Links ]
GOODALL JD, AW JOHNSON & RA PHILIPPI 81946) Las aves de Chile, su conocimiento y sus costumbres. Vol. I, Platt Establecimientos gráficos, Buenos Aires. 435 pp. [ Links ]
GRAGAL A (1991) Digestive efficiency of the hoatzin (Opisthocomus hoatzin), a folivorous bird with foregut fermentation. PhD. dissertation, University of Florida, Gainesville, Florida, USA, 111 pp. [ Links ]
GRAJAL A (1995a) Structure and function of the digestive tract of the hoatzin (Opisthocomus hoatzin): a folivorous bird with foregut fermentation. Auk 112: 20-28. [ Links ]
GRAJAL A (1995b) Digestive efficiency of the Hoatzin, Opisthocomus hoatzin: a folivorous bird with foregut fermentation. Ibis 137: 383-388. [ Links ]
GRAJAL A, SD STRAHL, R PARRA, MG DOMINGUEZ & A NEHER (1989) Foregut fermentation in the hoatzin, a Neotropical avian folivore. Science 245: 1131-1134. [ Links ]
GREEN DA & JS MILLAR (1987) Changes in gut dimensions and capacity of Peromyscus maniculatus relative to diet quality and energy needs. Canadian Journal of Zoology 65: 2159-2162. [ Links ]
GROSS JE, Z WANG & BA WUNDER (1985) Effects of food quality and energy needs: changes in gut morphology and capacity of Microtus ochrogaster. Journal of Mammalogy 66: 661-667. [ Links ]
GUGLIEMO C, WH KARASOV & WJ JAKUBAS (1996) Nutritional costs of a plant secondary metabolite to a herbivore: the basis for avoidance of coniferyl benzoate in quaking aspen flower buds by ruffed grouse. Ecology 77 1103-1115. [ Links ]
HAMMOND KA & BA WUNDER (1991) The role of diet quality and energy need in the nutritional ecology of a small herbivore, Microtus ochrogaster. Physiological Zoology 64: 541-567. [ Links ]
HERD RM & TJ DAWSON (1984) Fiber digestion in the Emu, Dromaius novaehollandiae, a large bird with a simple gut and high rates of passage. Physiological Zoology 57: 70-84. [ Links ]
HINDS DS, RV BAUDINETTE, RE MACMILLEN & EA HALPERN (1993) Maximum metabolism and the aerobic factorial scope of endotherms. Journal of Experimental Biology 182: 41-56. [ Links ]
HUME I (1989) Optimal digestive strategies in mammalian herbivores. Physiological Zoology 62: 427-451. [ Links ]
HUME I (1998) Optimization in design of the digestive system. In: Weibel E, R Taylor & L Bolis (eds) Principles of animal design: 212-219, Cambridge University Press, Cambridge. [ Links ]
JAKUBAS WJ, GUGLIELMO, CG VISPO & WH KARASOV (1995) Sodium balance in Ruffed Grouse as influenced by sodium levels and plant secondary metabolites in quaking aspen. Canadian Journal of Zoology 73: 1106- 1114. [ Links ]
KARASOV WH (1986) Energetics, physiology and vertebrate ecology. Trends in Ecology and Evolution 1: 101-104. [ Links ]
KARASOV WH (1990) Digestion in birds: chemical and physiological determinants and ecological implications. Studies in Avian Biology 13: 391-415. [ Links ]
KARASOV WH (1996) Digestive plasticity in avian energetics and feeding ecology. In: Carey C (ed) Avian energetics and nutritional ecology: 61-84. Chapman & Hall, New York. [ Links ]
KARASOV WH & JM DIAMOND (1988) Interplay between physiology and ecology in digestion. BioScience 38: 602-611. [ Links ]
KARASOV WH & ID HUME (1997) The vertebrate gastrointestinal system. In: Dantzler WH (ed) Handbook of Physiology, Section 13: Comparative Physiology, Vol 1: 407-480, Oxford University Press, New York. [ Links ]
KENDEIGH SC, VR DOLNIK & VM GAVRILOV (1977) Avian energetics. In: Pinowski J & SC Kendeigh (eds) Granivorous birds in ecosystems: 127-204. Cambridge University Press, Cambridge. [ Links ]
KEHOE FP, CD ANKNEY & BRT ALISAUSKUS (1988) Effects of dietary fiber and diversity on digestive organs of captive Mallards (Anas platyrynchos). Canadian Journal of Zoology 66:1597-1602. [ Links ]
KLASING KC (1998) Comparative avian nutrition. University Press, Cambridge, UK. 350 pp. [ Links ]
KLEIBER M (1961) The fire of life: an introduction to animal energetics. Robert E. Krieger Publishing Company, Malabar, Florida. 453 pp. [ Links ]
LOPEZ-CALLEJA MV (1999) Forrajeo, energética y digestión en aves: ¿Qué factores limitan el presupuesto de energía? Tesis de Doctorado, Facultad de Ciencias, Universidad de Chile. 150 pp. [ Links ]
LOPEZ-CALLEJA MV & F BOZINOVIC (1999) Feeding behavior and assimilation efficiency of the Rufous-tailed Plantcutter: a small herbivore. Condor 101: 705-710. [ Links ]
MARTINEZ DEL RIO C (1990) Dietary, phylogenetic, and ecological correlates of intestinal sucrase and maltase activity in birds. Physiological Zoology 63: 987-1011. [ Links ]
MARTINEZ DEL RIO C, KE BRUGGER, JL RIOS, ME VERGARA & M WITMER (1995) An experimental and comparative study of dietary modulation of intestinal enzymes in the European Starling (Sturnus vulgaris). Physiological Zoology 68: 490-511. [ Links ]
MARRIOT RW & DK FORBES (1970) The digestion of Lucerne chaff by Cape Barren Geese Cereopsis novaehollandiae Latham. Australian Journal of Zoology 18: 257-263. [ Links ]
MAUSETH JD (1995) Botany. An introduction to plant biology. 2nd edition, Saunders College Publishing, London. 794 pp. [ Links ]
McLELLAND J (1979) Digestive system. In: King AS & J McLelland (eds) Form and function in birds: 69-167. Academic Press, New York. [ Links ]
McNAB BK (1986) The influence of food habits on the energetics of eutherian mammals. Ecological Monographs 56: 1-19. [ Links ]
McNAB BK (1988a) Food habits and the basal rate of metabolism in birds. Oecologia 77: 343-349. [ Links ]
McNAB BK (1988b) Complications inherents in scaling the basal rate of metabolism in mammals. Quarterly Review in Biology 63: 25-54. [ Links ]
McNAB BK (1994) Energy conservation and the evolution of flightlessness in birds. American Naturalist 144: 628-642. [ Links ]
McWILLIAMS SR, E cavieres-vidal & WH karasov (1999) Digestive adjustments in Cedar Waxwings to high feeding rate. Journal of Experimental Zoology 283: 394-407. [ Links ]
MEYNARD C, MV LOPEZ-CALLEJA, F BOZINOVIC & P SABAT (1999) Digestive enzymes of a small avian herbivore, the Ruffous-tailed Plantcutter. Condor 101: 904-907. [ Links ]
MORTON ES (1978) Avian arboreal folivores: Why not? In: Montgomery GG (ed) The Ecology of arborean folivores: 123-130. Smithsonian Institution Press, Washington, DC. [ Links ]
MOSS R (1974) Winter diet, gut lengths, and interspecific competition in Alaskan Ptarmigan. Auk 91: 737-746. [ Links ]
NAGY KA (1987) Field metabolic rates and food requirement scaling in mammals and birds. Ecological Monograph 577: 111-128. [ Links ]
NOBLE JC (1991) On ratites and their interactions with plants. Revista Chilena de Historia Natural 64: 85-118. [ Links ]
NORBERG UM (1996) Energetics of flight. In: Carey C (ed) Avian energetics and nutritional ecology: 199-249. Chapman & Hall, New York. [ Links ]
PARRA R (1978) Comparison of foregut and hindgut fermentation in herbivores. In: Montgomery GG (ed) The ecology of arboreal folivores: 205-229. Smithsonian Institution Press, Washington, DC. [ Links ]
PENRY DL & PA JUMARS (1986) Chemical reactor analysis and optimal digestion. Bioscience 36: 310-314. [ Links ]
PENDARGAST BA & DA BOAG (1974) Nutritional aspects of the diet of Spruce Grouse in central Alberta. Condor 73: 437-443. [ Links ]
PETERS RH (1983) The ecological implications of body size. Cambridge University Press, Cambridge. 437 pp. [ Links ]
PETERSON CC, KA NAGY & J DIAMOND (1990) Sustained metabolic scope. Proceeding of Naturalist Academy of Science 87: 2324-2328. [ Links ]
PRINZINGER R, R GÖPPEL, A LORENZ & E KULZER (1981) Body temperature and metabolism in the Red-backed Mousebird (Colius castanotus) during fasting and torpor. Comparative Biochemistry and Physiology 69A: 689-629. [ Links ]
RICKLEFS RE (1996) Morphometry of the digestive tract of some passerine birds. Condor 98: 279-292. [ Links ]
SABAT P (2000). Enzymes activities and digestive constrains in two species of Cinclodes (Passerine: Furnaridae). Revista Chilena de Historia Natural. [ Links ]
SABAT P, F NOVOA, F BOZINOVIC & C MARTINEZ DEL RIO (1998) Dietary flexibility and intestinal plasticity in birds: a field and laboratory study. Physiological Zoology 71: 226-236. [ Links ]
SCHMIDT-NIELSEN K (1990) Animal physiology. Adaptation and environment. Cambridge University Press, New York. 444 pp. [ Links ]
SHORT HL, RM BLAIR & CA SEGELQUIST (1974) Fiber composition and forage digestibility by small ruminants. Journal of Wildlife Management 38: 197-209. [ Links ]
SIBLY RM (1981) Strategies in digestion and defecation. In: Townsend CR and P Calow (eds) Physiological ecology: an evolutionary approach to resource use: 109-139. Blackwell Scientific Publications, Oxford. [ Links ]
SKADHAUGE E (1976) Osmoregulation in birds. Springer-Verlag, Berlin. [ Links ]
TAKEKAWA JY (1987) Energetics of Canvasbacks staging on an Upper Mississippi river pool during fall migration. Ph.D. dissertation Iowa State University, Ames. [ Links ]
VAN SOEST PJ (1982) Nutritional ecology of the ruminant. Cornell University Press, Ithaca, New York, USA. [ Links ]
VEHRENCAMP SL, JW BRADBURY & RM GIBSON (1989) The energetic cost of display in male Sage Grouse. Animal Behavior 38: 885-896. [ Links ]
WARNER ACI (1981) Rate of passage of digesta through the gut of mammals and birds. Nutritional Abstract Review B51: 780-820. [ Links ]
WEATHERS WW (1979) Climatic adaptation in avian standard metabolic rate. Oecologia 42: 81-89. [ Links ]
WEINER J (1992) Physiological limits to sustainable energy budgets in birds and mammals: ecological implications. Trends in Ecology and Evolution 7: 384-388. [ Links ]
ZISWILER V & DS FARNER (1972) Digestion and the digestive system. In: Farner DS & JR King (eds) Avian Biology: 313-405. Academic Press, London. [ Links ]