ORNITOLOGIA NEOTROPICAL 18: 21–36, 2007 © The Neotropical Ornithological Society
DIETS OF CRACIDS: HOW MUCH DO WE KNOW?
Marcia C. Muñoz1 & Gustavo H. Kattan
Fundación EcoAndina/Wildlife Conservation Society Colombia Program, Avenida 2 Oeste, No. 10-54, Cali, Colombia. E-mails: [email protected] & [email protected]
Resumen. – Dietas de crácidos: ¿qué tánto sabemos? – Los Cracidae son una familia Neotropical de 50 especies de aves galliformes, muchas de las cuales están amenazadas. A través de una revisión de litera- tura, evaluamos el conocimiento actual de los hábitos alimentarios de los crácidos y establecimos algunos patrones generales. La dieta ha sido relativamente bien documentada para 17 especies, mientras que para otras 19 especies hay información anecdótica, y para 14, no hay información disponible. La fruta es la cate- goría de alimento más importante para los crácidos y se han documentado 672 especies de frutas de todos los tipos en sus dietas (tales como drupas, bayas y arilos). Las familias de plantas más importantes en la dieta de la mayoría de los crácidos son también las más comunes y diversas en los bosques Neotropicales. El follaje, las flores y el material animal (vertebrados e invertebrados) también son comunes en la dieta. El consumo de follaje en particular es común en la mayoría de las especies, pero la folivoría no ha sido ade- cuadamente estudiada en estas aves. Las especies de la subfamilia Penelopinae generalmente pasan las semillas intactas a través del tracto digestivo y son potenciales diseminadoras de semillas. Las especies de Cracinae, en cambio, tienen mollejas fuertes y se alimentan de las semillas grandes; sólo las semillas peque- ñas pasan por el tracto intactas. En general los crácidos parecen tener dietas amplias y generalistas, aunque se han documentado dietas restringidas en respuesta a condiciones locales. Pocos estudios han evaluado las variaciones estacionales y entre hábitats en la disponibilidad de recursos y las respuestas de los crácidos a tales variaciones. El estudio de los patrones de uso y disponibilidad de recursos es esencial para entender los patrones de uso de hábitat, las necesidades de espacio y la dinámica poblacional de los crácidos. Abstract. – The Cracidae are a Neotropical family of 50 species of galliform birds, many of which are threatened. Through a literature review, we evaluated current knowledge of cracid food habits and estab- lished general dietary patterns. Diet has been relatively well documented for 17 species, anecdotal informa- tion is available for 19 species, and no information is available for 14 species. Fruit is the most important food category for cracids, and 672 species in all fruit types (e.g., drupes, berries, arillate fruits) are reported. For most species, the most important plant families in their diets are also the most common and diverse families in Neotropical forests. Foliage, flowers and animal foods (invertebrate and vertebrate) are also common items in cracid diets. Consumption of foliage, in particular, is widespread but folivory has not been adequately studied in these birds. Penelopinae usually pass seeds intact through the digestive tract and are potential seed dispersers. Cracinae, in contrast, have strong gizzards and usually feed on large seeds, with only small seeds passing intact. In general, cracids seem to have broad and generalist diets, although restricted diets in response to local conditions have been reported. Few studies have evaluated seasonal and habitat variations in resource availability and cracid responses to such variation. An understanding of patterns of resource use and availability is essential for understanding habitat use, space needs and popula- tion dynamics of Cracids. Accepted 14 October 2006. Key words: Cracidae, Cracinae, diet, frugivory, folivory, Penelopinae, seed dispersal. ______1Present address: Department of Biology, University of Puerto Rico, San Juan, PR 00931.
21 MUÑ0Z & KATTAN
INTRODUCTION We conducted a literature search to com- pile information on cracid diets. From each The Cracidae (chachalacas, guans and curas- study we extracted information on geo- sows) are a family of 50 species of large-bod- graphic location, methods, and food items ied, galliform birds with a Neotropical reported in the diet. Because of the heteroge- distribution. Most species inhabit dense tropi- neity in methods and the nature of data, we cal and subtropical forest; only a few species quantified diets in terms of the number of of chachalacas are found in open woodlands taxonomic units (number of items) reported (del Hoyo 1994, Delacour & Amadon 2004). for each cracid species. For plants (fruits, Almost all species in this family are under leaves and flowers), items represent species, some degree of threat because of habitat loss but for insects items represent orders or fami- and hunting (Strahl & Grajal 1991, Collar et al. lies, and vertebrates include items such as 1992, del Hoyo 1994, Stattersfield & Capper "frog" or "rat". 2000, Brooks & Strahl 2000, BirdLife Interna- We organized this review as a series of tional 2004). This situation has led to the topics or questions. After presenting the two development of conservation action plans for cracid subfamilies, we review information on some species (e.g., Brooks & Strahl 1998, the qualitative and quantitative composition Kattan & Valderrama 2006). of cracid diets. Next, we discuss food quality One limitation for developing conserva- and digestive adaptations, and review our tion plans for these species is the lack of knowledge of seasonal and geographic varia- detailed knowledge of their biology, particu- tion in cracid diets. Then we discuss the ques- larly in basic aspects such as patterns of habi- tion whether cracids are selective or have tat and space use. Some species are sedentary, generalist diets. We finish by discussing the but others apparently perform seasonal role of cracids as seed dispersers. movements (habitat shifts or regional migra- tions) (Chaves-Campos 2004). This knowl- THE CRACIDAE edge is critical for designing conservation areas that can sustain viable populations. The family Cracidae is divided into two sub- An important factor determining move- families, the Penelopinae and the Cracinae ment patterns is resource use. Cracids are (del Hoyo 1994, Pereira et al. 2002). Penelopi- omnivores, feeding on fruit, foliage and nae (36 species of guans and chachalacas, 42– insects (Delacour & Amadon 2004), but 91 cm in total length, and 385–2430 g in body curassows have also been reported feeding on mass) have arboreal habits. Cracinae (14 spe- vertebrates and seeds (Érard et al. 1991, cies of curassows) are larger (50–95 cm in Yumoto 1999, Santamaría & Franco 2000, total length and 1250–4800 g in body mass) Jiménez et al. 2001). However, the diet of few and mostly terrestrial, although they may species has been studied in detail, and it is roost and nest in trees (del Hoyo 1994). unclear to what extent they have specialized Recently, the genera Ortalis and Oreophasis or generalized diets. Here we present a review were transferred to the subfamily Cracinae of studies on cracid diets. In addition to (Pereira et al. 2002). These birds, however, are reviewing current knowledge on the food ecologically more similar to the Penelopinae, habits of this family, information provided and we followed del Hoyo (1994) and Dela- here could be useful for guiding future studies cour & Amadon (2004) in retaining them in and developing models for understanding this subfamily. Both genera are old, having cracid ecology. diverged about 31.1 and 30.9 million years
22 DIETS OF CRACIDS
TABLE 1. Species of cracids with information about diet, type of study in which information was obtained, country where studied, and conservation priority according to IUCN/Cracid Specialist Group.
Species Conservation Type of Country References3 priority1 study2 Ortalis O. vetula Sp, Co Unites States 7, 19, 27 O. garrula O. cinereiceps Co 7 O. poliocephala Sp Mexico 12 O. wagleri O. leucogastra O. ruficauda INCP Sp Venezuela 2, 7 O. erythroptera VHCP Co Ecuador 15 O. canicollis Sp, Co Argentina 5, 7 O. guttata Co 7 O. superciliaris ICP O. motmot Penelope P. purpurascens INCP Co, Tc Colombia, Costa Rica 26, 28 P. perspicax ICP Tc, Co Colombia 22, 23, 30, 35 P. albipennis ICP Co Peru 7, 36 P. ortoni HCP P. marail Sp Guyana, Surinam 14, 37 P. jacquacu Sp, Co Colombia, Venezuela 3, 40 P. ochrogaster HCP Co Brazil 24 P. pileata HCP P. dabbenei HCP P. jacucaca HCP P. superciliaris Tc, Co Brazil 7, 21 P. obscura INCP Tc, Co Argentina 6, 18, 20 P. argyrotis INCP Co 7 P. barbata APC P. montagnii INCP Co Colombia 23 Pipile P. pipile INCP Co Trinidad 7, 16 P. cumanensis Sp, Co Venezuela 7, 40 P. cujubi INCP P. jacutinga VHCP Tc, Co Brazil 9, 25 Aburria Aburria aburri HCP Co Colombia 32 Chamaepetes C. goudotii INCP Co Colombia 7, 23, 29 C. unicolor VHCP Co Costa Rica 7, 38 Penelopina P. nigra HCP Co Mexico 7, 11 Oreophasis O. derbianus ICP Co, Tc Mexico 7, 10
23 MUÑ0Z & KATTAN
TABLE 1. Continued.
Species Conservation Type of Country References3 priority1 study2 Nothocrax N. urumutum Co Colombia 3 Mitu M. mitu ICP Co 7 M. tuberosa INCP Co Peru 7, 13 M. salvini INCP Tc Colombia 7, 33, 39 M. tomentosa Sp Venezuela 40 Pauxi P. pauxi ICP Co Venezuela 4, 7 P. unicornis VHCP Co Bolivia 7, 31 Crax C. rubra HCP Tc Salvador 7, 34 C. alberti ICP C. alector Tc, Sp, Co Colombia, Guyana, Surinam, 1, 3, 8, 14, 17, 40 Venezuela C. daubentoni HCP C. fasciolata HCP Co 7 C. globulosa HCP C. blumenbachii ICP Co 7
1ICP: Immediate conservation priority, VHCP: very high conservation priority, HCP: high conservation priority, INCP: intermediate conservation priority.
2Co: Casual observations in short-term studies, Sp: data obtained from specimens, Tc: methodical studies with temporal continuity.
31 (Álvarez-Cordero 1997), 2 (Arriaga & Bermúdez 1997), 3 (Benett & Defler 1997), 4 (Calchi & Pérez 1997), 5 (Caziani & Protomastro 1994), 6 (Chalukian 1997), 7 (Del Hoyo 1994), 8 (Érard et al. 1991), 9 (Galetti et al. 1997), 10 (González-García 1994), 11 (González-García et al. 2001), 12 (Gurrola 1981), 13 (Gutiérrez 1997), 14 (Held & Werkhoven 1997), 15 (Isherwood & Willis 1999), 16 (James & Hislop 1997), 17 (Jiménez et al. 2001), 18 (Malzof et al. 2006), 19 (Marion 1976), 20 (Merler et al. 2001), 21 (Mikich 2002), 22 (Muñoz 2003), 23 (Nadachoswki 1994), 24 (Olmos 1998), 25 (Paccagnella et al. 1994), 26 (Pacheco 1994), 27 (Pence & Scott 1978), 28 (Pérez & Pinedo 2002), 29 (Renjifo 1997), 30 (Renjifo 2002), 31 (Renjifo & Renjifo 1997), 32 (Ríos et al. 2005), 33 Santamaría & Franco 2000), 34 (Sermeño 1997), 35 (Silva 1997), 36 (Tejada & Díaz 1997), 37 (Théry et al. 1992), 38 (Wheelwright et al. 1984), 39 (Yumoto 1999), 40 (Zent 1997).
24 DIETS OF CRACIDS 6.4 2.7 9.1 %Others invertebrates and invertebrates f
5 (Mo) %Vertebrates 3 8,3 9.5 3.1 6.7 2.4 21.9 4.3 (Ga) 4.3 %Invertebrates (Co, Le, Hy, Ho) Hy, Le, (Co, (Ho, Di, Co, Ho) Co, Di, (Ho, 50 25 21 6.4 9.5 9.4 5.6 6.3 9.1 12.5 24.4 16.7 %Flowers 50 8.6 6.7 2.9 9.1 19.1 16,7 14.3 16.7 16.7 12.5 14.3 %Leaves 75 75 76 95 100 100 100 100 100 100 63.8 66.7 78.1 87.5 78.9 72.9 94.4 66.6 77.1 87.5 86.6 97.1 72.7 83.3 %Fruits 1 8 1 2 4 1 8 48 12 21 32 23 37 54 30 48 52 22 46 15 34 11 20 42 128 # Items ) and its percent in the diet of each species. species. each of diet the in percent ) and its 1 O. erythroptera O. vetula O. cinereiceps poliocephala O. O. ruficauda O. canicollis O. guttata jacquacu P. ochrogaster P. montagnii P. perspicax P. P. marail argyrotisP. superciliaris P. albipennis P. P. obscura purpurascens P. A. aburri cumanensis P. jacutinga P. pipile P. C. unicolor C. goudotii P. nigra derbianus O. Species Penelopinae Cracinae TABLE 2. Items recorded in the diets of cracids. The table indicates the total number of items (plant species, order or class o class or order species, (plant items of number total the Theindicates table cracids. of diets the in recorded 2. Items TABLE vertebrates
25 MUÑ0Z & KATTAN 16 50 7.0 ptera, Is: ptera, 17.2 Gym: Gymnophiona, 12 25 2.3 1.6 5.0 Ar) (Fro, Gym) (Fro, (Fro, Li, Mo, Se, Se, Mo, Li, (Fro, era, Ho: Homoptera, Hy: Hymeno era, Ho: Homoptera, 12 12 5.8 5.0 1.2 De) 15.4 50 (Di, Col) (Di, 50 (Le, Or, Co) Or, (Le, Op: Opiliones, Ar:Op: Opiliones, Armadillo, Ho, He, Di, Co, Le, Le, Co, Di, He, Ho, (Od, Or, Ph, Ma, Is, Ph, Ma, Is, Or, (Od, Hy, Ur, Ar, Am, Op, Op, Am, Ar, Ur, Hy, 2.9 100 ptera, Ga: Gastropoda, He: Hemipt Gastropoda, Ga: ptera, era, Ph: Phasmida, Ur: Phasmida, Ph: era, Uropygi, 8 20 4,6 1.9 7.7 52 50 25 70 100 100 100 84.9 70.6 76.9 1 2 2 4 1 86 12 27 20 13 306 N. urumutum N. M. salvini M. tomentosa M. tuberosa M. mitu pauxi P. unicornis P. C. alector C. rubra C. fasciolata blumenbachii C. Isoptera,Lepidoptera, Le: Ma: Mantodea,Od: Odonata, Or: Orthopt Li: Lizard, Fro: Frog, Mo: Mouse, Se: Snake. Snake. Se: Mouse, Mo: Frog, Fro: Lizard, Li: Am: Amblypygi, Ar: Co: Coleoptera, Araneae, De: Decapoda, Di: Di Species # Items %Fruits %Leaves %Flowers %Invertebrates %vertebrates %Others 1 TABLE 2. Continued.
26 DIETS OF CRACIDS
Cracinae Penelopinae 45 40 35 30 25 20 15 10 5 0 Number of species of plants of species of Number e ae ae eae e eae e eae eae ea c ceae iac tac ac ac ba el ali inaceae Mora Fa rs indac ArecaceaeRubiaceae M Lauraceaetomatac Myr Ar agin y Burseraceae Solanaceae or M ap Cecropiaceae B S Melas Fam ilies
FIG. 1. Number of plant species most consumed per family by the two subfamilies of cracids. ago, respectively (Pereira et al. 2002). Likewise, (Galetti et al. 1997), Oreophasis derbianus for 8 the current Penelopinae genera are the oldest months (González-García 1994), Mitu salvini in the family, having diverged on average 18– for 14 months (Santamaría & Franco 2000), 19 million year ago, whereas Cracinae are Crax alector for 10 months (Jiménez et al. 2001) more recent, appearing 6–12 millions year ago and C. rubra for 16 months (Sermeño 1997). (Pereira et al. 2002). Information is lacking for the other 14 spe- cies, 10 of which are under some threat cate- WHAT DO CRACIDS EAT? gory (Table 1). The mean number of food items reported Information on food habits of cracids has in the diet is 32 for 36 species of cracids been published for 36 of the 50 species. Most (Table 2). The mean number of items for of the information consists of lists of items Penelopinae is 27.2, varying between 1 (Ortalis eaten by cracids and comes from anecdotal erythroptera and Penelope argyrotis) and 128 (P. studies (19 species) or from examination of perspicax). For Cracinae, the mean is 43 and stomach contents (8 species). Only 9 species the range is 1 (Nothocrax urumutum and C. fasci- have been studied methodically and with olata) to 306 (C. alector). Fruit is an important some temporal continuity: Penelope perspicax component in the diet of all species, ranging was studied for over 2 years (Muñoz 2003, from 50 to 100% of recorded items (ignoring Kattan et al. in press, Muñoz et al. in prep.), P. species with less than 20 records; Table 2). A obscura for 4 months (Merler et al. 2001) and 1 total of 672 species of fruits have been year (Malzof et al. in press), P. superciliaris for 8 reported in cracid diets. All fruit types are rep- years (Mikich 2002), P. purpurascens for 1 year resented. Drupes are the most common fruit (Pacheco 1994), Pipile jacutinga for 2 years type (41% of species), followed by berries
27 MUÑ0Z & KATTAN
Penelopinae Cracinae 16 14 12 10 8 6 4 2 0
ae e ae e eae eae ce ceae ceae ceae c acea rac a a iaceae
Number of species of cracids of species of Number i bia ataceae nace b u op reca nda si abacea yrt en seraceae MoraceaeR r Lau A m F M b r api Myr er S sto V BignoniaceaeBu Cec a Euphor Mel Families
FIG. 2. Number of species of cracids reported eating different plant families.
(19%), capsules (11%), arillated seeds (4%), of Cracinae (Érard et al. 1991, Jiménez et al. legumes (4%), syconia (Ficus spp.; 4%) and 2001; see seed dispersal below). multiple fruits (3%). Other fruit categories Feeding on invertebrates has been (e.g., nut, sorosis, samara) add to 14%. reported for 14 species and may represent The six most important plant families in over 20% of items. Feeding on vertebrates cracid diets are Moraceae, Arecaceae, Rubi- (frogs, rats) has only been reported for 5 spe- aceae, Fabaceae, Cecropiaceae and Lauraceae cies of Cracinae and for Penelopina nigra. Most (Fig. 1), but a total of 113 families are studies suggest that cracids feed on animals reported. Diets of Penelopinae are broader, opportunistically and occasionally, but it may including more plant families than Cracinae be more important than previously thought (Fig. 1) and conversely, more species of (e.g., P. perspicax; Rios et al. 2006). Penelopinae are reported feeding on each Few studies present quantitative data on plant family (Fig. 2). cracid diets. Fruit may represent over 90% of Foliage and flowers usually represent less the bulk of the diet of Penelope marail in than 20% of items, but may be over 30% French Guiana (Érard & Théry 1994). A (Penelope albipennis). In the two best studied study based on stomach contents of C. alector species, P. perspicax and C. alector, these two in French Guiana (69 birds hunted between food categories represent 18% and 4.8%, 1977 and 1981) showed that fruit represented respectively. In general, foliage and flowers 84% of dry matter and that insects, leaves and seem to represent a more important food flowers represented less than 1% each (Érard source for Penelopinae than for Cracinae. In et al. 1991). Another study in eastern Colom- contrast, seeds are more important in the diet bia followed three individuals of C. alector for
28 DIETS OF CRACIDS
7 months, determining the number of items ceae and Solanaceae). Eating such a diversity eaten per day (Jiménez et al. 2001). Overall, of fruits provides energy in the form of car- fruit represented almost 50% of items bohydrates, lipids and proteins (e.g., Muñoz ingested per day, leaves about 15%, and inver- 2003). Drupes and arillate fruits tend to be tebrates a little over 10% for the three curas- rich in lipids, and berries tend to be rich in sows; these animals also fed on seeds and carbohydrates (Moermond & Denslow 1985), seedlings (Jiménez et al. 2001). but great variation exists even within genera. The diet of O. vetula has been determined For example, among fruits eaten by the Cauca in Texas on the basis of 42 stomach contents Guan, Muñoz (2003) found that Miconia acu- (Marion 1976). Invertebrates were a small minifera (Melastomataceae) had a much higher proportion of the diet (3.0% of diet by vol- lipid content than Aniba muca (Lauraceae). ume) and included hemipterans (less than Feeding on foliage is reported for most 0.1%), insect larvae (1.4%) and gastropods species, but its importance in cracid diets has (1.6%). This species ate large quantities of not been rigorously quantified. Comparing seeds (three species). The most consumed foods as different as fruits, foliage and insects seed species accounted for 10.1% of the diet in terms of their contribution to the energy by volume, and the others 0.2% and 0.1%. and nutrient budget is difficult. Studies on Leaves represented 6.5% (five species), but foraging ecology usually quantify foods in one species represented most of this con- terms of feeding bouts or food volume, but sumption (3.8%). Stamens and fruit were the these do not reflect the energetic contribution parts with the highest volume (19.2% and of the different items. On the other hand, 57.3%, respectively) in the diet of this chacha- some foodstuffs may provide essential nutri- laca. On the other hand, another study on the ents, even if consumed in small quantities. same species suggested that it is herbivorous Foliage is a low-quality food compared to and frugivorous because arthropods were not fruits or insects. In the absence of special found in 19 chachalacas collected in one adaptations such as gut fermentation, as month (Pence & Scott 1978). occurs in the Hoatzin (Opisthocomus hoatzin) (Grajal et al. 1989), folivorous birds such as FOOD QUALITY AND DIGESTIVE geese (Anseriformes) compensate by process- ADAPTATIONS ing large quantities of foliage and passing it rapidly through the digestive tract (Buchs- The variety of food types eaten by cracids baum et al. 1986). With the exception of P. suggests that these birds are behaviorally plas- perspicax, which seasonally feeds on large tic and have digestive tracts adapted to a gen- quantities of foliage when fruit is scarce eralist diet. Cracinae have well developed (Muñoz 2003), cracids reportedly eat leaves in gizzards capable of crushing seeds, which is small quantities and mixed with other food- helped by ingesting grit (Moermond & Den- stuffs. Preliminary data indicate that with a slow 1985, Érard et al. 1991), while Penelopi- highly folivorous diet, guans loose weight nae do not have this capacity. Otherwise, no (Muñoz unpubl.). It is unlikely, therefore, that special morphological or physiological diges- guans derive an important proportion of their tive adaptations have been reported for crac- energy budget from foliage. Plant foods are ids. more nutritionally diverse than animal foods Cracids eat a very wide variety of fruit (Klasing 1998), so cracids may be obtaining types, ranging from large drupes (Lauraceae important nutrients from foliage. Folivory in and Arecaceae) to small berries (Melastomata- cracids is an open research line, with impor-
29 MUÑ0Z & KATTAN tant ecological and physiological implications. quality foods, or performing local to regional Animal foods (insects and vertebrates), on (elevational) migrations (Fleming et al. 1987, the other hand, although making up a small Van Schaik et al. 1993, Sun et al. 1997, Sun & proportion of cracid diets in terms of volume Moermond 1997, Stiles 1988, Jiménez et al. or feeding bouts (Marion 1976, Jiménez et al. 2001). For instance, in Costa Rica, some indi- 2001), may provide an important portion of viduals of P. purpurascens remained in the same their energy and nutrient budget. Lepi- place throughout the year, but part of the dopteran larvae, for example, provide 49.4– population migrated altitudinally in response 58.1% protein and 10–20.7% lipids on a dry to fruit abundance (Chaves-Campos 2004). A weight basis (Landry et al. 1986) and are population of Cauca Guans in the central important sources of calcium and phospho- Andes of Colombia showed a diet shift, rus (Robel et al. 1995). resorting to folivory in response to a decrease Assessing diet quality requires not only in fruit availability (Kattan et al. in press, determining nutrient content of foodstuffs, Muñoz et al. in prep.). M. salvini also per- but also the capacity of animals to digest the formed habitat shifts in response to changing food and assimilate nutrients. In addition, resource availability in lowland forest (Parra et changes in diet may induce morphological al. 2001). and physiological changes in bird digestive In contrast, studies on C. alector in French tracts (e.g., Martínez del Río et al. 1995), so Guiana (Érard et al. 1991) and eastern Colom- studies on diet quality must take into account bia (Jiménez et al. 2001) have shown little vari- these considerations. These aspects have not ation in diet composition among seasons, been investigated in cracids. except for an increase in the consumption of seeds and seedlings during the rainy season in VARIATIONS IN CRACID FOOD the Colombian study. HABITS SELECTIVE FEEDERS? Little information is available on temporal and spatial variation in cracid diets. In sub- Some authors have suggested that cracids are tropical and temperate zones, food availability selective frugivores. For example, Théry et al. changes drastically between summer and win- (1992) found that P. marail in French Guiana ter. Thus, in Texas the diet of O. vetula was fed mostly on drupes, and preferred four out dominated by berries and seeds during spring of 23 fruit species recorded in the diet. In and fall, and leaves and buds during winter southern Brazil, P. superciliaris was found to and summer. Lowland forests in the Neotro- feed heavily on one species of palm (Euterpe pics may also show marked seasonality in fruit edulis) for a period of several months (Mikich availability (Frankie et al. 1974, Van Schaik et 2002). al. 1993), even causing animal mortality (Fos- Other studies, however, have found that ter 1982). In contrast, fruit availability in cracids are opportunistic generalists. For montane forest varies seasonally, but appar- example, P. perspicax was observed eating 89 ently there is no season of absolute scarcity species of fruit (80.2% of items) in 1 year, and (Giraldo 1990, Ataroff 2001, Cavelier et al. species were eaten in proportion to their 2001, Muñoz 2003). availability (Muñoz et al. in prep.). This species Fruit-eating animals may show varied also fed on foliage (9.9%), flowers (9.9%), responses to periods of fruit scarcity, includ- and insects (fragments found in 111 fecal ing habitat and diet shifts, resorting to low- samples of 391 samples collected) during a 1-
30 DIETS OF CRACIDS year study (Muñoz et al. in prep.). This species digestive tracts and may act as seed dispersers was also observed following army ants and (Galetti et al. 1997, Merler et al. 2001, Mikich feeding on flushed insects (24 observations in 2002, Muñoz 2003). For example, seeds main- eight months; Rios et al. 2006), and eating fila- tain their germination capacities after passing mentous algae on boulders in the river (W. through the digestive tract of P. marail and P. Cardona, pers. com.). perspicax, and birds disperse them away from Another line of evidence suggesting that parent trees, depositing them at the edges of cracids are generalists is that the most com- treefall gaps and other situations conducive to mon plant families in cracid diets (Fig. 1) cor- forest regeneration (Érard & Théry 1994, respond to the most common and diverse Théry et al. 1992, M. Muñoz, unpubl.). plant families in Neotropical forests. Most Some Penelopinae, however, may digest Penelopinae inhabit montane forest, and the seeds. Stomachs of O. vetula contained seeds most common plant families in their diets of Ulmus crassifolia, Acacia farnesiana and Serja- (Lauraceae, Rubiaceae, Moraceae, Melasto- nia brachycarpa (Marion 1976). These species mataceae and Arecaceae) are also the most produce dry fruits, so chachalacas likely diverse in mid- and high-elevation (1500– digested the seeds. Another Penelopinae spe- 2900 m) Andean forest (Gentry 2001). cies, P. albipennis, fed on Bombax sp. seeds, Cracinae, in contrast, are mostly lowland for- which also produces dry fruits. est species. The most common families in For Cracinae, in contrast, seed consump- Cracinae diets (Moraceae, Arecaceae, tion is a routine part of their diets, but they Rubiaceae, Leguminosae and Meliaceae) are may act as dispersers of small seeds (Yumoto also the most common among 90 plant fami- 1999, Santamaría & Franco 2000, Jiménez et lies in Neotropical lowland forest (Gentry al. 2001). For example, M. salvini feeds on big 2001). seeds and is a disperser of small seeds (< 5.5 The available data, thus, suggest that crac- mm length), as only small seeds are excreted ids have broad diets, feeding on a variety of intact. Érard et al. (1991) showed that C. alector plant and animal foods (and other minor food crushes seeds in its gizzard, which contains categories) that are probably obtained oppor- large amounts of grit. tunistically. Extrapolating from general pat- The potential of cracids as seed dispersers terns at the family level to particular species is important from a conservation perspective should be made with caution, however, as (the role they play in the ecosystem; Strahl & even congeneric species may diverge in their Grajal 1991). The effectiveness of a frugivore food habits. Species may exhibit restricted as a seed disperser depends on two parame- diets in response to local conditions (Mikich ters, the number of seeds dispersed and the 2002). Diets may also change seasonally, and quality of dispersion (Schupp 1993). Each short-term studies do not reflect the ampli- parameter, in turn, has several components, tude of conditions to which cracids are including number of visits to the plant, num- exposed (see seasonal variation above). ber of seeds removed per visit, seed manipula- tion and movement patterns of frugivores. CRACIDS AS SEED DISPERSERS Cracids, particularly Penelopinae, have the capacity to move enormous numbers of seeds The role of fruit-eating animals as seed dis- and to deposit them in varied situations, but persers partially depends on the fate of seeds the exact role that they play as dispersers in passing through the digestive tract. Penelopi- comparison with other frugivores remains to nae usually pass seeds intact through their be determined. Currently, there is only one
31 MUÑ0Z & KATTAN study evaluating dispersion by M. salvini their valuable suggestions that substantially (Yumoto 1999). This species is a seed preda- improved the manuscript. tor, but it is the most important disperser of Geophila rupens. Out of 11 species of plants REFERENCES consumed by this curassow, two species of plant (G. rupens and Ficus sphenophylla) were Álvarez-Cordero, E. 1997. Distribución y car- dispersed. acterísticas del hábitat de los Crácidos Ortalis motmot y Crax alector en la zona inundada del CONCLUSIONS embalse Guri, Estado Bolivar, Venezuela. Pp. 23–25 in Strahl, S. D., S. Beaujon, D. M. This review revealed that few rigorous quanti- Brooks, A. J. Begazo, G. Sedaghatkish, & F. tative studies on cracid diets are available. The Olmos (eds.). The Cracidae: Their biology and bulk of cracid diets is made up by fruits, but conservation. Hancock House Publishers Ltd., Surrey, British Columbia, and Blaine, Washing- they opportunistically feed on a variety of ton. plant and animal foods. However, it is Arriaga, I., & S. Bermúdez. 1997. Dieta de la Gua- unknown to what extent the different compo- characa (Ortalis ruficauda) en el Estado Cojedes. nents of the diet are providing energy or Pp. 34–47 in in Strahl, S. D., S. Beaujon, D. M. essential nutrients. More importantly from a Brooks, A. J. Begazo, G. Sedaghatkish, & F. conservation perspective, little is known Olmos (eds.). The Cracidae: Their biology and about seasonal and geographic variation in conservation. Hancock House Publishers Ltd., resource use. In particular, the role of foliage Surrey, British Columbia, and Blaine, Washing- as a complementary or seasonal resource in ton. cracid diets needs to be elucidated. Ataroff, M. 2001. Venezuela. Pp. 397–442 in Kap- Patterns of resource use may have impor- pelle, M & A. D. Brown (eds.). Bosques nubla- dos del Neotrópico. Instituto Nacional de tant consequences for population dynamics Biodiversidad de Costa Rica., San José, Costa and habitat requirements. Under certain cir- Rica. cumstances, cracid diets may be specialized or Benett, D. S., & T. R. Defler. 1997. Anotaciones restricted, but it is unknown whether this is a sobre los crácidos del bajo Apaporis en el sur- local or seasonal response to food availability. este de Colombia. Pp. 289–297 in Strahl, S. D., A varied diet may be important for the gen- S. Beaujon, D. M. Brooks, A. J. Begazo, G. eral health and vigour of the animals. Isolated Sedaghatkish, & F. Olmos (eds.). The Cracidae: populations may survive on a few food Their biology and conservation. Hancock sources (e.g., Merler et al. 2001), but are not House Publishers Ltd., Surrey, British Colum- necessarily healthy. Understanding all these bia, and Blaine, Washington. features of cracid biology is essential for BirdLife International. 2004. IUCN red list of threatened species.
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Paccagnella, S. G., R. A. Filho., A. I. Lara, & P. S. Densidad poblacional e historia natural de la Neto. 1994. Observaçoes sobre Pipile jacutinga Pava negra (Aburria Aburri) en los Andes cen- Spix, 1825 (Aves, Cracidae) no Parque Estadual trales de Colombia. Ornitol. Neotrop. 16: 205– de Carlos Botelho, Sao Paulo, Brasil. Iheringia 217. Ser. Zool. 76: 29–32. Ríos, M. M., M. C. Muñoz, & G. Londoño. 2006. Pacheco, C. 1994. Hábitos alimenticios y uso esta- Historia natural de la Pava caucana (Penelope cional de hábitats de la pava crestada (P. pur- perspicax). Ornitol. Colomb. 4: 16–27. purascens) en el bosque seco tropical, Parque Robel, R., B. M. Press, B. Henning, & K.W. Nacional de Santa Rosa, Costa Rica. Doctoral Johnson. 1995. Nutrient and energetic charac- Thesis, Univ. Nacional, Heredia, Costa Rica. teristics of sweepnet–collected invertebrates. J. Parra, J. L., M. Agudelo, Y. Molina, & G. Londoño. Field Ornithol. 66: 44–53. 2001. Use of space by a pair of Salvin’s Curas- Santamaría, M., & A. M. Franco. 2000. Frugivory sows (Mitu Salvini) in northwestern Colombian of Salvin’s Curassow in a rainforest of the Amazon. Ornitol. Neotrop. 12: 189–204. Colombian Amazon. Wilson Bull. 112: 473– Pence, D., & G. Scott. 1978. Notes on food habits 481. of the Plain Chachalaca from the lower Rio Schupp, E. 1993. Quantity, quality and the effec- Grande Valley. Wilson Bull. 90: 647–648. tiveness of seed dispersal by animals. Vegetatio Pérez, M. T., & I. E. Pinedo. 2002. Notas sobre la 107/108: 15–29. historia natural de la pava (Penelope purpurascens) Sermeño, A. 1997. Alimentación y reproducción en Bolivar, Colombia. Bull. IUCN/Birdlife/ del paujil (Crax rubra) en El Salvador. Pp. 71–78 WPA CSG 15: 10–13. in Strahl, S. D., S. Beaujon, D. M. Brooks, A. J. Pereira, S., A. Baker, & A. Wajntal. 2002. Com- Begazo, G. Sedaghatkish, & F. Olmos (eds.). bined nuclear and mitochondrial DNA The Cracidae: Their biology and conservation. sequences resolve generic relationships within Hancock House Publishers Ltd., Surrey, British the Cracidae (Galliformes, Aves). Syst. Biol. 51: Columbia, and Blaine, Washington. 946–958. Silva, L. 1997. Biología de Penelope perspicax. B. Sc. Renjifo, L. M. 1997. Observaciones preliminares de thesis, Univ. del Valle, Cali, Colombia. dos especies de pavas en el alto Quindío, Stattersfield, A. J., & D. R. Capper. 2000. Threat- Colombia. Pp. 14–16 in Strahl, S. D., S. Beau- ened birds of the world. Lynx Edicions & jon, D. M. Brooks, A. J. Begazo, G. Sedaghatk- BirdLife International, Barcelona, Spain, & ish, & F. Olmos (eds.). The Cracidae: Their Cambridge, UK. biology and conservation. Hancock House Stiles, G. 1988. Elevational movements of birds on Publishers Ltd., Surrey, British Columbia, and the Caribbean slope of Costa Rica: implications Blaine, Washington. for conservation. Pp. 243–258 in Almeda, F., & Renjifo, L. M. 2002. Penelope perspicax. Pp. 124–130 C. M. Pringle (eds.) Tropical rain forest: diver- in Renjifo, L. M., A. M. Franco–Maya, J. D. sity and conservation. California Academy of Amaya–Espinel, G. Kattan, & B. López–Lanús Sciences, San Francisco, California. (eds.). Libro rojo de las aves de Colombia. Insti- Strahl, D., & A. Grajal. 1991. Conservation of large tuto de Investigación de Recursos Biológicos avian frugivores and the management of Neo- Alexander von Humboldt y Ministerio del tropical protected areas. Oryx 25: 50–55. Medio Ambiente, Bogotá, Colombia. Sun, C., & T. Moermond. 1997. Foraging ecology Renjifo, J., & T. Renjifo 1997. Pauxi unicornis: of three sympatric turacos in a montane forest Biología y ecología. Pp. 89–92 in Strahl, S. D., S. in Rwanda. Auk 114: 396–404. Beaujon, D. M. Brooks, A. J. Begazo, G. Sun, C., T. Moermond, & T. Givnish. 1997. Nutri- Sedaghatkish, & F. Olmos (eds.). The Cracidae: tional determinants of diet in three turacos in a Their biology and conservation. Hancock tropical montane forest. Auk 114: 200–211. House Publishers Ltd., Surrey, British Colum- Tejada, O. E., & V. R. Díaz. 1997. Estudio de bia, and Blaine, Washington. campo y reevaluación de la población de pava Ríos, M. M., G. Londoño, & M. C. Muñoz. 2005. aliblanca (Penelope albipennis). Pp. 218–232 in
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Strahl, S. D., S. Beaujon, D. M. Brooks, A. J. Guindon. 1984. Tropical fruit-eating birds and Begazo, G. Sedaghatkish, & F. Olmos (eds.). their food plants: a survey of a Costa Rican The Cracidae: Their biology and conservation. lower montane forest. Biotropica 16: 173–192. Hancock House Publishers Ltd., Surrey, British Yumoto, T. 1999. Seed dispersal by Salvin’s Curas- Columbia, and Blaine, Washington. sow, Mitu salvini (Cracidae), in a tropical forest Théry, M., C. Érard, & D. Sabatier. 1992. Les fruits of Colombia: direct measurements of dispersal dans le régime alimentaire de Penelope marail distance. Biotropica 31: 654–660. (Aves, Cracidae) en forêt Guyanaise: Frugivorie Zent, S. 1997. Piroa and the Cracidae: game man- stricte et sélective?. Rev. Ecol. (Terre Vie) 47: agement under shifting cultivation. Pp. 177– 383–400. 194 in Strahl, S. D., S. Beaujon, D. M. Brooks, Van Schaik, C. P., J. W. Terborg, & S. J. Wright. A. J. Begazo, G. Sedaghatkish, & F. Olmos 1993. The phenology of tropical forest: adapta- (eds.). The Cracidae: Their biology and conser- tive significance and consequences for primary vation. Hancock House Publishers Ltd., Surrey, consumers. Annu. Rev. Ecol. Syst. 24: 353–377. British Columbia, and Blaine, Washington. Wheelwright, N., W. A. Haber, K. G. Murray, & C.
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