The Feeding Ecology and Digestive Tract Morphometry of Two Sympatric Tinamous of the High Plateau of the Bolivian Andes: The

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ORNITOLOGIA NEOTROPICAL 14: 173–194, 2003 © The Neotropical Ornithological Society

THE FEEDING ECOLOGY AND DIGESTIVE TRACT MORPHOMETRY OF TWO SYMPATRIC TINAMOUS OF THE HIGH PLATEAU OF THE BOLIVIAN ANDES: THE ORNATE TINAMOU (NOTHOPROCTA ORNATA) AND THE DARWIN’S NOTHURA (NOTHURA DARWINII)

Álvaro Garitano-Zavala1, Jacint Nadal2 & Pamela Ávila1

1Instituto de Ecología, Unidad de Zoología (Colección Boliviana de Fauna), Universidad Mayor de San Andrés, P.O. Box 10077, La Paz, Bolivia. E-mail: [email protected] 2Departamento de Biología Animal, Facultad de Biología, Universidad de Barcelona, Av. Diagonal 645, E-08028 Barcelona, España. E-mail: [email protected]

Resumen. – Ecología alimentaria y morfometría del tracto digestivo de dos tinamúes simpátricos del altiplano de los Andes bolivianos: el Tinamú Pisacca (Nothoprocta ornata) y el Tinamú de Darwin (Nothura darwinii). – Estudiamos la amplitud de nicho trófico y el grado de solapamiento en la dieta invernal de dos especies simpátricas de tinamúes del altiplano boliviano, el Tinamú Pisacca (Nothoprocta ornata) y el Tinamú de Darwin (Nothura darwinii), analizando los contenidos de buches y mollejas de anima- les coleccionados por cazadores deportivos. También determinamos el grado de solapamiento en el uso invernal de los hábitats de forrajeo, y las diferencias en proporción de cada componente del tracto digestivo que puede implicar diferencias en la asimilación de los alimentos. Ambas especies consumen un amplio espectro de alimentos, preferentemente semillas y frutos monoseminados. El Tinamú de Darwin tiene una amplitud de nicho alimenticio mayor que el Tinamú Pisacca, pero el consumo de alimento es independiente de la especie y del sexo, lo cual es confirmado por un alto grado de solapamiento interespe- cífico. En cuanto al consumo en peso, hemos determinado diferencia interespecífica significativa sola- mente para un item (Trifolium spp). Existe un alto grado de solapamiento en el uso de hábitats de forrajeo, y no existe ninguna diferencia interespecífica en la proporción relativa de los componentes del tracto digestivo. Nuestros resultados indican que las poblaciones del Tinamú Pisacca y del Tinamú de Darwin en el altiplano boliviano muestran un bajo nivel de especialización trófica en su dieta invernal. Queda por res- ponder si el generalismo y oportunismo son estrategias adaptativas de los tinamúes para explotar su nicho alimenticio o si son el reflejo de una restricción filogenética debida a sus particulares características craneo- cinéticas. Abstract. – We studied the trophic niche breadth and the degree of overlap in the winter diets of two sympatric species of tinamous in the Bolivian Andes, the Ornate Tinamou (Nothoprocta ornata) and the Darwin’s Nothura (Nothura darwinii), by analyzing crop and gizzard contents of birds collected by sport hunters. We also measured the overlap in the winter use of foraging habitats, and the proportion of differences between digestive tract components that could imply distinct assimilation of food resources. The Ornate Tinamou and the Darwin’s Nothura consume a wide variety of food items, especially seeds and monoseminated fruits. The former has a greater niche breadth than the latter, but consumption of food items is species and sex independent, which is confirmed by high interspecific diet overlap. There was a significant interspecific difference in the amount of food consumed for only one item (Trifolium spp). There was high overlap in the use of foraging habitats, and no interspecific difference in the relative proportion of the components of the digestive tract. Our results indicate that the populations of the Ornate Tinamou and

173 GARITANO-ZAVALA ET AL. the Darwin’s Nothura in the Bolivian highlands show low degree of trophic specialization in their winter diet. However, it is not clear whether generalism and opportunism are adaptive strategies that allow the tinamous to exploit their alimentary niche, or rather indications of phylogenetic restrictions related to the cranial kinesis of tinamous. Accepted 27 August 2002. Key words: Bolivian Andes, Darwin’s Nothura, feeding ecology, intestinal morphometry, Nothoprocta ornata, Nothura darwinii, Ornate Tinamou.

INTRODUCTION components of their digestive tracts.

Tinamous (Aves: Tinamiformes) are poorly METHODS known Neotropical birds, and few ecological studies have been carried out on the Ornate Specimen collection. All specimens were obtained Tinamou (Nothoprocta ornata ornata) and the from sport hunters (helped by pointer dogs) Darwin’s Nothura (Nothura darwinii agassizii), between 1995 and 1998. Specimens were col- two sympatric species which inhabit agrosys- lected between the end of May and the end of tems in the Bolivian Andes (Pearson & Pear- October, i.e., during the dry season (southern son 1955, Bump & Bump 1969, Mosa 1997, winter) of the Bolivian highlands. Birds were 2000; Garitano-Zavala 2000). This study obtained between 10:45 and 17:25, most cap- examines trophic degree of generalism and tures occurring from 13:00 to 16:30. The col- opportunism, diet overlap and use of foraging lection sites ranged from 16º12 'S to 17º04 'S habitat in these two species. These ecological (Fig. 1). Although these latitudes differ by parameters were chosen because they are almost 1°, we assumed that this parameter indications of trophic niche specialization. does not affect results because of the random This study deals with diet breadth specializa- distribution of collections. tion or relative polyphagy, and relative plastic- ity (Sherry 1990). Breath and overlap of feeding niches. The contents Differentiation in the relative proportion of 40 crops and gizzards (ten crops and giz- of the components of the digestive tract may zards per sex of the two species) were ana- indicate a corresponding differentiation in the lyzed quantitatively to characterize winter assimilation of food resources. The few stud- diets. Ten individuals per sex was considered ies on the morphology and morphometry of enough to characterize the diet of a species at the digestive tract in other tinamous species a particular time of year (Rosenberg & Coo- (Chikilián & Bee de Speroni 1989, 1996; Mor- per 1990). In diet studies based on gastric ato & Bohórquez 1994) have shown that the contents, it is desirable to control the follow- digestive tracts do not have particular ing factors: origin of the animals, habitat het- morphological adaptations at the macro- erogeneity, time of day, weather on collection scopic level. Chikilián & Bee de Speroni day and foraging activity (Rosenberg & Coo- (1996) reported a relative intra- and inter-spe- per 1990). We did not record these factors cific homogeneity in the organization of because of our dependence on the hunters. the tract, with slight variations in morphome- Crops and gizzards were emptied and the try and mucous surface. Therefore, this contents were preserved separately in Petri study also aims to determine whether capsules with 70% ethanol to separate and the Ornate Tinamou and the Darwin’s identify all the food items by means of a stere- Nothura differ in some morphological omicroscope. Quantitative analysis was car-

174 FEEDING ECOLOGY OF ANDEAN TINAMOUS

FIG. 1. Study sites in the northern Bolivian highlands. Circles: localities for habitat, diet and morphometric studies; triangles: localities for habitat and morphometric studies; squares: localities for morphometric study only. ried out only on crop contents because they of the rapid dehydration allowed by ethanol. provide less biased results, since gizzard con- The dry weight of each item was measured tents were already digested; therefore they with an accuracy of 0.0001 g in an electronic were used only to complete the qualitative semi-microbalance (Sartorius® Research reports. Each item type was oven-dried at R160P). Arthropods and fragments were 40ºC to constant dry weight, taking advantage weighed as a whole. In the category of

175 GARITANO-ZAVALA ET AL.

FIG. 2. Direct and indirect field observations of the altitudinal distribution of Ornate Tinamous and Dar- win’s Nothuras in the northern Bolivian highlands.

“others” we included all vegetable items that tables, considering P < 0.05 to be significant. weighed less than 0.005 g. Thus, the total dry This test was preferred over the statistical G weight of the content of each crop included (Log-likelihood ratio) because some cells pre- the dry weights of all the food items, the min- sented an absolute value of the difference eral material, and the unidentified vegetable between the expected and observed frequen- material, plus detritus ingested with the food. cies that was greater than the expected fre- Feeding niche breadth is expressed by the quency (Williams 1976). When any of the richness of food items consumed, and by expected frequencies of an item was smaller Levins’ (1968) index of dietary diversity, using than five, a value that can affect the results of the relative biomass of each item. The fre- the test by rejecting the null hypothesis with a quency of each food item was determined as probability greater than α (Zar 1999), this the number of given items per crop and giz- item was not analyzed because no criterion of zard divided by the total number of birds of combination of cells reflected the true rate of each sex and species. We also considered food consumption of each food item. Therefore items that, owing to their scarcity, could not the test was carried out only with the most be quantified in dry weight. The feeding niche frequent food items. overlap was evaluated using Pianka’s (1973) Dry weight proportion was obtained for index over the relative frequency of each food each item in relation to the total weight of item. The dependence or independence of each crop content. To determine the interspe- the consumption of food items was deter- cific difference of consumption, the dry mined for each species and sex within each weight proportions of items that presented a taxon by a chi-square test in contingency frequency of at least two repetitions per

176 FEEDING ECOLOGY OF ANDEAN TINAMOUS tinamous species were compared with the 1998), in a total of 18 localities (Fig. 1). The Kolmogorov-Smirnov statistic with Lilliefors observational effort in each physiographic significance level at 0.05. These comparisons unit and habitat was homogenized by count- were not carried out between sexes because of ing the observation hours in each of the habi- the low number of repetitions. All statistical tat types in any one locality. In each of the 21 analyses were done with SPSS 10.01 for Win- habitats, a total of 32 hours were devoted to dows (SPSS 1999). observation. The hunting excursions in the final year of this study (1998) allowed us to Overlap in feeding habitat use. The secretive hab- complete the number of hours in those habi- its of tinamous do not allow direct observa- tats in which this number had not been tions of their feeding behavior. The degree of reached in preceding years. In this study, we interspecific overlap in the use of foraging assumed that the high number of observation habitats can be quantified by the frequency of hours in each habitat reduced the effect of Ornate Tinamous and Darwin’s Nothuras in locality, latitude, hour and date. distinct habitat types, assuming that feeding is The degree of overlap in habitat use was their main winter activity during the day. determined using the overlap index of Pianka Quantification was carried out according (1973), considering the 10 altitude ranges, to both direct observations and indirect sig- each of 50 meters, and the 21 habitat types in nals. Observations were recognition of a) the four physiographic units. young or adult individuals taking off with “explosive flight”, or when observed feeding Morphometric differences in the gastrointestinal tract. or running, b) vocalizations, and c) excre- To remove the effect of individual size (which ments, tracks, feathers and feeding remains, also implies the elimination of the sex factor) which were taken only when identification of on the morphometric parameters of the gas- the species was not doubtful. trointestinal tract, external measurements of Habitats were assigned to four altitude 69 Ornate Tinamous (27 males and 42 categories, corresponding to physiographic females) and 36 Darwin’s Nothuras (23 males units, as follow: alluvial plain area (between and 13 females) were obtained. The birds local basal level to 3820 m a.s.l.), piedmont were obtained from sport hunters (helped by area (between 3820 to 3850 m a.s.l.), hill area pointer dogs) in 20 localities (Fig. 1). It was (between 3850 to 3950 m a.s.l.), and mountain not possible to control hunting date and local- area (between 3950 to 4200 m a.s.l.). This ity, nor the number of specimens. The maxi- classification was previously used by Gari- mum latitudinal variation among localities was tano-Zavala (1995) to characterize tinamous 1º34’, greater than in the diet study, and birds habitats. In each unit, habitats were classified were obtained between 3850 and 4200 m a.s.l. as: rocky areas, dense shrubs, open shrubs, All birds were obtained during the southern bush areas, fallow and cultivated fields. Not all winter, between May and October, except for these habitats are present in all the physio- three individuals killed in summer. Here we graphic units; therefore, the habitat factor was assumed that locality, altitude, and the date of considered at 21 levels only. To determine the hunting did not exert a significant influence relative preference regarding altitude, altitude on morphological variation. ranges were considered every 50 m (Fig. 2). Ten external morphometric variables were Observations were carried out in all the considered: body weight (measured immedi- hunting excursions during the non-reproduc- ately after death, with a manual Pesola with tive season (southern winters of 1996 at 0.1 g accuracy), flat and stretched wing length,

177 GARITANO-ZAVALA ET AL. bill length from the inflection point of the bill trointestinal tract were obtained from 14 male with the skull, head diameter at the level of and 16 female Ornate Tinamous, and 16 male the posterior orbital border, bill height at the and 20 female Darwin’s Nothuras, all adults. level of the divergence point of the ram- Viscera were extracted on the first or second phothecal basal pieces, tarsus length, tarsus day after death and conserved in 70% etha- width, medium toe length, medium toe width nol. The following measurements were taken: and claw length. All measurements were total length of esophagus (including the cervi- obtained for all the individuals, except those cal and thoracic portions), length of proven- affected by fractures or other injuries caused triculus from the beginning of their by the shot-gut bullets, impact with the broadening until the gastric isthmus, maxi- ground, or the teeth of dogs. All measure- mum diameter of proventriculus, length, ments were performed with an accuracy of height and width of gizzard, sum of the maxi- 0.1 mm, except for the flat and stretched wing mum width of the caudodorsal and cranio- length (0.1 cm, with ruler). Body length, ventral gizzard walls in sagittal plane, intestine which is a widely used variable in ornithologi- length from the beginning of duodenum to cal studies, is a soft measurement in the case the intersection with the ceca, the sum of the of tinamous and has little reliability because length of both ceca, and the rectum plus clo- the hair-like tail feathers do not have a aca length from the intersection with ceca defined edge. The skins of the individuals until the cloacal opening. Proventriculus and studied are deposited in the Colección Bolivi- gizzard measurements were obtained to 0.1 ana de Fauna of La Paz City (Bolivia). mm accuracy, while the others were made The measurements of external morphom- with a ruler with 0.1 cm accuracy; esophageal etry were used to select the variable that could and intestinal diameters were not measured be used to correct the measurements of mor- because they are highly modified by the con- phologic variation of the digestive tract tents of the gastrointestinal tract. In some between sexes and species. The effect of spe- individuals, we did not take measurements of cies size is evident, and it was therefore the digestive tract components because they unnecessary to carry out statistical tests for had been destroyed by the shot-gun bullets or this parameter. On average, the Ornate the teeth of dogs. Results are expressed as Tinamou doubles the weight (513.86 ± 69.27 means ± SD. g, n = 70) of the Darwin’s Nothura (233.73 ± To determine the differences in the rela- 32.41 g, n = 37) (values are means ± SD). tive proportion of each digestive tract compo- Determination of significant differences nent between the two tinamous species, the in the external morphometric variables effect of individual size was eliminated by between the sexes of each species was carried means a linear regression index among the out by means of a t-test, at P < 0.05. transformed log10 of total bird weight (g) and Although the Ornate Tinamou and the Dar- the transformed log10 value of each gas- win’s Nothura are phylogenetically related, it trointestinal variable (mm). The residuals was not necessary to carry out corrections (deviations) of the allometric regressions were with phylogenetically independent contrasts retained to determine the morphometric dif- (PICs) to eliminate the effect of differential ferences between species with an analysis of phylogenetic relationships between taxa, variance (ANOVA) at P < 0.05. The use of because we studied only two species (Felsen- the residuals of the allometric regressions stein 1985). implies the correction of each measurement The morphometric variables of the gas- for the effect of individual size.

178 FEEDING ECOLOGY OF ANDEAN TINAMOUS

RESULTS Feeding niche breath and overlap. Of the 81 food items identified, 60 were present in Ornate Diet. A total of 81 food items were found in Tinamous and 67 in Darwin’s Nothuras; thus the two tinamous species, among which vege- the latter showed a slightly wider diet. The table material prevailed with 69 species of indexes of niche breadth confirmed greater seeds and monoseminated fruits, five leave niche breadth in Darwin’s Nothuras (6.65 vs. types, four flower types or parts of them, and 3.06 for Ornate Tinamous). one tuber. Moreover, mouse excrements and Only 46 food items were consumed by whole animal material (contained in a single both species. However, the 35 articles eaten article) were present; the latter was composed by only one tinamou species were rather almost entirely of insects in immature or casual because the majority appeared only imaginal phases, and occasionally spiders, once, and the others never more than three chilopoda and acari. Animal material had a times (Table 1). In contrast, only few items low mean proportion in weight in the crops: were detected frequently. In Ornate 1.4 ± 2.6% (n = 6) for Ornate Tinamou, and Tinamous, only six food items were present in 2.5 ± 3.7% (n = 13) for Darwin’s Nothura half or more of the crops of both sexes (Trifo- (Table 1). This observation allowed us to lium, arthropodes, Erodium cicutarium, Hordeum group material of animal origin into a single vulgare, Bromus and Tagetes sp. 1). In Darwin’s article. Nothuras, 10 items were eaten more fre- Most of vegetable items were identified at quently (Trifolium, arthropodes, Erodium cicu- genus level only, and some may account for tarium, mouse excrements, Tarassa tenella, more than one species that cannot be discrim- Relbunium, Agrostis sp. 1, Festuca, E. cicutarium inated by the characteristics of the seeds, i.e., and Paspalum pygmaeum). the genera Trifolium, Relbunium and Azorella. The chi-square test on all food items dem- We were unable to identify 17 articles to onstrates consumption independence 2 genus level. between the two tinamous (χ 80 = 84.50, P = Plant material comprised species of annual 0.34). However, this analysis contains 77% of herbs belonging to 18 angiosperm families. cells with expected frequencies less than five, The most diverse families were, in diminish- and although the null hypothesis was ing order, Poaceae, Asteraceae and Fabaceae. accepted, the same analysis was carried out Of the 79 vegetable items, 75 were weeds with the 17 most frequent food items (to from cultivated and fallow fields, and four avoid the contingency table showing cells with were from cultivated species (Table 1). expected frequencies less than five). The anal- The food of animal origin was composed ysis demonstrates the lack of a significant dif- of a great diversity of arthropod species, par- ference in the consumption frequency of the 2 ticularly insects which were not separated tax- most frequent food items (χ 16 = 15.16, P = onomically to avoid lowering the relative 0.51). frequencies and weights in crops. The orders With respect to the consumption of the found were, in diminishing order, Coleoptera food items that differentiated the sexes, 100% (juveniles and adults, mainly Curculionidae of male and female Darwin’s Nothuras con- and Carabidae), Hymenoptera (juveniles and sumed Trifolium and insects while, in Ornate adults, mainly Formicidae), Hemiptera Tinamous, 100% of females vs 60% males (nymphs and adults), Homoptera (adults), consumed this seed. Trifolium is the food item Lepidoptera (caterpillars) and Diptera (adults most frequently consumed by the tinamous of and juveniles). the Bolivian highlands. No statis-tically signif-

179 GARITANO-ZAVALA ET AL. a 0 0 0 % Nc Nc Nc Nc Nc Nc Nc 2.0 (1) 0.3 (1) 0.6 (1) namous and 16.6 (1) i 7.4 ± 8.5 (7) 7.4 ± 0.2 (2) 0.5 ± 0.4 (3) 1.1 34.0 ± 47.0 (2) 34.0 ± 34.4 (6) 42.0 ± 40.3 (4) 22.7 Mean ± SD (n) a Item weight Item 0 0 0 0.03 (1) 0.28 (1) 0.01 (1) 0.02 (1) < 0.005 < 0.005 < 0.005 < 0.005 < 0.005 < 0.005 < 0.005 Weight (g) 0.02 ± 0 (3) 0.56 ± 0.77(2) 0.23 ± 0.30(7) 2.42 ± 3.07(6) 0.01 ± (2) 0.15 ± 0.20(4) Mean ± SD (n) Darwin’s Nothura Darwin’s 0/0 0/0 0/0 Total 1/0.4 2/0.7 1/0.4 2/0.7 2/0.7 1/0.4 1/0.4 6/2.2 1/0.4 6/2.2 4/1.4 9/3.2 3/1.1 10/3.6 10/3.6 10/3.6 10/3.6 0/0 0/0 0/0 0/0 0/0 0/0 0/0 1/0.8 1/0.8 1/0.8 1/0.8 3/2.5 1/0.8 5/4.1 4/3.3 2/1.6 1/0.8 4/3.3 3/2.5 2/1.6 Female Item occurrence Item 0/0 0/0 0/0 0/0 0/0 Male 1/0.6 2/1.3 1/0.6 1/0.6 7/4.5 1/0.6 5/3.2 1/0.6 5/3.2 6/3.8 4/2.5 3/1.9 5/3.2 7/4.5 1/0.6 Occurrence/Occurrence % 0 0 0 ges of each food item present in the winter diet of Ornate of T diet winter the in present item food each ges of % Nc Nc Nc Nc Nc Nc Nc Nc 1.7 (1) 0.1 (1) 1.7 (1) 4.5 ± 5.0 (2) 4.5 ± 4.0 (2) 4.2 ± 4.0 (3) 5.4 ± 9.9 (2) 8.3 17.2 ± 24.1 (8) 17.2 ± 34.2 (9) 68.9 Mean ± SD (n) Item weitht 0 0 0 0.01 (1) 0.01 (1) 0.03 (1) < 0.005 < 0.005 < 0.005 < 0.005 < 0.005 < 0.005 < 0.005 < 0.005 Weight (g) 1.14 ± 2.21 (8) 0.02 ± 0.01 (2) 0.08 ± 0.04 (2) 5.33 ± 4.27 (9) 0.22 ± 0.15 (3) 0.04 ± 0.02 (2) Mean± SD (n) Ornate Tinamou 0/0 0/0 0/0 0/0 Total 3/1.2 1/0.4 1/0.4 1/0.4 4/1.6 3/1.2 8/3.3 3/1.2 2/2.0 5/2.0 6/2.4 2/0.8 1/0.4 5/2.0 11/4.5 12/4.9 0/0 0/0 0/0 0/0 0/0 0/0 0/0 1/0.8 3/2.5 5/4.1 1/0.8 4/3.3 7/5.8 1/0.8 1/0.8 4/3.3 3/2.5 1/0.8 1/0.8 1/0.8 Female Item occurrence 0/0 0/0 0/0 0/0 0/0 Male 2/1.6 1/0.8 1/0.8 1/0.8 1/0.8 6/4.8 2/1.6 4/3.2 5/4.0 2/1.6 1/0.8 1/0.8 3/2.4 1/0.8 4/3.2 Occurrence/Occurrence % Occurrence/Occurrence from the Bolivian highlands. Sex discriminationfrom the Bolivian highlands. is presented only for item occurrence.

* Occurrence, occurrence percentage, means percenta weight and weight sp. 1 sp.

sp. 2 sp. 3 sp. sp. 1 sp. 2 sp. Cyperaceae sp. 1 Cyperaceae sp. 2 Ciperaceae sp. Eleocharis Sisyrinchium 1 sp. Gramineae 2 sp. Gramineae 3 sp. Gramineae Agrostis Agrostis Bromus Eragrostis Festuca vulgareHordeum Nassella Nassella Nassella pygmaeum Paspalum Piptochaetium Sporobolus indicus ichu Stipa Food items Food SEED & FRUITS Cyperaceae Iridaceae Gramineae TABLE 1. Nothuras Darwin’s

180 FEEDING ECOLOGY OF ANDEAN TINAMOUS 0 Nc Nc Nc Nc Nc Nc Nc Nc Nc 0.7 (1) 0.7 (1) 5.2 (1) 4.2 (1) 1.9 (1) 0.7 0.8 ± 0.8 (2) ± 0.8 0.8 (2) ± 1.5 3.6 (2) ± 0.6 0.9 (2) ± 0.4 1.2 (6) ± 6.1 3.9 10.1 ± 18.6 (5) 0 ± SD (n)± SD (n) ± Mean 0.02 (1) 0.02 (1) 0.17 (1) 0.13 (1) 0.06 (1) 0.02 < 0.005 < 0.005 < 0.005 < 0.005 < 0.005 < 0.005 < 0.005 < 0.005 < 0.005 0.01 ± 0.01 (2)0.01 ± 0.08 (2)0.10 ± 0.02 (2)0.05 ± 0.01 (2)0.02 ± 0.18 (6)0.14 ± 0.38 (5)0.26 0/0 3/1.1 1/1.1 1/0.4 1/0.4 1/0.4 6/2.2 6/2.2 1/0.4 3/1.1 1/0.4 2/0.7 1/0.4 3/1.1 8/2.9 1/0.4 1/0.4 5/1.8 1/0.4 1/0.4 1 / 0.4 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 1/0.8 1/0.8 1/0.8 4/3.3 2/1.6 1/0.8 1/0.8 1/0.8 2/1.6 5/4.1 3/2.5 0/0 0/0 0/0 0/0 2/1.3 2/1.3 1/0.6 1/0.6 2/1.3 4/2.5 1/0.6 2/1.3 1/0.6 2/1.3 1/0.6 3/1.9 1/0.6 1/0.6 2/1.3 1/0.6 1/0.6 (n) Male Female Total Mean 0 0 0 0 0 0 0 0 0 0 0 Nc Nc 9.1 (1) 9.1 (1) 5.6 (1) 0.1 0.5 ± 0.2 (2) ± 0.2 0.5 (4) ± 0.4 0.5 (4) ± 3.0 3.0 (6) ± 9.1 5.1 22.2 ± 3.0 (4) 0 0 0 0 0 0 0 0 0 0 0 0.34 (1) 0.63 (1) 0.01 (1) < 0.005 < 0.005 0.03 ± 0.01 (2) 0.04 ± 0.03 (4) 0.14 ± 0.21 (4) 0.09 ± 0.07 (4) 0.21 ± 0.31 (6) Ornate Tinamou Nothura Darwin’s 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 6/2.4 2/0.8 9/3.7 1/0.4 5/2.0 2/0.8 6/2.4 1/0.4 4/1.6 11/4.5 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 3/2.5 6/5.0 1/0.8 2/1.7 3/2.5 5/4.1 1/0.8 1/0.8 Item occurrence Item weitht Item occurrence Item weight 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 3/2.4 2/1.6 3/2.4 3/2.4 2/1.6 3/2.4 6/4.8 3/2.4 Occurrence/Occurrence %Occurrence/Occurrence (g) Weight % % Occurrence/Occurrence (g) Weight % sp. 1 sp. sp. 1 sp. sp. 2 sp. Continuation. Continuation. sp. 1 sp.

sp. 1 sp. sp. 1 sp. sp. 2 sp. Bidens andicola Bidens Bidens Chuquiraga Cotula Eupatorium Heterosperma nana Hymenoxys Hypochoeris Schkuhria multiflora Sigesbeckia Stevia Tagetes Tagetes Cruciferae Lepidium Amaranthus Azorella Daucus montanus Compositae Baccharis Baccharis ompositae Cruciferae Amaranthaceae Umbellifera C Food itemsFood Male Female Total Mean(n)± SD Mean ± SD TABLE 1.

181 GARITANO-ZAVALA ET AL. 0 0 Nc Nc Nc Nc 1.5 (1) 2.0 (1) 0.4 (1) 0.2 (1) 6.9 ± 6.4 (3) 6.9 ± 1.3 (2) 1.5 46.3 ± 43.0 (5) 46.3 46.4 ± 60.6 (2) 46.4 ± 18.8 (9) 18.3 ± 18.7 (6) 12.7 31.1 ± 27.2 (14)31.1 0 0 0.05 (1) 0.07 (1) 0.01 (1) 0.01 (1) < 0.005 < 0.005 < 0.005 < 0.005 0.29 ± 0.23(3) 1.16 ± 1.26(2) 0.57 ± 0.78(5) 0.98 ± 1.35(9) 0.36 ± 0.56(6) 0.04 ± 0.05(2) 1.08 ± 1.01 (14) 1.08 0/0 0/0 2/0.7 7/2.5 2/0.7 2/0.7 1/0.4 1/0.4 1/0.4 7/2.5 1/0.4 2/0.7 1/0.4 20/7.2 14/5.0 12/4.3 12/4.3 0/0 0/0 0/0 0/0 0/0 1/0.8 1/0.8 1/0.8 1/0.8 1/0.8 4/3.3 6/4.9 3/2.5 1/0.8 1/0.8 7/5.7 10/8.2 0/0 0/0 0/0 0/0 1/0.6 6/3.8 1/0.6 1/0.6 1/0.6 1/0.6 3/1.9 1/0.6 8/5.1 9/5.7 1/0.6 5/3.2 10/6.4 (n) Male Female Total Mean ± SD (n) Mean ± SD (n) 0 0 0 Nc Nc Nc Nc 0.1 (1) 0.1 (1) 3.3 (1) 3.6 (1) 81.0 (1) 19.0 (1) 2.6 ± 3.0 (2) 2.6 18.4 ± 24.0 (7) 18.4 ± 17.7 (7) 14.4 12.5 ± 20.0 (12)12.5 0 0 0 0.38 (1) 0.01 (1) 0.01 (1) 0.51 (1) 0.12 (1) 0.25 (1) < 0.005 < 0.005 < 0.005 < 0.005 0.27 ± 0.47 (7) 0.32 ± 0.35 (7) 0.28 ± 0.36 (2) 0.43 ± 0.68 (12) Ornate Tinamou Nothura Darwin’s 0/0 0/0 0/0 2/0.8 3/1.2 1/0.4 1/0.4 1/0.4 1/0.4 3/1.2 3/1.2 1/0.4 9/3.7 1/0.4 7/2.8 16/6.5 12/4.9 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 2/1.7 1/0.8 1/0.8 1/0.8 3/2.5 6/5.0 2/1.7 3/2.5 10/8.3 Item occurrence Item weitht Item occurrence Item weight 0/0 0/0 0/0 0/0 0/0 0/0 2/1.6 1/0.8 1/0.8 1/0.8 2/1.6 6/4.8 1/0.8 6/4.8 7/5.6 1/0.8 4/3.2 Occurrence/Occurrence % (g) Weight % Occurrence/Occurrence % (g) Weight % sp. 1 sp. Continuation. Continuation.

Paronychia Atriplex * Chenopodium quinoa Chenopodium Dichondra seriacea Dichondra Chamaesyce Adesmia Astragalus Lupinus Medicago Trifolium * Vicia faba Erodium cicutarium Tarassa tenella Urocarpidium Portulaca Relbunium Food itemsFood Caryophyllaceae Chenopodiaceae Male Female Total± SD (n) Mean SD ± Mean Convolvulaceae Euphorbiaceae Leguminosae Geraniaceae Malvaceae Portulacaceae Rubiaceae TABLE 1.

182 FEEDING ECOLOGY OF ANDEAN TINAMOUS 0 0 0 0 0 0 0 0 Nc Nc Nc Nc Nc Nc Nc Nc Nc 1.0 (1) 12.2 (1) 1.4 ± 1.6 (2) 1.4 ± 1.1 (3) 1.0 0 0 0 0 0 0 0 0 0.02 (1) 0.65 (1) < 0.005 < 0.005 < 0.005 < 0.005 < 0.005 < 0.005 < 0.005 < 0.005 < 0.005 0.04 ± 0.03(2) 0.03 ± 0.04(3) 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 4/1.4 1/0.4 1/0.4 1/0.4 1/0.4 3/1.1 1/0.4 3/1.1 1/0.4 5/1.8 4/1.4 4/1.4 2/0.7 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 1/0.8 1/0.8 1/0.8 2/1.6 1/0.8 2/1.6 1/0.8 3/2.5 2/1.6 1/0.8 2/1.6 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 3/1.9 1/0.6 1/0.6 1/0.6 1/0.6 2/1.3 2/1.3 3/1.9 (n) Male Female Total Mean ± SD (n) Mean ± SD (n) 0 0 0 Nc Nc Nc Nc Nc Nc Nc 0.4 (1) 0.6 (1) 0.2 (1) 7.0 (1) 0.3 (1) 0.2 (1) 72.2 (1) 0.9 ± 1.1 (3) 0.9 ± 2.4 (2) 3.1 18.9 ± 26.3 (2) 18.9 ± 17.0 (7) 14.7 0 0 0 0.04 (1) 0.01 (1) 0.31 (1) 0.01 (1) 0.05 (1) 0.01 (1) 0.02 (1) < 0.005 < 0.005 < 0.005 < 0.005 < 0.005 < 0.005 < 0.005 0.10 ± 0.14 (3) 0.31 ± 0.02 (2) 1.28 ± 1.80 (2) 0.69 ± 0.63 (7) Ornate Tinamou Nothura Darwin’s 0/0 0/0 0/0 2/0.8 3/1.2 1/0.4 2/0.8 2/0.8 1/0.4 1/0.4 1/0.4 2/0.8 5/2.0 1/0.4 3/1.2 1/0.4 6/2.4 3/1.2 7/2.8 2/0.8 8/3.3 0/0 0/0 0/0 0/0 0/0 0/0 0/0 1/0.8 2/1.7 1/0.8 2/1.7 1/0.8 1/0.8 2/1.7 3/2.5 1/0.8 1/0.8 5/4.1 1/0.8 2/1.7 3/2.5 Item occurrence Item weitht Item occurrence Item weight 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 1/0.8 1/0.8 1/0.8 1/0.8 1/0.8 2/1.6 1/0.8 2/1.6 1/0.8 2/1.6 5/4.0 2/1.6 5/4.0 Occurrence/Occurrence % (g) Weight % Occurrence/Occurrence % (g) Weight % Compositae

Trifolium Trifolium B. incarum B. incarum L. pinnata Continuation. Continuation.

Indeterminate 1 Indeterminate 2 Indeterminate 3 Indeterminate 4 Indeterminate 5 Indeterminate 6 Indeterminate 7 Indeterminate 8 Indeterminate 9 Indeterminate 10 Indeterminate 11 Gramineae of Anthers of Leaves Flowers of Flowers Buds of Compositae of GeraniaceaeFlowers of Leaves of Leaves 1 Longs Leaves 2 SucculentsLeaves Solanum tuberosum* Food itemsFood Indeterminates Male Female Total± SD (n) Mean SD ± Mean PARTS VEG. OTHER TUBERS Solanaceae TABLE 1.

183 GARITANO-ZAVALA ET AL. 2.4 ± 2.2 (9) 2.4 ± 1.5 (5) 2.0 2.5 ± 3.7 (13) 1.1 ± 0.7 (19) 7.3 ± 6.2 (20) ated (Nc). (Nc). ated 0.08 ± 0.10(9) 0.05 ± (5) 0.06 ± 0.09 (13) 0.06 ± 0.02 (19) 0.03 ± 0.29 (20) 0.23 14/5.0 20/7.2 7/5.7 10/8.2 7/4.5 10/6.4 (n) Male Female Total Mean ± SD (n) Mean ± SD (n) 1.5 ± 1.5 (5) 1.5 ± 2.6 (6) 1.4 ± 0.8 (8) 1.1 2.2 ± 3.2 (17) 11.9 ± 14.3 (19)11.9 0.05 ± 0.05 (5) 0.07 ± 0.10 (6) 0.09 ± 0.08 (8) 0.03 ± 0.04 (17) 0.24 ± 0.19 (19) Ornate Tinamou Nothura Darwin’s 7/2.8 12/4.9 it was less it was than 0.005 g in all then thethe cases, percentageweight not was calcul 4/3.3 7/5.8 Item occurrenceItem weight Item occurrence Item weight Item 3/2.4 5/4.0 Occurrence/Occurrence % (g) Weight % Occurrence/Occurrence % (g) Weight % Continuation. Continuation.

Mouse feces Mouse Arthropods Various Mineral material Detritus The not determined was weight item because Food itemsFood MISCELLANEOUS Male Female Total± SD (n) Mean SD ± Mean *Cultivated species. species. *Cultivated TABLE 1. a

184 FEEDING ECOLOGY OF ANDEAN TINAMOUS icant sexual differences were detected for the quency do not necessarily correspond to 67 articles consumed by Darwin’s Nothuras those with greatest relative proportion in 2 (χ 66 = 51.36, P = 0.91), nor for the 60 articles weight. This is due to differences in the biom- 2 consumed by Ornate Tinamous (χ 59 = 51.98, ass of each item; for example, a H. vulgare P = 0.73). grain weighs around 30 times more than that Similarly to the analysis for species, these of Trifolium. analyses produced high percentages of cells The Kolmogorov-Smirnov test demon- with expected frequencies less than five (87% strated a significant difference only for Trifo- for Darwin’s Nothuras, and 90% for Ornate lium, with a very marginal rejection value of Tinamous). Therefore, the analyses were the null hypothesis (Z = 1.36, P = 0.05). This made for the six most frequent items for each item was more consumed by Darwin’s Nothu- species. These also demonstrated indepen- ras (Table 1). The other items were consumed dence among the items consumed by each sex by both species in a weight proportion that 2 in each species (Ornate Tinamou: χ 5 = 1.37, did not differ significantly. 2 P = 0.93; Darwin’s Nothura: χ 5 = 3.24, P = 0.66). The data of relative consumption fre- Overlap of feeding habitats. For the quantitative quency of each food item show a high value study, a total of 728 direct and indirect obser- of interspecific feeding niche overlap (O = vations were recorded with certainty of spe- 0.88). cies identification: 420 for Ornate Tinamous From the 81 food items, 25 were recorded and 516 for Darwin’s Nothuras. as present only, because their individual biom- The altitudinal distribution of Ornate ass in crops was less than 0.005 g. The data Tinamous in the localities here studied was for weight and weight percentage in relation between 3830 m to 4200 m a.s.l., and most of to the total weight in crops for the remaining the observations were between 3850 to 4050 56 articles for each species are shown in Table m a.s.l. (82%). This species was more fre- 1. quently observed in the mountain and hill The weights of total crop contents of both areas (41% and 48%, respectively), but was species together ranged from 0.04 g to 14.85 g not detected in the plains (Fig. 2, Table 2). (4.22 ± 3.80 g). Darwin’s Nothuras showed The specific habitats frequented by Ornate higher values (between 0.15 g and 14.85 g), Tinamous were rocky areas, dense shrubs and but a lower average (3.87 ± 3.64 g) than bushes, but this species was also observed in Ornate Tinamous (4.58 ± 4.04 g, range open areas (including some which were between 0.04 g and 11.78 g). The crop of one almost denuded by cattle), fallow and potato Ornate Tinamou was empty. fields up to 3900 m a.s.l. (Table 2). Very few items were consumed in high Darwin’s Nothura was observed between proportion. Those with the highest average 3710 m and 4150 m a.s.l. However, it was very dry weight consumed by Ornate Tinamous rarely observed above 4000 m, and was partic- (i.e., those with an average > 1 g) were Hor- ularly frequent between 3800 and 3950 m a.s.l. deum vulgare (barley), Bromus and Leaves 2 (suc- (77%) in the piedmont and hill areas (35% culents). Those consumed by Darwin’s and 40% respectively) (Fig. 2, Table 2). This Nothuras were H. vulgare, Chenopodium quinoa species was observed more frequently in bush and Trifolium. In the latter, two of the three areas of Stipa ichu and Festuca spp. growing items are cultivated species, and of these H. between cultivated fields and houses in the vulgare was observed in both species. It should piedmont, hill and plains areas (Table 2). It be noted that the food items with greatest fre- was also observed in dense shrubs, fallow

185 GARITANO-ZAVALA ET AL. 0 (0) Total 181 (35) 67 (12.9) 48 (11.3) 64 (12.5) 199 (47.5) 204 (39.6) 173 (41.2) ands. In parenthesis In ands. l 0 (0) 0 (0) 9 (1.7) 9 (2.1) 24 (4.6) 32 (7.6) 28 (5.4) 19 (4.5) Cultivated fields Cultivated 0 (0) 31 (6) 31 8 (1.9) 17 (3.3) 46 (8.9) 34 (8.1) 22 (5.2) 14 (2.7) Fallow fields 0 (0) 6 (1.4) 27 (5.2) 37 (8.8) 33 (7.9) 19 (3.7) 52 (10.1) 54 (10.5) Bush areas 0 (0) 8 (1.6) 14 (2.7) 14 (3.3) 27 (5.2) 17 (4.1) 35 (6.8) 29 (6.9) Open shrubs 46 (11) 11 (2.6) 32 (6.2) 49 (9.5) 34 (8.1) 23 (4.5) Dense shrubsDense 0 (0) 7 (1.4) 33 (7.9) 36 (8.6) Rocky areas Ornate Tinamou Nothura Darwin’s Ornate Tinamou Nothura Darwin’s Ornate Tinamou Nothura Darwin’s Ornate Tinamou Nothura Darwin’s Alluvial plain area Alluvial plain Piedmont area Hill area Mountain area TABLE 2.Number Nothura of fieldthe inTABLE observations habitat units of the northernOrnate of Tinamou and Darwin’s high Bolivian the percentoftotal observationsspecies. for each

186 FEEDING ECOLOGY OF ANDEAN TINAMOUS P 0.001 0.010 0.539 0.018 0.586 0.551 0.771 0.960 0.007 0.724 3.82 2.74 0.62 2.48 0.55 0.60 0.29 0.05 2.86 0.36 13 13 13 13 13 13 13 13 13 13 6.50 ± 0.58 3.63 ± 0.22 3.33 ± 0.20 6.03 ± 0.54 20.41 ± 0.83 20.41 ± 0.94 18.34 ± 1.16 38.11 ± 0.85 28.70 ± 146.46 ± 4.72146.46 ± 255.9223.30 ± 23 23 21 21 21 22 21 21 21 21 Mean SD n Mean ± SD n t 6.86 ± 2.266.86 ± 0.263.65 ± 0.193.13 ± 0.596.11 ± 20.20 ± 1.08 17.68 ± 0.62 38.37 ± 1.25 28.67 ± 1.46 142.65 ± 3.56 226.13 ± 21.98 P 0.001 0.000 0.479 0.004 0.052 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 7.37 3.55 5.63 0.71 4.69 5.30 3.70 4.38 3.00 1.98 39 42 40 40 40 41 39 39 39 40 9.74 ± 0.80 4.64 ± 0.27 4.33 ± 0.35 34.78 ± 2.17 21.16 ± 1.54 51.63 ± 1.58 39.00 ± 1.97 10.15 ± 1.52 202.12 ± 13.4 552.31 ± 54.24 Ornate Tinamous Nothuras Darwin’s 26 27 25 24 25 27 26 26 26 26 ternal morphometric variables (mm) of Ornate Tinamou and Darwin’s Nothura. ternal morphometric(mm)Ornate of variables Tinamouand Darwin’s Males Females t-test Males Females t-test 8.79 ± 0.79 4.39 ± 0.28 4.05 ± 0.36 9.47 ± 1.08 31.79 ± 1.93 31.79 ± 1.45 20.88 ± 1.60 49.54 ± 1.65 36.95 ± 192.67 ± 4.12 192.67 ± 457.6944.82 ± VariablesWeight Flat wing length Bill length Head diameter height Bill Mean ± SDTarsus length n width Tarsus length toe Medium Mean ± SDMedium toe width n length Claw t TABLE 3. Student t analysis for ten ex for ten analysis t 3. Student TABLE

187 GARITANO-ZAVALA ET AL. fields and active crops where even broods regression indexes, the use of the residuals of were spotted. these regressions as morphometric values The index of habitat overlap using the corrected for individual size was considered height ranges was O = 0.75, and the corre- appropriate. sponding result for habitat category was O = The results of the ANOVAs carried out 0.70. Therefore, there was a considerable with the residuals of the linear regressions degree of overlap in the use of altitudinal shown that no component of the digestive ranges for both species, and also both species tract significantly differed between the two foraged in the same habitats in each range. species (Table 5). This finding is consistent with the fact that the two species can take off with “explosive DISCUSSION flights” from the same places. Generalism and opportunism. The presence of Alimentary tract. The statistical analyses carried only one empty crop demonstrates that the out on the morphometric measurements winter diet analysis of Darwin’s Nothuras and demonstrate high sexual dimorphism in Ornate Tinamous was a sample of daily con- Ornate Tinamous, expressed as significant sumption. The finding of 81 distinct food differences in all the variables studied, except items, without counting the arthopod taxo- head diameter and claw length of the medium nomic groups, is an indication of the wide toe (Table 3). Our results show that females trophic spectrum of these birds, which are larger than males. Darwin’s Nothuras appears larger in Darwin’s Nothuras. On the showed lower sexual dimorphism because other hand, only a low proportion of con- only four variables exhibit significant differ- sumption involved food of animal origin. Our ences. Similarly, in Darwin’s Nothuras, results characterise the Bolivian highland females were also larger (Table 3). tinamous as mainly granivorous, and occa- Weight was the only variable that showed sionally folivorous and insectivorous, at least a significant difference with P < 0.001 in both in winter. This is consistent with Dorst & species. Rising & Somers (1989) determined Vuilleumier (1986), who considered tinamous this variable to be that which best represents as large terrestrial granivorous-insectivorous bird size, a variable which is even better than birds of the tropical Andes. wing size, a favorite for many ornithologists. Practically all the studies on tinamous For this reason weight was used to correct for demonstrate wide diet spectra (Mosa 1997, the effect of size of each individual in each 2000; Jimbo 1957, Bonetto et al. 1960, Bump species by linear regression of the trans- & Bump 1969, Grigera 1973, Silva & Sander formed log10 variables. Table 4 shows the 1981, Cabot 1992). The family was qualified means for the measurements of gastrointesti- as opportunistic, with more consumption of nal variables in each sex of both species. Table food of plant origin, and less of animal origin 5 shows the parameters of the lineal regres- (Cabot 1992). sions of the same 10 measurements. All these Although the wide range of food items variables show a significant correlation with consumed indicates a generalist feeding strat- weight (P ≤ 0.001), but some regression egy, one of the most important findings of indexes denote the accumulation of less than this study is that very few articles are con- 50% of the variability, e.g., proventriculus sumed with greater frequency and abundance. diameter and intestine length. However, given This also indicates an opportunistic strategy, that most of the variables show relatively high since some of the more frequent items were

188 FEEDING ECOLOGY OF ANDEAN TINAMOUS n 11 11 11 12 12 12 12 12 12 12 Females 9.57 ± 0.88 Mean ± SD Mean ± 93.73 ± 8.00 17.88 ± 1.77 33.53 ± 1.67 29.51 ± 1.60 18.89 ± 0.85 21.50 ± 2.35 76.92 ± 5.87 547.50 ± 49.65 290.58 ± 27.90 n 13 16 16 16 16 16 16 15 16 16 Darwin’s Nothuras Darwin’s Males 8.65 ± 0.79 8.65 ± Mean ± Mean SD 90.77 ± 6.37 90.77 ± 1.30 17.59 ± 2.14 31.58 ± 1.86 27.95 ± 1.20 17.81 ± 3.01 19.79 ± 7.97 74.25 ± 516.6045.15 ± 273.9423.41 ± n 14 15 15 16 16 16 15 15 15 15 Females 9.93 ± 1.08 Mean ± Mean SD 23.53 ± 3.35 23.53 ± 2.90 40.08 ± 2.45 33.70 ± 2.04 21.49 ± 3.99 31.75 ± 9.99 84.13 ± 125.50 ±13.98 746.6090.77 ± 383.3348.55 ± n 12 14 14 14 14 14 14 14 14 14 Ornate Tinamous Males 9.72 ± 1.36 Mean ± SD Mean ± 21.88 ± 1.99 37.41 ± 2.63 31.66 ± 2.09 20.21 ± 1.44 28.60 ± 3.80 86.43 ± 7.31 118.83 ± 12.58 731.43 ± 46.44 364.00 ± 42.80 Variables Esophagus length length Proventriculus diameter Proventriculus length Gizzard heigth Gizzard width Gizzard width walls Gizzard Intestine length Ceca length length cloaca plus Rectum TABLE 4. of Descriptives TABLE ten morphometric gastrointestinal Nothura. tract of Ornatevariables Tinamou and Darwin’s

189 GARITANO-ZAVALA ET AL. cultivated grains that remained in the fields diet overlap. after reaping. Therefore, Ornate Tinamous High overlap levels in the use of food and Darwin’s Nothuras feed on reaped fields items and foraging habitats support the to take maximum advantage of these hypothesis that the Darwin’s Nothuras and resources. Similar results were reported the Ornate Tinamous are generalists and for the Red-winged Tinamou (Rhynchotus opportunists in the Bolivian highlands, at rufescens) in Brazil (Sander 1982), the Darwin’s least in winter. Mosa (2000) suggests that Nothura and Andean Tinamou (Notho- temporal variations of the niche amplitude procta pentlandii) in Argentina (Mosa 1997, and overlap degree between Darwin’s Nothu- 2000), and for the Spotted Nothura in Argen- ras and Andean Tinamous result in temporal tina (Bump & Bump 1969, Silva & Sander variations of the degree of opportunism and 1981). generalism of these species. May be, it is true Generalistic and opportunistic strategies in the Bolivian highlands and more studies are in tinamous are also evident from the fre- needed to confirm. quent consumption of foods that demon- Menegheti (1983) emphasized the mor- strate low selection capacity. This is the case phological difference among the bills of these of mouse excrements that are reported here species. The Red-winged Tinamou, like all the for Tinamiformes for the first time. Similar Nothoprocta species, has a longer, stronger and low selection capacity has been reported in more curved bill than Nothura species, imply- other studies (Bump & Bump 1969, Bohl ing the potentiality for exploiting a wider diet 1970, Mosa 1993). spectrum (including tubers, bulbs and rhi- zomes). However, Spotted Nothuras were Food resources and habitat use. Both tinamous more abundant and prospering in the Brazil- species of the Bolivian highlands showed high ian fields. Menegheti (1983) attributed this overlap in their winter qualitative use of food phenomenon to a greater synantropic degree resources and foraging habitats, and no differ- in Spotted Nothuras. Their distribution range ences were observed in the amount of increased following the substitution of natural consumed biomass of the most frequent habitats by agrosystems. Our results showed a nutritious articles, except for Trifolium. very similar situation in the Bolivian high- Although the results show high values of lands. habitat overlap, it is important to consider that there is a wide altitudinal overlap, Gastrointestinal tract. The organization of the but there are also areas which are mainly digestive tracts of Ornate Tinamous and Dar- exploited exclusively by Darwin’s Nothuras win’s Nothuras corresponds to the descrip- or by Ornate Tinamous (Fig. 2). The former tions of other tinamous (Chikilián & Bee de has a larger range, which also coincides Speroni 1989, 1996; Morato & Bohórquez with the wider diet spectrum. Mosa (2000) 1994). Intestine length and animal biomass in conclude that the overlap degree between the two species matches the most frequent Darwin’s Nothuras and Andean Tinamous norm in birds, as indicated by the relationship in Argentina depends on the station of suggested by McLelland (1979): Intestine the year: in winter, the diet and space length (cm) = 3√ Body weight (g). The ceca of overlap is greater. The study of Menegheti these species are highly developed; the cumu- (1983) with the Spotted Nothuras and lative length of both ceca is a little less than Red-winged Tinamous in Brazil demonstrates half the total length of the intestine (Table 4). a relatively low habitat overlap but a wider The ceca differ morphologically from those

190 FEEDING ECOLOGY OF ANDEAN TINAMOUS

TABLE 5. Linear regression values between the log10 of weight and the log10 of the specified measurements. The two last columns show the ANOVA results obtained between the two tinamou species with the regression residuals. n = number of cases, F1 = ANOVA Fisher’s F value for the linear regression correla- 2 tion, P1 = their corresponding probability value, r = linear regression value, F2 = ANOVA Fisher’s F for the analysis with both tinamou species using the regression residuals, P2 = their corresponding probability value.

2 Variables n F1 P1 r F2 P2 Esophagus length 50 137.17 0.000 0.74 0.04 0.840 Proventriculus length 56 81.65 0.000 0.59 0.04 0.837 Proventriculus diameter 56 12.04 0.001 0.17 0.25 0.618 Gizzard length 58 154.89 0.000 0.73 0.31 0.580 Gizzard width 58 98.42 0.000 0.63 0.73 0.396 Gizzard height 58 63.27 0.000 0.52 0.30 0.588 Gizzard walls width 57 121.67 0.000 0.68 0.04 0.833 Intestine length 56 183.50 0.000 0.77 0.17 0.679 Rectum plus cloaca length 57 28.08 0.000 0.33 0.11 0.738 Ceca length 57 114.08 0.000 0.67 0.01 0.905 of large ratites that have highly modified or ture of the gastrointestinal tract in birds is reduced ceca (Beddard 1898, McLelland highly flexible (Starck 1999), and it is possible 1979). However, they are similar to the ceca of that this can vary in time and space regardless kiwis (Beddard 1898), which can be inter- of the variations in diet. But our results sug- preted as the permanency of the most primi- gest that the lack of difference in winter diet is tive morphology in these two palaeognathous related with a lack of difference in tract mor- groups. A function of the intestinal ceca in phometry, which would support the generalis- birds deals also with water reabsorption and tic diet strategy hypothesis. fermentation of nitrogenic residuals excreted by the kidneys (Remington 1989). Thus, the Generalism and opportunism: Ecological adaptation relatively large intestinal ceca in the two or phylogenetic restrictions? Studies on specializa- tinamous species studied appears to be related tion in the exploitation of trophic niches by to the optimization of nitrogen obtained from animals have resulted in niche theories based a granivorous diet as well as to reduce water on foraging optimization, ecomorphology, expenditure in their habitats. comparative morphology, and phylogeny We did not observe large morphological (Sherry 1990). According to niche theories, differences between the gastrointestinal tract natural selection favors “effective organisms” components of Darwin’s Nothuras and that can find enough food in time and space. Ornate Tinamous. Statistically, they are mor- Therefore, models of niche theory also pre- phologically similar, given the difference in dict that a generalist and/or opportunist feed- size between sexes and species. For other ing strategy is likely to be adaptive in variable tinamous, a relative intra- and interspecific habitats (Levins 1968). homogeneity in the digestive tract organiza- In the Bolivian highlands, the inter-annual tion has also been reported, with slight mor- climatic variations, the prevalence of pioneer phometric and mucous surface variations vegetable species with unpredictable phenolo- (Chikilián & Bee de Speroni 1996). The struc- gies, and the human establishment and han-

191 GARITANO-ZAVALA ET AL. dling of agricultural practices, are three ACKNOWLEDGMENTS dimensions resulting in environmental unpredictability in time and space for the tinamous. The authors thank Ramiro López and Esther The basic adaptation expected in granivorous Valenzuela at the National Herbarium of birds would be to take advantage of the Bolivia for their collaboration with the identi- unpredictable appearance of large amounts of fication of plant material. Ernesto Hug and certain seeds by consuming them rapidly, and Oscar Aguilar, sport hunters of tinamous, by searching for other abundant food sources allowed us access to their hunted animals. (Wiens & Johnston 1977). Unpredictability Robin Rycroft and Xavier Ruíz offered useful could therefore exert an important selective comments on a draft version, R. Rycroft cor- pressure that could explain the generalism, rected the English redaction too. Álvaro Gari- opportunism and relative synanthropy, with tano-Zavala thanks to the Spanish Agency of rapid changes in the diet according to the International Cooperation for the concession habitat offer, observed in the tinamous of the of a MUTIS scholarship to complete studies Bolivian highlands. Then, the use of the ali- at the University of Barcelona (Spain). mentary niche could be interpreted as adaptive. REFERENCES However, according to Zweers et al. (1997), tinamous and ratites constitute a lin- Beddard, F. E. 1898. The structure and classifica- eage that evolved with a palaeognathous rhyn- tion of birds. Longmans, Green and Co., Lon- chokinetic skull, a primitive cranial type. don, UK. Thus, they are in the tinamou-like browsers Bohl, W. H. 1970. The study of the Crested guild that take big mouthfuls with a low level Tinamou of Argentina. US Fish Wildl. Serv. of manipulation of the food in the bill. The Spec. Sci. Rep.-Wildl. 131: 1–101. rudimentary size of the tongue increases this Bonetto, A. A., C. Pignalberi, & P. Saporito. 1960. relative cranioinertial feeding with little selec- Acerca de la alimentación de Nothura maculosa tivity, and these characteristics are probably nigroguttata (Salvadori) con especial referencia a su actividad entomofaga. Physis 22(63): 53–60. responsible for a low trophic radiation of the Bump, G., & J. W. Bump. 1969. A study of the palaeognathes (Gussekloo & Zweers 1997, Spotted Tinamous and the Pale Spotted Tomlinson 1997a, 1997b). A corollary of the Tinamous of Argentina. US Fish Wildl. Serv. hypothesis of Zweers et al. (1997) is that the Spec. Scie. Rep.-Wildl. 120: 1–160. tinamous would have an evolutionary restric- Cabot, J. 1992. Family Tinamidae (tinamous). Pp. tion that impedes specialization in the diet, 112–138 in del Hoyo, J., A. Elliot, & J. Sargatal also reflected in morphology, physiology and (eds.). Handbook of the birds of the world. behavior. Volume 1: Ostrich to ducks. Lynx Edicions, All the characters studied here show that Barcelona. Ornate Tinamous and Darwin’s Nothuras in Chikilián, M., & N. Bee de Speroni. 1989. Varia- the Bolivian highlands have a low degree of ciones morfológicas e histoquímicas del tubo digestivo de Nothura maculosa (Conover, 1950) trophic specialization. Are generalism and durante las estaciones de invierno y verano opportunism adaptive strategies in tinamous (Aves: Tinamidae). Rev. Asoc. Cienc. Nat. Lito- to exploit their alimentary niche, or are they ral 20 (1–2): 99–109. the reflection of phylogenetic restrictions? We Chikilián, M., & N. Bee de Speroni. 1996. Compar- hope that our study will result in the realiza- ative study of the digestive system of three spe- tion of more studies on the feeding biology cies of tinamou. I. Crypturellus tataupa, and ecology of tinamous. Nothoprocta cinerascens, and Nothura maculosa

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