ORNITOLOGIA NEOTROPICAL 10: 193–206, 1999 © The Neotropical Ornithological Society

COMPARATIVE LIFE HISTORY OF COTINGAS IN THE NORTHERN PERUVIAN AMAZON

Daniel M. Brooks1,4, Lucio Pando-Vasquez2 & Angel Ocmin-Petit2,3

1Department of Wildlife and Fishery Science, Texas A&M University, College Station, Texas 77843, USA. 2Explorama, Box 446, Iquitos, Peru. 3Deceased.

Abstract. We investigate sociobiology of sympatric cotingas by comparing variation of common characters. The species studied (smallest to largest) are: Iodopleura isabellae, Porphyrolaema porphyrolaema, Cotinga maynana, C. cayana, Lipaugus vociferans, Phoenicircus nigricollis, Querula purpurata, Gymnodoerus foetidus and Cephalopterus ornatus. The relationship between size and sexual dimorphism was correlated, with mass and tail length being significant, and all other characters (total length, wing chord, sexual dichromatism and ornamenta- tion) being non-significant. For mass and tail length, smaller species are characterized by females being larger than males, whereas females are smaller in the larger species. Although not significant with all spe- cies along the size gradient, sexual dichromatism is more extreme in certain smaller species (i.e., Porphyro- laema and Cotinga), and sexual ornamentation is present primarily in larger species. Dietary specialization increases with size, and most species exhibit low food resource defense intra- and interspecifically. Smaller species use higher parts of habitat structural attributes, whereas larger species use lower parts. Most of the smaller species are solitary, whereas larger species tend to travel in small flocks. Regarding courtship, smaller species are characterized by solitary male systems (including polygamy), with lekking in the medium species and/or monogamous courtship in the larger species. We offer three hypotheses (modified from Alcock’s model) as they relate to cotinga courtship strategy: 1) Solitary, dichromatic males of smaller species are attracted above the canopy because it highlights their iridescence and lures in females (cost = increased predation risk above the canopy, benefit = lower energy expenditure). 2) Actively courting males of medium species are attracted below the canopy to more aggregated fruit clumps; since bright coloring cannot be detected as well under the canopy, the males compensate through active courtship such as lek- king and/or vocalizing to lure in females (benefit = decreased predation risk below the canopy, cost = increased energy expenditure during courtship). 3) Males of larger species are lured to their courting sites by females that are attracted to the habitat containing the preferred resource; males typically court a single female using subtle ornamentation, as well as calling in some species. Accepted 24 June 1999. Key words: Cotingas, comparative sociobiology, Amazonian birds, resource distribution.

INTRODUCTION This family is characterized by extensive mor- phological and chromatic variation at the The family Cotingidae contains 25 genera and generic level. For example this family contains approximately 66 species (Stotz et al. 1996). the most variable size range of all Passerines, ______with the largest species weighing 80 times that 4Current address: Cracid Specialist Group Headquar- of the smallest (Snow 1982). Although the ters, PO Box 132038, Houston, Texas 77006, USA. primary factors (i.e., habitat separation and E-mail: [email protected] size assortment) driving cotinga community

193 BROOKS ET AL.

FIG. 1. A map of the study region. 1 = Iquitos (major city), 2 = Amazon River bank site, 3 = Yana Mono Tributary/Yana Mono Lodge, 4 = Napo River bank site, 5 = Sucusari Tributary/Camp, 6 = ACEER, 7 = Yarina Island/Rosario Island, 8 = Chimiguy Lake, 9 = Lorenzo Lake, 10 = Urco Tributary, structure in the northern Peruvian Amazon throated Cotinga Porphyrolaema porphyrolaema, have been identified (Brooks 1998), relatively Bare-necked Fruitcrow Gymnodoerus foetidus, little is known about the amount of variation Purple-throated Fruitcrow Querula purpurata, in sociobiology, particularly for cotingas living and Amazonian Umbrellabird Cephalopterus in the same region. ornatus. Although former classification (e.g., Herein we examine life history correlates Snow 1973a) included tityras and becards in of 9 species of sympatric cotingas in the this family, we follow current classification northern Peruvian Amazon comparing varia- (e.g., Stotz et al. 1996). tion among common characters. The species studied include Black-necked Red Cotinga METHODS Phoenicircus nigricollis, White-browed Purple- tuft Iodopleura isabellae, Screaming Piha Lipau- Data collection can be divided into data col- gus vociferans, Plum-throated Cotinga Cotinga lected from the field and data collected from maynana, Spangled Cotinga C. cayana, Purple- the museum. Mensural data were obtained

194 COTINGA LIFE HISTORY STRATEGY from museum specimens and other dimor- 20 m apart. Primary, interior rainforest is high phism characters (sexual dichromatism and in plant diversity, is characterized by a dark ornamentation) were obtained from both understory due to few penetrable light gaps, field and museum data. Other data including and contains tall trees that form part of the habitat association, sociality and courtship canopy, buttresses, or canopy emergents (e.g., were obtained from the field. Field data on Cedrela sp., Ceiba pentandra, Ficus insipida and feeding (limited observations) and species Inga sp.), often exceeding 35 m. Other tall with limited sample size (i.e., Phoenicircus, trees in the region include palms (e.g., Euter- Iodopleura and Porphyrolaema) were supple- pes prectoria, Mauritia flexuosa, Scheelea sp., mented with museum specimen tag data or Socratea sp.), often occupying a gradient of obtained from available literature (e.g., Wal- habitats, from river edge to interior forest. lace 1849, Von Hagen 1937, Nicéforo 1947, Sampling was done during 11 weeks from Sick 1951, 1954, 1979, 1993; Ellis 1952, Pinto November 1993 to October 1998 at the end 1953, Snow 1961, 1971, 1982, 1985; Dia- of high water (March–May) and low water mond & Terborgh 1967, Haverschmidt 1968, (October–November) seasons to account for Béraut 1970, Howe 1982, Hilty & Brown seasonal variation, that did not appear to vary 1986, Terborgh 1986, Terborgh et al. 1990, significantly (Brooks 1998). Sampling meth- Trail & Donahue 1991, Davis 1993, Ridgely ods were similar to those used previously by & Tudor 1994, Thiollay 1994, Brooks 1998). others. Habitat associations were logged for all visually or auditorily recorded encounters Field collected data. Field data were collected in of Cotingids at each site visited per trip. Data the Napo River intersect region (2°45’S; were collected by walking slowly along 72°55’W, see Fig. 1) of the Peruvian Amazon. transects with frequent stops (Pearson 1975) Habitats have been overviewed elsewhere and boating along waterways (Diamond & (e.g., Brooks 1997, 1998), but will be Terborgh 1967). Additionally supra-canopy described here briefly. The habitats sampled observations were facilitated by using the are primarily situated along water, within for- canopy walkway at ACEER (Amazonian est, or a transition/edge situation between Center for Environmental Education and these habitats. Regions along the immediate Research). Species were identified using Hilty edges of water (e.g., marshes, lakes, streams & Brown (1986) and Parker et al. (n.d.). and rivers) are often dominated by sawgrass or cane, followed by thick undergrowth fur- Museum collected data. Mensural data were col- ther inland from the water. Island edge vege- lected at the Museum of Natural Science, tation is similar, unless the island is young, in Louisiana State University on 3 October which case it will be monocultured with rap- 1996. Mass (indicative of size) was recorded idly colonizing plant species that are primary (in g) from the tags when available; standard successional island specialists (e.g., Cecropia measurements taken in cm using a metal ruler sp., Gynerium sp., and Heliconia sp.). Aquatic included total length, wing chord and tail edge vegetation is separated from interior length (indicative of size and maneuverability rainforest by dense forest with thick under- in habitat). Measurements taken in cm with growth, with canopy height often not exceed- standard dial calipers include maximum man- ing 10–15 m. The exception includes dibular height (indicative of masticator mus- floodplain, which is characterized by continu- culature – bite force) and maximum ous short stems and grasses (e.g., Tridescantia mandibular width (indicative of gape-size of sp.) and tall, leafy trees with trunks spaced 5– food taken) (Snow 1973b).

195 BROOKS ET AL.

An effort was made to measure at least throughout the study)], courtship strategy four specimens of each sex per species. In (type of courtship and number of males/dis- cases where specimens were represented by play group) and competition at feeding trees. less than four individuals of a given sex from Information on feeding strategy was Dpto. Loreto, additional specimens measured largely supplemented with the literature, and included those that were closest to the sam- species were identified as gorgers (species pling region. that sit in low bushes or mistletoe and gorge), seasonal resource specialists (species that sea- Analytical methods. Morphological life history sonally concentrates on insects or fruit) and parameters included size and sexual dimor- riverine specialists (species preferring fruits phism. Mass was used to measure size, rank- growing along river, such as palm fruits). Spe- ing the species from smallest to largest in cies habitat associations were identified based range. Sexual dimorphism was measured by upon strata of tropical forest occupied (i.e., obtaining male/female (M/F) ratios for mass, mid-upper, upper or canopy) or type of total length, tail length, and wing chord. Val- aquatic habitat occupied (i.e., varzea/water ues < 1 indicated females were larger than edge transition or island varzea). males; values >1 indicated males were larger Competition at feeding trees was exam- than females. Sexual dimorphism was also ined at two levels. The first involved different measured by examining degree of sexual scales of taxonomic orientation: whether con- dichromatism and ornamentation. Sexual specifics of the same or different sexes, other dichromatism was defined as extreme colora- cotingas, or other avian species were present tion differences where the female is more in the same tree at the same time. The second drab and was ranked as: 0 (none, for no dif- examined intraspecific competition between ferences between male and female), 1 (slight, sexes more closely by plotting M/F ratios of for subtle differences, with both sexes rela- maximum mandibular height against maxi- tively drab), 2 (moderate, for subtle differ- mum mandibular width (Selander 1966). The ences with both sexes relatively colorful) and closer the value is to 1, the more likely the 3 (extreme, for male relatively colorful and chance of the sexes competing for the same female drab). Sexual ornamentation was food resources. defined as modified external morphology adapted for displaying and was ranked as: 0 RESULTS (none, for no differences), 1 (slight, for slight differences between male and female) and 2 Size. The plotted trend in size from smallest (moderate, for both sexes sharing similar to largest is as follows (with letter codes used ornamentation, but male having stronger in tabularized data following each species par- ornamentation). Pearson product-moment enthetically): I. isabellae (Ii), P. porphyrolaema correlations were used to assess the relation- (Pp), C. maynana (Cm), C. cayana (Cc), L. vocif- ship between size [ranked from smallest (1) to erans (Lv), P. nigricollis (Pn), Q. purpurata (Qp), largest (9)] and each sexual dimorphism char- G. foetidus (Gf) and C. ornatus (Co). acter, using the computer program SPSS (1996). Sexual dimorphism. Sexual dimorphism closely Other life history parameters include matches the range of sizes. Significant corre- feeding strategy, habitat association, sociality lations occur between size and M/F mass (r = [mean flock size and relative abundance 0.976, P < 0.001, N = 9) and M/F tail length (expressed by numbers of encounters/species (r = 0.728, P < 0.05, N = 9), but not for M/F

196 COTINGA LIFE HISTORY STRATEGY total length (r = 0.502, ns, N = 9), M/F wing 110267) had arachnid remains in its stomach. chord (r = 0.431, ns, N = 9), sexual dichro- The most general trend for feeding strat- matism (r = –0.554, ns, N = 9) or ornamenta- egy was that smaller species tend to be gorg- tion (r = 0.730, ns, N = 9). ers, medium and larger sized species shift For mass and tail length there is a trend of their diet seasonally depending upon whether females being relatively larger in the smaller fruits or animal prey are more abundant, and species towards the reverse (i.e., males being the largest two species enjoy fruits such as larger) in the larger species (Table 1). The palm fruits that grow along the river (Table strongest exception to this rule is wing chord, 1). In sum there appears to be a general trend which is relatively longer in females in all spe- towards increased dietary specialization with cies except for C. cayana and Phoenicircus. It is larger size. interesting to note that C. cayana is the only smaller-sized species that shows reverse Habitat association. The general trend is for trends in dimorphism; total and tail lengths in smaller species to be associated with higher C. cayana are relatively longer in males than in parts of the forest and larger species to use females and wing chord is shorter in males. lower parts of the forest (Table 1). Smaller The case of Phoenicircus is equally interesting species are forest canopy specialists and/or because all measured sexual dimorphism are often observed perched along the upper ratios break the continuous trend towards part of a tree within thick riverine vegetation. increasingly larger males in larger species. In contrast, the medium to larger species uti- The most extreme measures of sexual lize the middle and/or upper strata of interior dichromatism characterizes species at the forest. The two largest species are water edge smaller end of the spectrum (i.e., Cotinga and specialists, with the largest (Cephalopterus) Porphyrolaema), with the most diminutive spe- being an island specialist. cies (Iodopleura) and some of the larger species showing slight or moderate sexual dichroma- Sociality. Most of the smaller species are soli- tism (Table 1). The two species exhibiting no tary whereas larger species tend to travel in sexual dichromatism whatsoever (Lipaugus small flocks (Table 1). It is possible that and Cephalopterus) are the two species where group living evolved to enhance food finding males use their voice to lure females. in larger, sub-canopy dwelling species versus Cotingids show relatively little sexual smaller, supra-canopy dwelling species. Since ornamentation, with only the smallest all species are frugivorous and fruit is spa- (Iodopleura) and largest two species exhibiting tially non-predictable, it should be beneficial slight to moderate ornamentation (Table 1). to have multiple individuals search for a fruit Both of the largest species exhibit ornamen- patch that provides plenty of food for all tation in the head and throat region; Gymnodo- group members. Group living may benefit erus males have fleshy facial folds whereas riverine species such as Gymnodoerus in finding Cephalopterus males have larger crests and an preferred resources such as palm fruits. This external air sac projecting from the throat. may also explain subtle differences in breed- ing strategy for the cooperative breeder, Feeding strategy. All species are primary frugi- Querula (Snow 1971). In contrast solitary, vores, consuming small invertebrates such as supra-canopy dwelling individuals can per- insects to a lesser extent. Although all litera- haps locate fruit easier because they can see ture reports Phoenicircus to be a strict frugi- farther distances unobstructed by forest vore, at least one specimen (LSUMNS- growth. It should be more profitable for

197 BROOKS ET AL. g i b b 0 2 35 Co 2.1 r/s sol. 571 1.65 1.14 1.08 1.12 vocal 1/fem k b b r 1 1 v 31 m Gf 1.5 284 1.49 1.02 1.03 1.09 visual lek/sol. b s c 1 0 u 29 2.4 Qp 111 1.06 0.93 0.93 1.05 visual 1/fem. lek/sol. m m b b 2 0 2 u 95 Pn 1.0 yes lek 0.97 0.92 0.89 0.93 visual Several m a b b s 0 0 m 77 44 Lv lek 2.9 0.99 0.99 1.00 1.06 vocal Several Species k b b c g 3 0 1 b 76 29 Cc 1.5 yes 1.08 1.01 0.94 m,q,g For all species, see values above see all values species, For c g 3 0 1 70 11 1.2 yes sol. c/v Cm 0.93 0.96 0.91 1.02 visual m b b b b b 3 0 v 2 49 1 Pp 1.0 0.91 0.97 0.91 1.03 m m m b b b g 1 1 Ii c 1 18 1.0 yes 0.80 0.91 0.87 1.03 > 1 i j d sexual ornamentation ornamentation d sexual d c h e f Parameters (g) mass Mean Sexual dimorphism mass Male/Female M/F length total length M/F tail M/F wing chord Sexual dimorphism ornamentation Sexual Feeding Habitat Soliality Mean flock size abundance Relative Courtship strategy an dichomatism Sexual group males/display of Number Solitary male or lek Visual or vocal trees at feeding Competition More than 1 sex present yes cotingas Other present TABLE 1. Life historyTABLE parameters of nine sympatric cotingas.

198 COTINGA LIFE HISTORY STRATEGY C. c = Gf, Gf, = n 1986, Ter- ); c = Giant k foetidus

1979, 1993; Ellis ); m = Cinereous G. = Qp, Qp, = ly sharedresource patches cyanoptera

yes k,m Tyrannopsis luteiventris Tyrannopsis purpurata Brotogeris

Q. = Pn, = a in primary rainforest canopy, atypical in primary habitat for rainforest canopy, Nicéforo1954, 1951,1947, Sick bb Species P. nigricollis 1968, Béraut 1970, Howe 1982, HiltyBéraut1968, 1970, & Brow Howe Gymnodoerus ,t,f = Lv, = Lv, k ); p = Cobalt-winged ( Parakeet ) and Dusky-chested Flycatchers ( Flycatchers ) and Dusky-chested vociferans

L. s,p m 1.03 0.99 0.93 0.97 1.07 0.95 1.10 ely & Tudor 1994, Thiollayely & Tudor 1994, Brooks 1998. = Cc, = Cc, ). riverine specialist. riverine 01 0.73 1.00 1.00 0.77 0.84 1.10 1.47 g: Wallace 1849, Von Hagen 1937, 1849, Von g: Wallace C. cayana Graydidascalus brachyurus Graydidascalus episcopus

= Cm, simultaneously mobbingfemale a Ii Pp Cm Cc Lv Pn Qp Gf Co Thraupis Empidonomus aurantioatrocristatusEmpidonomus G. foetidus. G. Diamond & Terborgh 1967, Haverschmidt 1967, Haverschmidt Diamond & Terborgh g = source specialist, r = specialist, source hypopyrrha C. maynana

L. ta, u = upper strata, c = canopy, v = varzea/water edge, i = island varzea. v = varzea/water ta, u = upper strata, c = canopy, = Pp, = Pp, and slight, 2 = moderate, 3 = slight, 2 extreme. = moderate, ); s = Short-tailed Parrot ( s ); = Short-tailed Parrot Q. purpurata, cayana

q = ); f = Crowned-slaty ( ); f = Crowned-slaty flew off shortly after being mobbed and was probably simply moving through the atypical habitat. atypical the through moving simply probably was and mobbed flew being shortly after off C. ); t = Blue-gray Tanager ( ); t = Blue-gray Tanager 1990, Trail & Donahue 1993, 1991, Davis Ridg 1990, Trail lbb P. porphyrolaema Ictinia plumbea et al. hypopyrrha oryzivora

C. maynana, maynana, C. = Ii, Gymnodoerus m = . The isabellae Laniocerca

Scaphidura I. cayana, cayana,

= Co. Co. = C. Data supplemented or obtained with one or more of the followin Data not available. Sexualornamentation: slight, 1 = = moderate. none, 2 0 = associated. loosely are often Leks Incident involving a Incidentfemale involving A maledisplace may another male from a preferred calling site. Sexual dichromatism: 0 = none, 1 0 = = none, Sexual dichromatism: strategy: g = re gorger, s = seasonally Feeding Species: Food competionbetween sexes Food gape M/F maximum M/F mandible height 0.98 0.95 0.99 1. Parameters present species Other Habitat m = mid-upper stra association: Habitat Quantified by whether other individuals were ever observed at tree or not. Lack of data should be interpreted as species possib species as interpreted be should data of Lack not. or tree observed at ever were individuals other whether by Quantified c = k = Plumbeous Kites ( withbut otherit undetected. went individuals, TABLE 1. 1. Continuation. TABLE a b c d e f g h i j k l m Gymnodoerus Mourner ( 1952, Pinto 1953, Snow 1961,Pinto1952, 1971, 1953, 1982, Snow 1985; ornatus borgh 1986, Terborgh Cowbird ( Cowbird

199 BROOKS ET AL. smaller species to forage alone if fruit clumps not dimorphic. are “thinner” above than below the canopy. There is an interesting relationship Courtship strategy. Smaller, supra-canopy dwell- between sexual dichromatism and group size. ing species tend to be more colorful (Table 1). The species with extreme or moderate sexual The males of primarily larger species (that dichromatism tend to be solitary (Table 1). show the least amount or no sexual dichro- The brighter coloration of males of the matism) attract females through vocalizations smaller, solitary species serves to attract and/or subtle ornamentation (Table 1). Such females. However this does not mean that vocalizations are often more intensified in females of these solitary species are territorial birds dwelling in interior forest (Morton for mating rights. For example two female C. 1975) as seen in the case of Lipaugus for maynana sharing the same tree showed no ago- example. The common underlying pattern nistic interactions despite being courted by here is that males utilize different adaptations the same male. Females of the more social to lure females to their courting site. species are lured to a display site by male The number of males displaying to activity such as lekking and/or vocalizations, females can be divided into three general pat- or are present at the site as part of an inte- terns (Table 1). 1) Smaller species tend to grated social unit (e.g., Querula). have only one male courting at a time, even if Despite species packing rules (i.e., an area polygamy is involved. In one aforementioned of the same size will contain more smaller case a single male C. maynana displayed to two species and fewer larger species; see Cot- females about 25 m away in an adjacent tree. greave 1993) the trend of relative abundance 2) Medium sized species (Lipaugus and Phoe- from smallest to largest species is somewhat nicircus) have communal display sites where reversed (Table 1). This can perhaps be several males will display at once. These dis- explained by variation in species biology. For play arenas often span areas of 2500 – 40,000 example, Porphyrolaema, a smaller species, is m2. Finally, 3) the larger species (e.g., Querula naturally rare and is encountered with far less and Cephalopterus) are quite variable depending frequency in the field than most of the other upon the situation, but a single male tends to species with the possible exceptions of court one female. In sum we see a trend from Iodopleura and Phoenicircus. Therefore the low solitary male systems including polygamy in abundance (2 individuals) can be explained by the smallest species, to lekking in the medium naturally low numbers of this species in species and/or monogamous courtship in the nature. In contrast Lipaugus is a loosely-asso- larger species (Table 1). ciated lekking species. A solitary individual Figure 2 depicts three courtship models was only encountered on one occasion; on all (modified from Alcock’s model 1984), each other occasions they were in groups. Thus the describing hypotheses built upon life history higher abundance of Lipaugus is perhaps due patterns described herein: 1) Solitary, dichro- to social courtship constraints (i.e., where matic males of smaller species are attracted there is one, there are many). For example, on above the canopy because it highlights their one occasion we observed a group of Lipaugus iridescence and lures in females. The cost is in a loosely associated lek, when suddenly increased predation risk above the canopy but they formed a very tight lek, calling more rap- the benefit is lower energy expenditure. 2) idly and louder. It is possible that a female Actively courting males of medium species entered the arena at that time, though we are attracted below the canopy where fruit were unable to verify this since the sexes are clumps may be more aggregated. Since bright

200 COTINGA LIFE HISTORY STRATEGY coloring cannot be detected as well under the length and wing chord) show a significant canopy the males compensate through active pattern of females being larger than males in courtship such as lekking and/or vocalizing smaller species towards males being larger to lure in females. The benefit is decreased than females in larger species (see Webster predation risk below the canopy but the cost 1992). C. cayana and Phoenicircus are the two is increased energy expenditure during court- species that show exception to this rule. Phoe- ship. 3) Males of larger species are lured to nicircus may be closer related to manakins their courting sites by females that are (Pipridae) than other cotingas, perhaps serv- attracted to the habitat containing the pre- ing as the phylogenetic link between the two ferred resource. The male typically courts a groups (Trail & Donahue 1991). single female using subtle ornamentation, as The benefit of females generally being well as calling in some species. larger in smaller species may be linked to parental investment (see Payne 1984). For Competition at feeding trees. Data for seven of example, larger egg and offspring size would the nine species indicate that more than one have a reduced chance of predation and sex, species of cotinga or species of bird may therefore favor mothers of smaller species be present at the same feeding tree (Table 1). being larger (see Lack 1968, Andersson However, with the possible exception of 1994). Alternatively, smaller females in fluctu- Cephalopterus, there appears to be a relatively ating environments may be able to breed at high amount of feeding morphology overlap an earlier age than larger females, therefore between sexes (Fig. 3). Nonetheless, several breeding at a younger age would favor smaller observations suggest relatively low food females of the larger species (see Downer- resource defense in these species. hower 1976). Finally, males of larger species For example, the same sexes of a given (e.g., Cephalopterus) may benefit through species may share feeding sites for at least enhanced defense of resources such as court- some species. We observed three male Cotinga ing sites (see Andersson 1994). maynana foraging together on one occasion. The pattern of size dimorphism (mass On other occasions we observed groups of and tail length) increasing with larger males is two male Cotinga cayana foraging together concordant with Snow’s hypothesis (1982). with or without females present. Although not significantly correlated with Moreover, during more than 10 weeks of size, smaller species such as Porphyrolaema and field time we only observed a single direct Cotinga show increased sexual dichromatism agonistic interaction at a feeding tree. This whereas Iodopleura and the largest species was an incident involving a female Cotinga cay- show slight or moderate ornamentation. ana and Laniocerca hypopyrrha simultaneously Thus what certain species lack in sexual mobbing a female Gymnodoerus in primary dichromatism they may partly compensate rainforest canopy, which is atypical habitat for with slight or moderate sexual ornamen- for Gymnodoerus. The Gymnodoerus flew off tation. Non-dichromatic species also com- shortly after being mobbed and was probably pensate through intense vocalizations simply moving through atypical habitat. produced by the males to lure in the females. It is important to note that different DISCUSSION results might be obtained at other study sites, even with slightly different communities (M. Sexual dimorphism. Size dimorphism characters Théry pers. comm.). For example, of 11 for- of mass and tail length (rather than total est-dwelling cotingas in French Guiana, at

201 BROOKS ET AL.

FIG. 2. Variability in life history strategies among different groups. lease three larger species (Haematoderus milita- enjoying items such as palm fruits. The two ris, Procnias alba and Rupicola rupicola) show largest species were both water edge special- strong sexual dichromatism but little size ists in terms of habitat preference. This is dimorphism (Snow 1982), contrary to the probably a consequence of their preference findings observed herein. for riverine fruits (Sick 1993). Thus it is plau- sible, at least for these larger species, that dis- What lures females to their habitat? Larger species tribution within a landscape is dictated by tend to be increasingly selective in their diet, their preferred foods (Fig. 4). In contrast

202 COTINGA LIFE HISTORY STRATEGY

FIG. 4. General life history trends in nine species of cotingas.

reveal a different picture. Of those species in FIG. 3. Food overlap between sexes. the Cotinga clade that C. maynana is closest related to (e.g., C. amabilis, C. ridgwayi and C. females of the smaller, solitary species appear nattererii), C. maynana resembles C. cayana the to be lured to the brighter coloration of males least because it has a yellow iris and predomi- (Fig. 4). Whereas females of the more social nantly blue wings rather than dark iris and species are lured to display sites by male wings like C. cayana and the other species. activity (e.g., lekking, vocalizations, etc.) (Fig. Despite lack of competition for food 2). resources, there is a relatively low amount of feeding morphology overlap between sexes Lack of competition for food resources. There (Fig. 3). Perhaps this merely suggests that appears to be relatively little competition for males and females of most species only utilize similar food resources. Moreover fruit grows the same food resources, rather than compete as a clumped resource that varies seasonally for them (see Clutton-Brock & Harvey 1977). in spatial distribution. It is not profitable for We observed different sexes of Cotinga associ- primary frugivores to defend a resource that ated at the same resource patch on more than may not occur with any predictability within one occasion. that territory (see Brown 1964, Snow 1985). The fact that food resources are not Male reproductive strategy. Fruit as the main defended is strengthened even more by look- food resource appears to play an important ing at the lack of social mimicry between two role in the lives of most species. Fruit is congeners: C. cayana and C. maynana. The always present temporally but often unpre- benefits of social mimicry include: 1) escap- dictable spatially. A lack of territoriality is ing attack from larger models, and 2) deriving beneficial in areas where food resources are higher status at a resource site – smaller spe- spatially unpredictable because the fruit may cies may be deterred from occupying the not blossom within the defended area. The same site where the seemingly larger model main benefit of a clumped, temporally pre- (that is really the mimic) is present (Diamond dictable resource is decreased foraging time 1982). For social mimicry to be achieved, two (i.e., take/search time) that permits a male to more distantly related species must be more mate with more than one female, and allows chromatically similar to one another than the female to raise the offspring alone (Snow they are to other more closely related species. 1985). The lack of territoriality between Although C. maynana and C. cayana look simi- males combined with the potential to mate lar from a distance, specimens in the hand with more than one female results in intense

203 BROOKS ET AL. sexual competition and the evolution of behavior may explain the increased male sex- extreme courtship displays (Snow 1985). This ual dimorphism in such larger species (see pattern is especially apparent in the smaller Andersson 1994). species that show higher sexual dichromatism (see Bradbury & Vehrencamp 1998). ACKNOWLEDGMENTS Bradbury & Vehrencamp (1998) have overviewed the pattern of more brightly col- We thank Marc Théry, David Snow and Ken ored species living above the canopy to Risenhoover for helpful comments on this opportune sunlight in order to advertise their ms. We are indebted to CONEPAC and iridescent coloration to females. Moreover, it INRENA for allowing us to work in the is more difficult for smaller species to adver- region. Logistical support was provided by tise auditorily (see Bradbury & Vehrencamp Explorations, Inc. and Peter Jenson of 1998), which may explain the bright iridescent Explorama. coloration in species such as Cotinga. Alcock (1984) predicts that species advertising with REFERENCES visual cues spend a low amount of energy doing so. The trade-off is that such bright col- Alcock, J. 1984. Animal behaviour: an evolutionary ors may also advertise the males presence to approach. Sinauer, Sunderland, Massachusetts. predators (Endler 1991). In contrast, the pat- Andersson, M. B. 1994. Sexual selection. Princeton tern of more drab species living below the Univ. Press, Princeton, New Jersey. canopy perhaps favors decreased predation Béraut, E. 1970. The nesting of Gymnoderus foetidus. (Bradbury & Vehrencamp 1998). However Ibis 112: 256. some of these species with decreased sexual Bradbury, J. W., & S. L. Vehrencamp. 1998. Princi- dichromatism (e.g., Lipaugus) advertise to ples of animal communication. Sinauer, Sun- females using auditory cues that Alcock derland, Massachusetts. (1984) predicts are energetically high, as con- Brooks, D. M. 1997. ¿Son la competencia, el firmed in multiple subsequent studies (e.g., tamaño y la superposición de dietas pronostica- dores de la composición de Ramphastidae? Pp. Eberhardt 1994). Nonetheless, auditory sig- 283–288 in Fang, T. G., R. E. Bodmer, R. nals are less constrained by environmental Aquino, & M. Valqui (eds.). Manejo de fauna factors (e.g., filtering by sub-canopy vegeta- silvestre en la Amazonia. OFAVIM, La Paz. tion) than visual signals (Bradbury & Vehren- Brooks, D. M. 1998. Competition and coexistence camp 1998). It appears that the courting site in Neotropical birds: a latitudinal comparison. of a male(s) is established to attract a Ph.D. diss., Texas A&M Univ., College Station, female(s) in the smaller and medium-sized Texas. species (Fig. 2). In this case the females pat- Brown, J. L. 1964. The evolution of diversity in tern of spatial distribution may be a conse- avian territorial systems. Wilson Bull. 76: 160– quence of male distribution rather than 169. presence of food resources. Clutton-Brock, T. H., & P. H. Harvey. 1977. Pri- mate ecology and social organization. J. Zool. There is a trend from solitary male sys- 183: 1–39. tems including polyandry in the smallest spe- Cotgreave, P. 1993. The relationship between body cies, to lekking in the medium species and/or size and population abundance in animals. monogamous courtship in the larger species. TREE 8: 244–248. Indeed, as mentioned previously male Cepha- Davis, S. E. 1993. Seasonal status, relative abun- lopterus have been observed displacing other dance, and behavior of the birds of Concep- males from a favored courting site. This cion, Dpto. Santa Cruz, Bolivia. Field. Zool. 71:

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