The Role of the Feet in Behavioral Thermoregulation of Hummingbirds

(hndor 85:2X1-285 ‘c: The Cooper Ornithological Society 1983

THE ROLE OF THE FEET IN BEHAVIORAL THERMOREGULATION OF HUMMINGBIRDS

MIKLOS D. F. UDVARDY

ABSTRACT. -Four species of hummingbirds (Archilochus alexandri, Cal_vpte anna, Selasphorussasin, and S. rufus) were observed to keep their feet and toes in a special patch of downy belly feathers at low ambient temperatures (T,), gradually expose them as temperatures rise, and hold them fully exposed at high T, when hovering and perching. Since the position of the feet depends upon T,, it probably influences the birds’ heat transfer coefficient.

In many speciesof hummingbirds, such as Al- tila) often flew with their legs conspicuously len’s Hummingbird (Selasphorus sasin; Al- extended. drich 1956) the posterior ends of the ventral I report here on follow-up observations,test- pteryla bear plumulaceous feathers that cover ing the hypothesis that the abdominal patch the entire belly below the sternal margin, just servesas a heat conserver for the feet and that anterior to the vent (Fig. 1). My scrutiny of the latter participate in thermoregulation fresh specimensof several species(e.g., Anna’s (Udvardy 1977). Hummingbird, Calypte anna) revealed that these feathers are semiplumes that are dark MATERIALS AND METHODS basally, and white at the tip. They form a patch Between 1975 and 198 1, I observed hum- that is often white and conspicuous,especially mingbirds at three sites in California: (1) near in otherwise dark-plumaged species, such as sea level in the Sacramento area (38”31’N, the Fork-tailed Emerald (Chlorostilbon cani- 121”3O’W) throughout the year; (2) at 260 m vetii). It is clearly visible in many photographs elevation at Three Rivers (36”45’N, 118”55’W; of North American hummingbirds, e.g., those July 1979); and (3) at 380 m elevation near in Grant and Grant (1968) and Udvardy Placerville (38”45’N, 120”56’W; summer only). (1977). Drawings ofhummingbirds show these Data were collected intermittently during all patchesin various positions (see,e.g., Peterson months of the year, but mostly during June- 196 1, Robbins et al. 1966, Petersonand Chalif Septemberand November-February, i.e., at the 1973) often creating the impression that there extremesof the hot, dry summer, and the rainy, is a conspicuous, fluffy white ring of down cool winter, respectively. At all three sites, a on the distal end of the shank. Such “tibia1 clear glassfeeder with red plastic flower-shaped tufts” or “puffs” -consisting of enlarged down bibs was hung outside a large window, behind or contour feathers- occur in certain neotrop- which the observer sat in plain sight. Sugar/ ical hummingbirds (see, e.g., photographs of water solution (1:3, v/v) was fed to the birds. the Sapphire-vented Puffleg, Eriocnemis luci- The feeder had no perch, and thus the birds ani, and Crimson Topaz, Topaza pella, in fed while hovering, as they usually do when Greenewalt 1960; of Boissonneauaspp., Er- feeding from flowers. During each observation iocnemis spp., and Ocreatus spp. in Schuch- of a hummingbird, the time of the day, am- mann 1979a). bient temperature (T,) in the shadeat the feed- While in Honduras during 1971 and 1976, er, and the species,sex, and, if possible,age of I noticed that in the foggy, cool, and often rainy the feeding bird were noted, together with the climate of El Hatillo, a suburb of the capital position of its feet. city of Tegucigalpa (elevation 1,460 m; The feet of a hovering hummingbird were 14”04’N, 87”13’W), Green Violet-ear (Colibri categorizedaccording to their position (Fig. 2). thalassinus),White-eared Hummingbird (Hy- Position O-feet completely withdrawn into the locharis leucotis), Red-billed Azurecrown muff on the belly; position 2-tibiae and tarsi (Amazilia cyanocephala),and C. canivetii fre- extended and held at approximately right an- quently hovered with their feet drawn into the gles to the flanks, and the toes fully extended; belly as if into a “muff.” In contrast, on the position 1-intermediate situations,e.g., when tropical seashoreof the Caribbean (near Brus the clenched “fist” was exposed and unfolded Laguna; 15”48’N, 84”3O’W), the three most or when the toes were slightly straightened. common speciesof hummingbirds (C. cani- I report here on 459 observations of Anna’s vetii; Green-breasted Mango, Anthracothorax Hummingbird (136 males, 114 females, 113 prevostii,and Cinnamon Hummingbird, A. ru- juveniles, and 96 undetermined), 46 obser- 12811 282 MIKLOS D. F. UDVARDY

FIGURE 1. Ventral view of a frozen specimen of Cu- lypfeanna (juvenile male). The grey ventral contour feathers have been plucked away to expose the two patchesof x white abdominal semiplumes. The feet have been spread 25 - laterally to show that the feathered thighs do not have down or semiplumes. vations of Black-chinned Hummingbird (Ar- chilochusalexandri; 42 males and 4 females), and 102 observations of Rufous (Selasphorus rufus) and Allen’s hummingbirds combined. The latter two speciesare transient in the Sac- 3-8 9-14 15-20 21-26 27-32 33-38 39.440 ramento area betweenJuly and September.The T, classes (“C) adult males of these Selasphorusspecies are easy to distinguish, but females and juveniles FIGURE 2. Percentages of observations of Anna’s are not. Consequently, I lumped my obser- Hummingbirds in different foot positions at various am- vations of these speciesinto a single category, bient temperatures(T,), pooled into 6°C classes. Selasphorusspp. The 102 observations com- prise 16 of male S. sasin, 25 of male S. ruftls, and 6 1 of unspecified females and juveniles. hours. However, whenever the temperature changed, the position of the feet varied ac- RESULTS cordingly. Correlation offoot position with ambient tem- During July and August 198 1, I also ob- perature is best illustrated by my data for C. served non-feeding hummingbirds perched on anna (Fig. 2; Y, = 0.75-0.8 1; P < 0.001, telephone lines, watchingthem from a distance Spearman’s Rank Correlation Test). Never- of lo-25 m with binoculars or a telescope. theless, the correlation was highly significant These observations, however, were not quan- in all species(rs = 0.75-0.86; P < 0.00 1). Foot tified. Birds perched in the sun during the cool position 0 wasthe rule below 1X, above which morning hours, but moved into the shadewhen it graded into position 1, which predominated the T, exceeded25-30°C. During cool periods, between about 26 and 30°C. Position 2 was they sat with their toes covered by the belly typical at T,s above 30°C. The processof ex- and flank feathers. Above 30-32°C they stood posing the toes (i.e., the transition from po- on relatively outspread feet, the axis of the sition 0 to position 1) appeared to be more body approximately perpendicular to the feet. gradual than that from 1 to 2. Between 30 and The wings drooped and the bend of the wing 32°C the toes opened and the tarsi were ex- was held somewhat away from the body (Fig. tended. Above 32°C all hummingbirds (70+ 4). observations covering all four species) held their feet in extreme position 2. Fewer obser- DISCUSSION vations were made of the Black-chinned Hum- While the position of the feet in my sample of mingbird and the Selasphorusspecies, but the hovering hummingbirds was artificially clas- pattern of exposingthe extremities with rising sified for the purpose of scientific notation, temperature was the same (Fig. 3). pooled data indicate a gradual shift in foot Male, female, and juvenile Anna’s Hum- position in response to changes in ambient mingbirds did not differ with respect to the temperature. The feet of birds are well known position of the feet as a function of T, (the rank to serve asa thermoregulatory device for either correlations were approximately the same for conservingor dissipatingheat (summarized by all sex and age classes).Several serial obser- Calder and Ring 1974). Similar changesin the vations disclosedthat position 2 was used ex- position of the tarsus and toes as a function clusively during the afternoon and evening of T, have been described in the Budgerigar HUMMINGBIRD THERMOREGULATION 283

N: 6 9 16 13 2 N: 8 17 35 33 9 100 cu .z 75 C g ; 50 S 5 25 S 0

.& 75 .z 8 z 50 P v $ 25 0 Jm-lL 0 .-5 75 .= 8 a 50 g v g 25 B 0 15-20 21-26 27-32 33-38 39-44 I-L-15-20 21-26 27-32 33-38 39-44 Ta Classes (“C) Ta Classes (“C)

FIGURE 3. Percentagesof observations of Black-chinned Hummingbirds (left) and Selusphorus hummingbirds (right) in different foot positions at various ambient temperatures.

(Melopsittacusundulatus; Tucker 1968) and in moregulation. Hovering birds of all four Cal- eight speciesof African birds (Frost and Sieg- ifornia species,in addition to those observed fried 1975). We can now extend these obser- in tropical Honduras, exposed their tarsi and vations to hummingbirds:when faced with heat feet on hot days (56 of 57 Anna’s Humming- losses,they withdraw their feet into the downy birds, and all Black-chinned Hummingbirds feathers on the belly. and Selasphorus;Table 1). The few exceptions Lasiewski (1964) demonstrated that resting at high T,s (e.g., one Anna’s Hummingbird had hummingbirds have a lower critical tempera- clenched feet at 35°C) may have been due to ture of about 27-30°C. Flight, however, in- sudden changes in temperature immediately creasesthe heat production of birds (e.g., Bau- around the birds, as, for example, caused by dinette et al. 1976) in general, and gustsof wind. hummingbirds (cf. Morrison 1962, Schuch- Lasiewski (1964) found resting body tem- mann 1979b) in particular. This may explain peratures (T,,) in the speciesstudied here to be why foot position 1 was most common at T,s between 34.4 and 4 1.2”C. Those of nine species between 26 and 30°C. Below this range of T,s, of Brazilian hummingbirds are between 39.5 the feet were increasingly withdrawn, and pro- and 44.6”C (Ruschi 1949). Even the lower ex- tected. The exceptions (toes showing or tarsi tremes of these values are higher than the T, extended by some Anna’s and Rufous hum- at which feet and toes are completely extended. mingbirds at T,s between 16 and 24°C) may Hummingbirds may regulate the temperature have been causedby exertion before birds vis- of the blood, and hence body temperature with ited the feeder, i.e., the birds may have de- countercurrent exchangersand arteriovenous veloped a heat load that had to be dissipated shunts in their hind limbs as do other birds while they fed. (Steen and Steen 1965). When the T, is below My observations suggestthat the extension the T,, the extended legs, when allowed full of feet at high T,s is a form of behavioral ther- circulation, may increase heat loss from the 284 MIKLOS D. F. UDVARDY

TABLE 1. Observationsof hummingbird foot positions at various ambient temperatures (T,). Total number of observations= 607. Position O-feet hidden in downy abdominal feathers, position l-toes visible, position 2- feet and toes exposed.

44 3 1 42 2 1 1 40 7 1 2 FIGURE 4. Posturesof restingAnna ’s Hummingbird in 11 1 5 responseto ambient temperature. Left: in the cold; feet 38 6 4 protected by abdominal feathers, plumage fluffed. Right: 6 2 8 hot and panting;feet fully exposedand spreadapart, plum- 36 11 3 6 age sleek,wings drooped and slightly away from the body. 1 4 3 1 34 5 3 7 2 1 22 2 7 32 4 14 4 in Trochilidae. Individuals of seven species 1 4 8 2 responded to rising T,s by elevating their T,. 30 1 8 5 2 Maximum T, ranged from 39.9” to 43.3”C at 1 17 3 1 2 28 5 19 10 6 T,s between 34 and 41°C respectively. These 5 14 4 10 birds, then, became hyperthermic at high T,. 26 3 15 3 1 7 Since this stored heat increasesthe difference 10 9 2 1 between their T, and the prevailing T,, it en- 24 7 7 1 1 6 6 2 1 ables them to dissipateadditional, excessheat 22 8 4 by exposing their tarsi and feet. In the light of 1 3 these findings, it would be desirable to repeat 20 8 2 1 Lasiewski’s experiments on North American 5 1 hummingbirds, exposingthem to high T,s and 18 11 3 1 4 5 1 watching for a thermoregulatory role of their 16 8 4 2 feet. 8 4 1 14 4 SUMMARY 7 4 12 16 4 The hummingbirds that I observed hid their 17 4 feet in the downy plumage on the lower ab- 10 24 2 domen at T,s below about 24°C. As the tem- 10 8 5 perature rose, the birds gradually exposedtheir 1 feet and toes, presumably to facilitate heat loss. 6 1 Above 32°C the feet and toes were exposedas 4 1 fully as possible. The two extremes and the 4 intermediate postures of the feet are closely 3 2 correlated with ambient temperature. The T, values at which these behavioral n 186 146 127 14 16 16 12 34 56 changesoccur in the Anna’s Hummingbird are independent of sex, age, season,or the time of the day. In the three other species,the trend blood by conduction and convection. This is the same, yet owing to their much smaller mechanism may be used by both hovering and size future detailed studies may reveal differ- perchingbirds, sincethe latter also exposetheir ences. A lower and narrower range of T,s for feet and toes in hot weather. While hovering, the intermediate foot position would reflect a such postulated heat loss may be augmented greater need for behavioral thermoregulation by convection currentsgenerated by the wings. at low as well as high ambient temperatures in Recent experimental work on several species these species. oftropical hummingbirds(Schuchmann 1979b, ACKNOWLEDGMENTS c, Schuchmann and Schmidt-Marloh 1979a, b, Schuchmann et al. 1979, Schmidt-Marloh I am grateful to Mary Bacon and Maud E. Udvardy for and Schuchmann 1980) castsdoubt on the gen- their original observations,which are reported here with mine. Mrs. Udvardy also typed the manuscriptand helped eral validity of the classicalconcept of thermal in many other ways. I also thank Harold W. Kerster for neutrality and associatedmetabolic responses doing the statistical analysis, Charles S. Papp for the il- HUMMINGBIRD THERMOREGULATION 285 lustrations, Monica L. Udvardy for editorial and gram- PETERSON,R. T., AND E. L. CHALIF. 1973. A field guide matical comments, and Peter Stettenheim for suggestions to Mexican birds. Houghton Mifflin Co., Boston. concerningthe feathers.Elmer C. Aldrich, George A. Bar- ROBBINS.C. S.. B. BRUUN.AND H. S. ZIM. 1966. Birds tholomew, Robert D. Montgomerie, Oliver P. Pearson,and of North America. Golden Press, New York. an anonymous reviewer gave thorough critiques of the RUSCHI,A. 1949. Observaqdessobre trochilideos. Bol. manuscript that helped to clarify my discussionand con- Mus. Biol. Prof. Mello-Leit%o 7: l-65. clusions.My 197l/ 1972 fieldwork in Honduraswas during SCHMIDT-MARLOH,D., AND K.-L. SCHUCHMANN.1980. a Fulbright lectureship,and in 1976, it was supported by Zur Biologiedes blauenVeilchenohr-Kolibris (Colibri a grant from the Frank M. Chapman Memorial Fund of coruscans). Bonn. zool. Beitr. 3 1:6l-77. the American Museum of Natural History. Mrs. C. S. de SCHUCHMANN,K.-L. 1979a. Kolibris, Haltung und Pflene. Beausset,Mrs. G. Eoff, and J. Eoff generouslyprovided Biotropic Vg., Frankfurt. the logistical base during my staysin Honduras. SCHUCHMANN.K.-L. 197913.Metabolism of flvine hum- , ” mingbirds. Ibis 121:85-86. SCHUCHMANN,K.-L. 1979~. Energieumsatz in AbhXn- LITERATURE CITED gigkeit von der Umgebungstemperaturbeim Kolibri Ocreatus u. underwoodii. J. Ornithol. 120:3I 1-3 15. ALDRICH,E. C. 1956. Pterylography and molt of the SCHUCHMANN,K.-L., AND D. SCHMIDT-MARLOH.1979a. Allen Hummingbird. Condor 58:121-133. Metabolic and thermal responseto heat and cold in BAUDINETTE,R. V., J. P. LOVERIDGE,K. J. WILSON,C. D. Streamertail Hummingbirds (Trochiluspolytmus and MILLS, AND K. SCHMIDT-NIELSEN.1976. Heat loss Trochilus scitulus, Trochilidae). Biotropica 11: I23- from feet of Herring Gulls at rest and during flight. 126. Am. J. Phvsiol. 230:920-924. SCHUCHMANN,K.-L., AND D. SCHMIDT-MARLOH. 1979b. CALDER, W. A:, AND J. R. KING. 1974. Thermal and Temperature regulation in non-torpid humming- caloric relations of birds, p. 259-413. In D. S. Farner birds. Ibis 121:354-356. and J. R. King [eds.],Avian biology. Vol. 4. Academic SCHUCHMANN,K.-L., D. SCHMIDT-MARLOH,AND H. BELL. Press, New York. 1979. Energetische Untersuchungen bei einer tro- FROST,P. G. H., AND W. R. SIEGFRIED. 1975. Use of pischenKolibriart (Amazilia tzacatl). J. Omithol. 120: legs as dissipators of heat in flying passerines.Zoo- 78-85. logica Africana 10:101-102. STEEN,I., AND J. B. STEEN. 1965. The importance of the GRANT, K. A., AND V. GRANT. 1968. Hummingbirds legs in the thermoregulation of birds. Acta Physiol. and their flowers. 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