Condor,80:216-221 @ The CooperOrnithological Society 1978

TERRITORIAL DEFENSE AGAINST AND INSECTS BY TROPICAL HUMMINGBIRDS

THOMAS C. BOYDEN

Studies of time and energy budgets generally ing. In nature, whether or not an intruder is require measuring the division of time among pursued should also depend on the frequency an ’ various activities and then con- of invasion of the territory by other classes of verting these values to appropriate energetic intruders and the amount of time and energy costs. For highly mobile animals, such infor- available for defense. The threat posed by a mation is often difficult to obtain because of competitor should depend on its size, appetite, problems of observing them at close range and foraging efficiency and ability to displace the the variability of their behavior. territory-defender. The frequency, distance Territorial hummingbirds are ideally suited and duration of chases of intruders of differ- for the study of time and energy budgets for ent classes should correspond to the threat the following reasons. (1) Their daily ac- that each poses to the territory. Different tivities are usually quite localized. (2) They types of intruders visiting the territory si- are not affected by the presence of a quiet ob- multaneously should be chased in the order server and consequently can be observed at of the threat they pose-for nectar depletion close range. (3) They feed almost exclusively or territorial displacement-the intruder pos- on nectar from flowers on their territories. ing the greatest threat being chased first. The caloric content of their food is therefore easily assessed. (4) Most of their daily activi- STUDY AREA AND METHODS ties in the wild are spent at two basic meta- bolic levels, hovering flight and resting (perch- Most of this work was conducted at Morgans’ Gar- dens, 5 km N of Balboa, Canal Zone from 23-25 June ing). The energetic costs at both these levels 1974. The main study site was a feeding territory have been measured and appear to be similar consisting of seven flowering bushes of the Pagoda for most studied (La- Plant ( Isertia hankaeana, Rubiaceae), covering an siewski 1963, Hainsworth and Wolf 1972a). area 8 m x 4 m x 3 m that was defended by a Many studies describe hummingbirds de- single Rufous-tailed Hummingbird ( Amuziliu tzucutl) . In addition, I observed a White-vented Plumeleteer fending flowers from other hummingbirds, but Hummingbird ( Chalyburu buffonii) defending a reports of chasing insects from their ter- feeding territory of ten I. hankaeuna bushes at a ritories are rare (Pitelka 1942, Stiles and Wolf woods trail 2 km W of the Bridge of the Americas 1970, Lyon 1974, Primack and Howe 1975). near Panama City, Panama on 3 July 1974. All dis- cussion which follows refers to the territory defended In addition, information on the frequency of by A. tzucutl unless stated otherwise. insect chasing by territorial hummingbirds, its I watched the Rufous-tailed Hummingbird over role in territorial defense, and its importance several periods totalling 11 h 43 min. These periods with respect to competition for nectar re- were generally between 06 :30-12 :00 because of un- sources is scant. In this paper I investigate the predictable weather conditions and a general decline in the activity of pollinators in the afternoon. The significance of insect chasing through a con- birds activities were recorded by two people using sideration of the time and energy budgets of stopwatches. Activity categories recorded were: territorial hummingbirds. I also test some Perching, Change of Perch, Display, Feeding, Chas- predictions of optimal behavior in humming- ing Birds, Chasing Bees and Gone. The last category birds defending flowers from intruders of dif- includes time the hummingbird was out of sight. No flycatching or foliage gleaning for insects was ob- ferent sizes. served during this study.

THEORY RESULTS AND DISCUSSION I hypothesize that a hummingbird should de- The most common insect visitors to the ter- fend a feeding territory whenever the distribu- ritory were the long-tongued euglossine bees tion of flowers and the quality and abundance (Eulaema nigrita and E. cingulata) and car- of nectar on the territory are such that the penter bees (Xylocopa spp. ) . Other occasion- is more than repaid the energy it expends in self-maintenance and defense. Each potential al visitors included small euglossines (e.g., competitor that invades the territory should, Euglossa mixta, E. cyanapsis) and butterflies. in theory, be chased by the bird, providing Both large and small euglossines fed on Isertia that the energy represented in nectar thus nectar for I saw several individuals probing saved outweighs the energetic expense of chas- the flowers with their tongues. Similarly, I I2161 TERRITORIAL DEFENSE BY TROPICAL HUMMINGBIRDS 217 observed carpenter bees perforating flower TABLE 1. A summary of actions by a single corollas at their base to obtain nectar. Amazilia tzacutl hummingbird defending a feeding territory against other hummingbirds and bees.* 1. hunkaeanu is native to Panama and it flowers from May to mid-September. The Intruder flowers have long tubular corollas, and are Large initially yellow, gradually changing to red- bees dish-orange over several days. Only the newer No. chased 588 131 yellow flowers are visited by hummingbirds No. not chased 11 95 and insects. Chase with vocal display 433 5 The defended area contained 104 inflores- Chase w/o vocal display‘ 155 126 cences, each bearing an average of 66 new Feeding after chase 46 66 flowers (S = 3.78, N = 20). The average vol- No feeding after chase 542 65 ume of nectar per flower (new) at the begin- X distance of chase (m ) 5.44 0.68 ning of each day (06:30) was 1.5 ~1 (S = 3.24, X duration of chase (s) 7.24 2.53 N = 60). Sugar content of the nectar, mea- j, no. Cal/chase (roundtrip) 2.16 0.75 sured in the field with a Bausch and Lomb * Other insects intruding on the territory during this period hand refractometer, averaged 22.1% by weight are discussed in the text. (S = 1.24, N = 36). The nectar was analyzed with the aid of paper chromatography in the laboratory and the sugar was primarily su- birds were pursued by the defending A. tza- crose. cat2 while only 131 large bees were chased. The average nectar content of the territory The three large butterflies were chased away at the beginning of each day was estimated at immediately upon landing on flowers, but 10,296 ~1. I calculated the energy content of none of the smaller skipper butterflies or small Isertia nectar as follows: a 22.1% sucrose solu- euglossine bees visiting flowers on the terri- tion by weight is equivalent to 0.87 Molar. tory were pursued. The Rufous-tailed Hum- To convert this to calories, I used a value of mingbird did not respond to other insects fly- 1349.6 Cal/ml for 1 M sucrose (or 1174 Cal/ml ing over or landing on the territory (e.g., for 0.87 M; see Hainsworth and Wolf 197213). dragonflies). The average energy content of the territory When intruder groups were ranked by size at the start of each day was thus estimated at (hummingbirds, large bees and butterflies, 12,087 cal. small bees and butterflies), the frequency of The oxygen consumption by A. tzacatl dur- chases relative to the total number of invasions ing forward and hovering flight was assumed differed among size classes significantly. to be 43 ml/g/h ( see Wolf et al. 1972). This Hummingbird chases by A. txacatl occurred is equivalent to 5 Cal/ml of 02 consumed at with significantly greater frequency than did a Respiratory Quotient (R.Q.) of 1 (see Hain- chases of large bees and butterflies (x2 = sworth and Wolf 197213). 233.3, P < .OOl ). Large bees and butterflies The crop capacity of all invading humming- were chased with significantly greater fre- birds was assumed to be equivalent to that of quency than were small bees and butterflies a 5 g hummingbird (684 J), while the honey- (x2 = 62.76, P < 601). Thus the frequency of stomach capacity of all E. nigrita, E. cingulata aggression shown by the defending humming- and Xylocopa bees was assumed to be equiv- bird towards different intruder groups ap- alent to that of a bumblebee of comparable peared to depend on their size and hence the size (100 pl; Hainsworth and Wolf 1972a, potential threat that they posed for depletion Heinrich 1975b). The smaller euglossines of nectar resources on the territory. were not quite honeybee size and were as- An alternative explanation for the chasing sumed to have a honey-stomach capacity of of intruders is that the bird was responding to 25 ~1 (honeybee capacity = 40 ~1; Heinrich the overall numbers of intruders rather than 1975a). to their size. Many more hummingbirds A total of 599 hummingbirds (primarily visited the territory than did large bees, and conspecifics) and 236 large bees (E. nigrita, many more large bees visited the territory E. cingulata and Xylocopa spp.) visited the than did small bees and butterflies. This ex- Isertia territory during the entire study (Table planation seems unlikely, however, because 1). Other flower visitors during this period only three large butterflies visited the terri- included 41 small skipper butterflies (Hes- tory and they were immediately pursued, periidae), 16 small euglossine bees, and three whereas none of the 41 small skippers or 16 large butterflies (two Phoebis sennae, one small euglossines was chased. Heliconius erato). Of these, 588 humming- The White-vented Plumeleteer defended its 218 THOMAS C. BOYDEN territory primarily from butterflies. During a tivities during peak periods of hummingbird 3 h period, it chased 24 large butterflies, six invasion. small butterflies, two large bees, one wasp Another habit that seemed to be related to and three hummingbirds from its territory. the frequency of hummingbird invasion was The butterflies chased included 18 Parides se- the perching position of the defending bird sostris, five P. arcus (Papilionidae), one Phoe- on the territory. During periods of intense his sennae (Pieridae), and six Eudamus spp. invasion by hummingbirds, the defender gen- (Hesperiidae). The bees were Eulaema ni- erally returned to one of two perches in the grita, the wasp was not identified, and the center of the territory, whereas, during periods hummingbirds were two Fork-tailed Emeralds when few or no hummingbirds were invading, (Chlorostilbon canivetii) and one Chalybura its perch sites on the territory were more buffonii. varied. By perching in a central location, the Primack and Howe (1975) observed a Ru- defending bird may have been able to see fous-tailed Hummingbird defending a terri- intruders more readily and maintain a more tory of Stachytarpheta jamaicensis flowers pri- effective defense. marily from skipper butterflies in Costa Rica. Bees were rarely chased beyond the bounds If skipper butterflies (and small bees) are of the territory (ii = 0.68 m), while humming- worth pursuing, the fact that they were not birds were usually chased well beyond them chased by the A. tzacatl I observed can be ex- (2 = 5.44 m; t = 4.62, P < .OOl). The differ- plained by the high frequency of invasion by ences in these distances may merely indicate other intruders with a greater potential to de- that a bee is more easily intimidated by a hum- plete the territorial resources. According to mingbird than is another hummingbird and energetic theory, visitors should be chased in that it is not necessary to pursue a bee as far order of the potential threat that they pose in as a hummingbird to achieve the same effect. terms of nectar depletion and territory dis- However, the pursuit of bees up to, but rarely placement. As many large bees were not beyond, the territorial boundary also left the chased from the territory and chases of large defending bird in a position to ward off pos- bees should take priority over chases of small sible hummingbird intruders. bees and butterflies, the fact that small bees The amounts of vocal display by the defend- and butterflies were not pursued appears to ing bird during pursuit of hummingbirds and make good energetic‘ sense.’ In contrast, hum- bees differed significantly ( i2 = 219.35, P < mingbirds defending territories with less fre- ,001) . A. tzacatl most often emitted a shrill quent invasion and fewer intruders, such as chattering trill during hummingbird chases but the plumeleteer I observed and possibly the made no vocalizations during most bee chases. Rufous-tailed Hummingbird observed by Pri- These observations also appear to correspond mack and Howe may, as a result, be able with energetic‘ logic.’ Vocalizations directed to extend their defense repertories to include towards bees by a territory-holding bird would chasing smaller intruders. seem to be an unnecessary energy expediture The behavior of A. tzacatl in response to in- because bees cannot hear and therefore are not truding hummingbirds and bees was quite dif- likely to respond to such signals. Vocalizations ferent. The defending bird pursued all hum- directed towards hummingbirds, on the other mingbird intruders, with the exception of hand, advertise the presence of the territory- larger, more dominant species and those in- holding bird and may serve to deter some in- dividuals who visited the territory during its dividuals from invading the territory. absence. Bees, however, were generally pur- sued only when hummingbirds were not in- vading or feeding on the territory. This lesser‘ THE ENERGETICS OF DEFENSE priority ’ of bee chases (also evident in the I did not assessthe impact of intruders on the data on the frequency of chases of these two total nectar resources available on the territory intruders groups) corresponds to energetic defended by either hummingbird because of theory. The defending bird also spent sig- the difficulties of monitoring the activities of nificantly more time feeding during the pe- riods when hummingbirds were not invading different intruders visiting the territory si- (x2 = 147.49, P < .OOl). By chasing bees and multaneously and in assessing quantities of feeding more during these periods, the de- nectar they extracted. However, it was pos- fender was presumably exhibiting optimal‘ sible to make some general energetic predic- behavior ’ because probably much less nectar tions based on the calculated energy ex- was removed from the territory than would penditure by A. txacatl, estimates of the have been the case had it performed these ac- honey-stomach capacity of intruders, and mea- TERRITORIAL DEFENSE BY TROPICAL HUMMINGBIRDS 219

TABLE 2. Time budget and calculated energy expenditure for a single A. tmcatl hummingbird defending a feeding territory against hummingbirds and insects.

C;h& Change Perchine Feedine of Derch chb:seis”g Dis&w_ GolIe Total Minutes 402.55 125.65 70.93 9.67 5.51 3.08 85.58 702.97 % of total time 57.26 17.87 10.09 1.38 0.78 0.44 12.17 100 Calories expended 716 2251 1271 173 99 55 - 4565 % of total calories expended 15.7 49.3 27.8 3.8 2.2 1.2 - 100

The number of calories expended perching was calculated for a S-g hummingbird at Resting Metabolic Rate (RMR) by using the equation of Herreid and Kessel (1967) relating thermal conductance to body weight and assuming a constant body temperature of 41-C at an ambient temperature of 3o”C, RMR = 106.7 Cal/h (see also Hainsworth and Wolf 1972a). Enerav expenditure in all other categories is based on hovering flight for a 5-g hummingbird (43 ml 0.,/h X 5 al/ml O., X 5g =?07< Cal/h); (Hainsworth a&Wolf 1972b, Wolf et al. i972). surements of the nectar resources available on nectar saved by chasing hummingbirds and the territory. bees from the territory greatly outweighs the In examining the energetics of defense, it energetic expense incurred by A. tzacatl in first seems necessary to determine whether the chasing either type of intruder. territory occupied by A. tzacatl was energeti- The 599 hummingbird and 226 bee visits cally worth defending, secondly, whether a to the territory probably represent repeated hummingbird or a bee was energetically worth intrusions by smaller numbers of individuals. pursuing, and finally, whether these intruders However, regardless of the total number of could be considered serious competitors for intruders, my calculations indicate that if each nectar on the territory. of the hummingbird visitors had been allowed The area defended by the Rufous-tailed to forage on the territory until it had filled its Hummingbird was relatively small, and the crop to 5% of capacity, or each of the bee visi- distribution of the inflorescences was such that tors had filled its honey-stomach to 90% of the defending bird appeared to have little dif- capacity, either group would have totally de- ficulty seeing or driving off intruders. Su- pleted two-thirds of the nectar resources avail- crose concentration in Isertia nectar falls with- able on the territory over a three-day period in the range (20-25%) determined by Baker (30,888 ~1). Thus, both hummingbirds and (1975) for hummingbird flowers. The cal- bees appear to represent a serious threat to the culated amount of energy expended by the resources on the territory. In a situation hummingbird in defense and self-maintenance where two intruder groups occur, each with during a 10.3 h period (4565 cal) was much the potential to seriously affect nectar re- less than that available on the territory at the sources, the best defense in energetic terms for start of each day (12,087 cal) (Table 2). a defending hummingbird should be exactly Thus, the distribution, quality and abundance what this Rufous-tailed Hummingbird did, of the resources appear to be such that the i.e. to defend against both hummingbirds and area was energetically worth defending. bees as defense against only one group might The calculations in Table 1 show that an prove futile. average of only 0.75 cal was expended by the I speculate that chasing hummingbirds defender in chasing a bee from the territory should take priority over chasing bees because and 2.16 cal was expended per hummingbird a hummingbird generally forages more effi- chase. By these estimates, a hummingbird ciently than a bee, can remove more nectar stealing only 2 ~1 of nectar (2.34 cal) or a bee per visit than a bee and also may be able to stealing as little as 1 ~1 of nectar (1.17 cal) displace the territory-defender (see Hain- would be worth pursuing. As most humming- sworth and Wolf 1972a, Heinrich 1975a). birds and bees would probably visit many Table 3 gives estimates for the length of florets if allowed to forage undisturbed and time that Rufous-tailed Hummingbirds of dif- could potentially remove 1.5 ~1 of nectar from ferent weights with a full crop of Zsertia hunk- each floret, both types of intruders should be aeanu nectar could exist at Hovering (HMR), worth pursuing. This would be especially true Resting (RMR) and Standard (SMR) Met- if a hummingbird or a bee was able to forage abolic Rates. To arrive at these theoretical on the territory until it filled its crop or values, I assumed 100% utilization of crop- stomach. Under such conditions a humming- storage energy and rates of nectar extraction bird could potentially remove a maximum of by A. tzacatl at flowers of I. hankaeana simi- 684 ~1 (803 cal) and a bee a maximum of 100 lar to those measured by Wolf et al. (1972) for Pl (117 Cal). These figures suggest that the A. tzacatl visiting flowers of Heliconia im- potential amount of energy represented in bricata. Foraging times in this table include 220 THOMAS C. BOYDEN

TABLE 3. Theoreticalestimates of the energy value of a full crop of Isertia hankaeuna nectar for A. tzacatl hummingbirds of different weights, and time required to use that amount of nectar at Hovering, Resting, and Standard Metabolic Rates.

Energy Time to value of a Time Time Time fill crop HMR atHMR RMR at RMR SMR at SMR (min)c (cal/h)e (h) (cal/h)f (h) (lxl/h)~ (h) 4.5 .638 2.46 749.0 967.5 0.77 101.5 65.4 11.45 5.0 .684 2.63 803.0 1075.0 0.75 106.7 70.8 11.34 5.5 .730 2.81 857.0 1182.5 0.72 111.3 7.7 75.8 11.30 6.0 .776 2.99 911.0 1290.0 0.71 116.2 7.8 80.8 11.27 n Weights approximate those measured for A. tzacatl by Wolf et al. 1972 (4.3-6.1 g, %= 5.0 g). b Calculated as in Hainsworth and Wolf (1972a). CCalculated by using the equation for nectar extraction efficiency of A. tzacatl at Heliconiaimbricata (Wolf et al. 1972). d Based on B nectar concentration of 0.87M by weight = 1174 cal/ml. e Based on an energy expenditure of 215 ml/g/h. f Calculated by using the equation of Herreid and Kessel ( 1967) relating thermal conductance to body weight and as- suming a constant body temperature of 41°C and an ambient temperature of 30°C (seealso Hainsworth and Wolf 1972a). p Calculated from the equation for SMR for nonpasserines,Lasiewski and Dawson (1967). only time when a bird had its bill inserted in- energy in nectar that these visitors could po- to a corolla, not hovering time between flow- tentially steal from the territory indicate both ers, as do the values in Table 2. The weights types of intruders to be worth pursuing. The of birds approximate the range measured by defenders’ behavior when chasing humming- Wolf et al. (1972) for A. txacatl. birds differed from that when chasing bees. The values in Table 3 demonstrate the pre- Hummingbird chases were more frequent, sumed adaptive advantages of defending or longer, and consequently, required significant- robbing a territory. A defending individual of ly greater energy expenditures than bee A. tzacatl weighing 5 g can obtain enough chases. The observations on Amuxilia and energy in 2.63 min of foraging on its territory Chalybura hummingbirds presented here also to survive for 45 min at HMR, 7.5 h at RMR, support the conclusion that insect chases by or 11.3 h at SMR. Similarly, another individ- hummingbirds may occur with greater regu- ual with the same weight may obtain enough larity and frequency than previously suspected calories in 15 s of feeding on another birds’ and may represent an important component territory to survive 4 min at HMR, 41 min at of defense against competitors at some types RMR or 62 min at SMR. of feeding territories.

SUMMARY ACKNOWLEDGMENTS Data presented here on a single Rufous-tailed I would like to express my gratitude to N. G. Smith Hummingbird ( Amazilia tzmxztl) defending a and A. S. Rand for their advice and support of all aspects of this study. C. Steele provided invaluable feeding territory from hummingbirds and in- assistance in the fieldwork. R. L. Dressler assisted sects correlate quite well with predictions of in the identification of bees. R. Blankenship and optimal‘ behavior ’ based on time and energy M. Hodgson typed the manuscript. B. J. D. Meeuse, considerations. The majority of time spent D. R. Paulson, J. S. Edwards, G. H. Orians, T. W. in defense was in chasing hummingbird intru- Schoener, N. Waser, F. G. Stiles, L. L. Wolf and V. Gunderson were all kind enough to read the manu- ders. Less time was spent chasing large bees script and offer helpful comments and criticisms. and butterflies; small bees and butterflies were This work was supported by a fellowship from the not chased from the territory. The amount of Smithsonian Tropical Research Institute, Balboa, time spent chasing different types of intruders Canal Zone. appeared to correspond to their size and hence to the potential threat that they posed to the LITERATURE CITED territory in terms of depletion of nectar re- BAKER, H. G. 1975. Sugar concentrations in nec- sources and displacement. tars from hummingbird flowers. Biotropica 7: My calculations indicate that the territory 37-41. occupied by the hummingbird was worth de- HAINSWORTH, F. R., AND L. L. WOLF. 1972a. Crop volume, nectar concentration, and hummingbird fending because the average amount of energy energetics. Comp. Biochem. Physiol. 42:359- available there at the beginning of each day 366. was approximately three times the amount HAINSWORTH, F. R., AND L. L. WOLF. 197213. Power used by the bird during 10.3 h of active de- for hovering flight in relation to body size in hummingbirds. Am. Nat. 106:589-596. fense. Comparisons of the amount of energy HEINRICH, B. 1975a. Energetics of pollination. expended by the defender in chasing hum- Annu. Rev. Ecol. Syst. 6:139-170. mingbirds and large bees, and the amount of HEINRICH, B. 197513. The role of energetics in TERRITORIAL DEFENSE BY TROPICAL HUMMINGBIRDS 221

bumblebee-flower interrelationships. In: Co- problems in North American hummingbirds. evolution of animals and plants. Univ. of Texas Condor 44: 189-204. Press, Austin. PRIMACK, R. B., AND H. F. HOWE. 1975. Inter- HERREID, C. F., AND B. KESSEL. 1967. Thermal ferencc competition between a hummingbird conductance in birds and mammals. Comp. Bio- ( Amazilia tzacatl) and skipper butterflies (Hes- them. Physiol. 21:405-414. periidae). Biotropica 7:55-58. LASIEWSKI, R. C. 1963. Oxygen consumption of STILES, F. G., AND L. L. WOLF. 1970. Humming- torpid, resting, active, and flying hummingbirds. bird territoriality at a tropical flowering tree. Physiol. Zool. 36: 122-140. Auk 87:467-491. LASIEW~KI, R. C., AND W. R. DAWSON. 1967. A re- WOLF, L. L., F. R. HAINSWORTH, AND F. G. STILES. examination of the relation between standard 1972. Energetics of foraging: rate and effi- metabolic rate and body weight in birds. Con- ciency of nectar extraction by hummingbirds. dor 69: 13-23. Science 176: 1351-1352. LYON, D. L. 1974. Territorial and feeding activity of Broad-tailed Hummingbirds (Selasphorus platycercus) in Iris missouriensis. Condor 75: Department of Botany, University of Washington, 346-349. Seattle, Washington 98195. Accepted for publication PITELKA, F. A. 1942. Territoriality and related 23 June 1976.