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Some aspects of the economics of territoriality in North American hummingbirds Armstrong, Doug P. 1986

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SOME ASPECTS OF THE ECONOMICS OF TERRITORIALITY IN NORTH AMERICAN HUMMINGBIRDS by DOUG P. ARMSTRONG B.Sc. University of Guelph, 1983 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE in THE FACULTY OF GRADUATE STUDIES (Department of Zoology) We accept this thesis as conforming to the required standard THE UNIVERSITY OF BRITISH COLUMBIA February 1986 © Doug P. Armstrong, 1986 In presenting t h i s thesis i n p a r t i a l f u l f i l m e n t of the requirements for an advanced degree at the University of B r i t i s h Columbia, I agree that the Library s h a l l make i t f r e e l y available for reference and study. I further agree that permission for extensive copying of t h i s thesis for scholarly purposes may be granted by the head of my department or by his or her representatives. I t i s understood that copying or publication of t h i s thesis for f i n a n c i a l gain s h a l l not be allowed without my written permission. Department of ZoOLOG-V  The University of B r i t i s h Columbia 1956 Main Mall Vancouver, Canada V6T 1Y3 Date FEBROARV 2Ht i i A B S T R A C T T e r r i t o r i a l i t y o f p o s t - b r e e d i n g N o r t h A m e r i c a n h u m m i n g b i r d s i s o n e o f t h e c l e a r e s t e x a m p l e s o f e n e r g y - b a s e d f e e d i n g t e r r i t o r i a l i t y , a n d h a s p l a y e d a n i m p o r t a n t r o l e i n t h e f o r m u l a t i o n a n d t e s t i n g o f t h e o r i e s o n t e r r i t o r i a l i t y . T h i s t h e s i s f o l l o w s t w o l i n e s o f i n q u i r y . F i r s t , w h a t s p e c i a l f o r a g i n g s t r a t e g i e s a r e u s e d b y h u m m i n g b i r d s h o l d i n g e n e r g y -b a s e d f e e d i n g t e r r i t o r i e s ? S e c o n d , a r e e n e r g y - b a s e d m o d e l s a p p l i c a b l e t o t e r r i t o r i a l i t y o f b r e e d i n g a s w e l l a s n o n - b r e e d i n g h u m m i n g b i r d s ? I u s e a s i m u l a t i o n m o d e l t o e x a m i n e t h e p o s s i b l e b e n e f i t s f o r a n o n - b r e e d i n g t e r r i t o r i a l h u m m i n g b i r d o f a v o i d i n g r e c e n t l y v i s i t e d l o c a t i o n s w h i l e f o r a g i n g . T h e s i m u l a t i o n r e s u l t s s u g g e s t t h a t w h i l e b i r d s m i g h t b e n e f i t b y a v o i d i n g f l o w e r s v i s i t e d r e c e n t l y d u r i n g a f o r a g i n g b o u t , t h e y w o u l d n o t b e n e f i t s i g n i f i c a n t l y b y a v o i d i n g p a t c h e s o f f l o w e r s v i s i t e d o n p r e v i o u s b o u t s . A n i m p o r t a n t b e n e f i t o f s h o r t - t e r m a v o i d a n c e o f f l o w e r s f o r m o d e l b i r d s i s t h a t t h e y c a n e m p t y a l l o r n e a r l y a l l f l o w e r s i n e a c h p a t c h v i s i t e d . T h e y t h e r e f o r e c r e a t e c o a r s e - g r a i n e d p a t t e r n s o f n e c t a r a v a i l a b i l i t y t h a t a r e e a s y t o e x p l o i t l a t e r o n . R e s u l t s o f a f i e l d s t u d y o n b r e e d i n g t e r r i t o r i a l i t y o f m a l e C a l l i o p e H u m m i n g b i r d s i n d i c a t e t h a t a s o l e l y e n e r g y - b a s e d m o d e l o f t e r r i t o r i a l i t y c a n n o t a c c o u n t f o r t h e b e h a v i o r o f t h e s e m a l e s . T h r o u g h o u t t h e 2 m o n t h b r e e d i n g s e a s o n , f l o w e r s a m p l i n g i n d i c a t e d t h a t m a l e s c o u l d h a v e o b t a i n e d e n e r g y f a s t e r b y f o r a g i n g o n n e a r b y u n d e f e n d e d a r e a s t h a n b y f o r a g i n g o n t h e i r t e r r i t o r i e s . During June, flowers blooming on the t e r r i t o r i e s were sparse and/or contained very l i t t l e nectar, and males could not have obtained enough energy from them even to compensate for the cost of hovering while foraging. Consequently, they did v i r t u a l l y a l l their foraging away from their t e r r i t o r i e s at that time. During May, when nectar a v a i l a b i l i t y on the t e r r i t o r i e s was at i t s peak, males did not leave, expand, or s h i f t their t e r r i t o r i e s in response to experimental exclosure of a l l flowers blooming on them. I develop a model of optimal t e r r i t o r y size for a promiscuously breeding male that defends a breeding t e r r i t o r y containing no energy sources, as did the Calliope males during June at my study s i t e . This model i s analogous in design to exist i n g models of energy-based feeding t e r r i t o r i a l i t y , but i s based on the premise that a male's optimal t e r r i t o r y size i s that which maximizes his immediate reproductive success. A prediction of t h i s model i s that a male's t e r r i t o r y size w i l l be limited by the rate at which he can obtain energy while foraging away from his t e r r i t o r y . An experiment performed on a Calliope male's t e r r i t o r y did not support t h i s prediction, and suggested that the size of his t e r r i t o r y may have been limited only by his a b i l i t y to detect intruders. i v T A B L E OF CONTENTS A B S T R A C T i i L I S T OF T A B L E S v i L I S T OF F I G U R E S v i i ACKNOWLEDGEMENTS i x C h a p t e r 1 G E N E R A L INTRODUCTION 1 C h a p t e r 2 FORAGING S T R A T E G I E S FOR NECTARIVOROUS B I R D S HOLDING F E E D I N G T E R R I T O R I E S 7 T h e M o d e l 14 F l o w e r d i s t r i b u t i o n a n d n e c t a r p r o d u c t i o n 16 H u m m i n g b i r d e n e r g e t i c s 18 F o r a g i n g t a c t i c s 19 S i m u l a t i o n R e s u l t s 21 A d j u s t i n g t h e p a t c h - l e a v i n g r u l e 21 The e f f e c t o f n e c t a r p r o d u c t i o n c h a r a c t e r i s t i c s 23 The e f f e c t o f t e r r i t o r y s t r u c t u r e 32 D i s c u s s i o n 35 C h a p t e r 3 ECONOMICS OF B R E E D I N G T E R R I T O R I A L I T Y I N M A L E C A L L I O P E HUMMINGBIRDS 40 S t u d y A r e a 44 P a r t I . P r o f i t a b i l i t y a n d e n e r g y p r o d u c t i o n o f t e r r i t o r i e s 51 M e t h o d s 51 Results 57 Comparative p r o f i t a b i l i t y of defended and undefended areas 57 Ter r i t o r y energy production and metabolic requirements of birds 64 Discussion 67 Part I I . Responses of males to experimental exclosure of t e r r i t o r y nectar sources 69 Methods 69 Results 70 Discussion 72 Chapter 4 WHAT DETERMINES THE SIZES OF BREEDING TERRITORIES HELD BY MALE CALLIOPE HUMMINGBIRDS? 78 The Model 80 Access to females 80 Cost of defense 81 Methods 83 Results 86 Discussion 90 Chapter 5 CONCLUDING REMARKS 96 Literature Cited 100 v i LIST OF TABLES Table 3 . 1 . Flower v i s i t a t i o n rates by male Calliope Hummingbirds on 4 plant species 60 Table 3 . 2 . Total number of flowers censused on t e r r i t o r i e s during each week in June 61 LIST OF FIGURES Figure 2.1. Flowchart representation of the model 15 Figure 2.2. Energy reserves of model birds at the end of the day as a function of patch-leaving rules, and of patch and flower memories 22 Figure 2.3. The influence of nectar production rate on foraging e f f o r t of model birds 25 Figure 2.4. The eff e c t of memory on the a b i l i t y of model birds to accumulate energetic reserves 27 Figure 2.5. The ef f e c t of temporal d i s t r i b u t i o n of nectar production on the minimum t o t a l production required to support model birds with no memory and perfect memory .. 29 Figure 2.6. The influence of nectar production rate on foraging e f f o r t when empty flowers reach a volume threshold in 4 hours ' 30 Figure 2.7. The eff e c t of a flower volume threshold on the minimum nectar production rate required to support model birds with no memory and perfect memory 31 Figure 2.8. The r e l a t i v e u t i l i t y of patch memory and flower memory 34 Figure 3.1. Positions of t e r r i t o r i e s 1 through 6 on 1 June 1985 45 Figure 3.2. Phenology of t e r r i t o r i a l i t y in the meadow, and approximate timing of reproductive a c t i v i t i e s 47 Figure 3.3. Nectar volumes of flowers blooming on and off v i i i t e r r i t o r i e s over the course of the breeding season 58 Figure 3.4. Concentration of nectar in flowers blooming on and off t e r r i t o r i e s 59 Figure 3.5. Comparative p r o f i t a b i l i t y of flowers blooming on and off t e r r i t o r i e s 62 ~, Figure 3.6. Estimated d a i l y energy production on t e r r i t o r i e s 65 Figure 3.7. Estimated proportion of dail y nectar production removed by insects 66 Figure 3.8. Changes in positions and sizes of t e r r i t o r i e s throughout May 71 Figure 3.9. Changes in time budgets of males in response to exclosure of Ribes bushes on their t e r r i t o r i e s 73 Figure 4.1. Design of experiment to examine the effect of energy a v a i l a b i l i t y on t e r r i t o r y size 84 Figure 4.2. Comparison of t e r r i t o r y defense when the male did and did not have access to an a r t i f i c i a l feeder outside his t e r r i t o r y 87 Figure 4.3. Changes in the behavior of t e r r i t o r y owner when he had access to a feeder 89 ix ACKNOWLEDGEMENTS I wish to thank my supervisor Lee Gass for his generous share of time, enthusiasm, and f i n a n c i a l support over the past 2 1/2 years. Steve Paton, Staffan Tamm, Glenn Sutherland, and Gayle Brown a l l contributed to making the Vivarium a supportive, generally pleasant, and suitably s i l l y research atmosphere. Lee G., Don Ludwig, Jamie Smith, and Judy Myers read an e a r l i e r draft of t h i s thesis, and offered a number of useful suggestions. One or more chapters were also reviewed by Steve P., Staffan T., Glenn S., Peter Arcese, Lynn Carpenter, Steve Lima, Diana Tomback, David Paton, Graham Pyke, and Ron Pulliam. Don L. And Peter Schumaker offered s t a t i s t i c a l advice. Si and Doreen Sieben provided l o g i s t i c support in the f i e l d in the form of cookies, lemonade, and rides into Keremeos. This research would never have been conducted i f not for the enthusiasm for ecology imparted to me at the University of Guelph by Dave Lavigne, Dave Noakes, E.H. Anthony, and especially Tom Nudds and Ron Brooks. This research was ultimately made possible by the tolerance of B. White, R. Black, and G. Green to my intrusions into their private l i v e s ; I wish to thank them for their interesting responses. Fi n a n c i a l support was provided by an NSERC Postgraduate Scholarship, a University of B r i t i s h Columbia Graduate Fellowship, and NSERC grant 67-9876 to C L . Gass. 1 CHAPTER 1 GENERAL INTRODUCTION Hummingbirds (Trochilidae) are a diverse family of at least 319 species (Johnsgard 1983), a l l found in North, Central, and South America. These birds are characterized by their extensive use of f l o r a l nectar as an energy source, and by a series of morphological, physiological, and behavioral c h a r a c t e r i s t i c s that are interpreted as adaptations to nectar feeding. Three other families of birds depend extensively on f l o r a l nectar: sunbirds (Nectariniidae), honeycreepers (Drepanididae), and honeyeaters (Meliphagidae). However, none of these exhibit the same degree of s p e c i a l i z a t i o n associated with nectar feeding that hummingbirds do. Adaptations of hummingbirds to nectar feeding, and of ornithophilous plants to bird-mediated p o l l i n a t i o n , have made this relationship a valuable one for the study of plant/animal coevolution (Grant and Grant 1968; S t i l e s 1978; Brown and Kodric-Brown 1979; Waser 1978; Feinsinger 1983). The great d i v e r s i t y of both hummingbirds and their food plants in t r o p i c a l America has stimulated considerable interest in the structure of hummingbird/plant communities (Wolf et a l . 1976; Feinsinger 1976,1978a,1978b; Feinsinger and Colwell 1978; Feinsinger et a l . 1985; Brown and Bowers 1985). As well, the unique c h a r a c t e r i s t i c s of hummingbirds that f a c i l i t a t e nectar exploitation a f f e c t many aspects of their biology beyond the bird/plant r e l a t i o n s h i p . 2 The most obvious c h a r a c t e r i s t i c of hummingbirds i s their small s i z e . Individual species range from the Cuban Bee Hummingbird (Mellisuga helenae), which probably averages s l i g h t l y less than 2 g, to the Giant Hummingbird (Patagonia  gigas), which averages 20.2 g (Brown and Bowers 1985). The median weight of 191 species l i s t e d by Brown and Bowers (1985) was 5.0 g. Their small size, in combination with proportionately large breast muscles, high muscle mitochondrial density, and specialized wing anatomy (Greenewalt 1960, 1975), allows hummingbirds to hover motionless in f l i g h t . Hovering, in turn, allows them to exploit a wide variety of flowers that would be unavailable to birds that perched while foraging. No other birds, including those of the three other nectarivorous families, are capable of sustained hovering. As a consequence of their small size, hummingbirds have metabolic rates that are higher than those of any other vertebrates except for some shrews (Johnsgard 1983). Therefore, their oxygen consumption, energy u t i l i z a t i o n , and thermoregulation have been of p a r t i c u l a r interest to comparative physiologists (Pearson 1950; Lasiewski 1963; Lasiewski and Dawson 1967; Calder and King 1974; Hainsworth 1974). Si m i l a r l y , energy regulation by hummingbirds in their natural environments has been of inte r e s t , p a r t i c u l a r l y during periods of energetic stress induced by nesting, migration, or inclement weather (Pearson 1954; Lasiewski 1962; Calder 1975; Hainsworth and Wolf 1978; Carpenter and Hixon 1985; Tooze and Gass 1985). This energy regulation i s partly achieved by physiological means. 3 However, the behavior of the birds is also c r i t i c a l in insuring that they do not suffer energetic s h o r t f a l l . Hummingbirds' behavior influences both the rates at which they lose energy through metabolic expenditures, and the rates at which they acquire energy from f l o r a l nectar. Energy expenditures depend on the thermal microclimates in which birds reside, and on the a c t i v i t i e s in which they engage. The rates at which birds acquire energy depend both on the foraging strategies they employ, and on the d i s t r i b u t i o n and abundance of available nectar. Birds' foraging strategies dictate their timing of foraging bouts (Hainsworth and Wolf 1983), and their choices as to which individual flowers and/or patches of flowers they v i s i t (Pyke 1978a, 1981; Gass and Montgomerie 1981; Montgomerie et a l . 1984; Stephens and Paton 1986). The p r o f i t a b i l i t y of birds' foraging environments i s at least p a r t i a l l y a consequence of factors beyond their control, such as the nectar production rates of flowers. Birds can, however, influence t h i s p r o f i t a b i l i t y by defending nectar resources from competitors. There are at least two reasons why hummingbirds should sometimes defend energy sources. F i r s t , because of their rapid metabolic rates, they may run a high r i s k of energetic s h o r t f a l l , so that they need constant access to energy sources. Second, because flowers are stationary and conspicuous, they are easier to defend than other types of food sources. Among North American species, t e r r i t o r i e s are defended by adult males during the breeding season ( S t i l e s 1970, and references within), and by 4 males, females, and juveniles outside the breeding season, p a r t i c u l a r l y during migration (Pitelka 1951; Armitage 1955; S t i l e s 1970; Paton and Carpenter 1984, and references within). In almost a l l cases, these t e r r i t o r i e s contain nectar producing flowers on which the owners feed. T e r r i t o r i a l i t y of non-breeding hummingbirds is one of the clearest examples of energy-based feeding t e r r i t o r i a l i t y (Davies and Houston 1984). The presence or absence of t e r r i t o r y defense by non-breeding Anna's Hummingbirds (Calypte anna) at s p e c i f i e d s i t e s can be dictated by manipulation of energy a v a i l a b i l i t y (Ewald and Carpenter 1978; Ewald 1980), and the sizes of t e r r i t o r i e s defended by migrating Rufous Hummingbirds (Selasphorus rufus) are c l o s e l y related to the density and energy production of the flowers they contain (Gass et a l . ^ 1976; Gass 1979; Kodric-Brown and Brown 1978; Montgomerie and Gass 1981; Hixon et a l . 1983). Consequently, hummingbird t e r r i t o r i a l i t y has played an important role in the formulation and testing of recent models of t e r r i t o r i a l i t y (Schoener 1983; Hixon et a l . 1983; Lima 1984, 1986; Jones and Krummel 1985). This thesis follows up t h i s work on hummingbird t e r r i t o r i a l i t y with two l i n e s of inquiry. Chapter 2 suggests some special foraging strategies for animals holding feeding t e r r i t o r i e s , and uses a simulation model to predict whether or not these strategies should be used by t e r r i t o r i a l hummingbirds. Chapters 3 and 4 report the results of an empirical study addressing the issue of whether or not energy-based models are applicable to breeding as well as non-breeding t e r r i t o r i a l i t y in 5 hummingbirds. The model in Chapter 2 i s based on t e r r i t o r i e s of postbreeding migratory Rufous Hummingbirds in C a l i f o r n i a (Gass and Sutherland 1985), and i s used to evaluate the benefits to a t e r r i t o r i a l hummingbird of avoiding recently v i s i t e d locations. Because birds e f f e c t i v e l y defend their t e r r i t o r i e s against intruders, their own foraging may account for a large proportion of the s p a t i a l v a r i a t i o n in nectar a v a i l a b i l i t y among flowers. The simulation results suggest that while birds might benefit by avoiding flowers v i s i t e d recently during a foraging bout, they would not benefit s i g n i f i c a n t l y by avoiding patches of flowers v i s i t e d on previous bouts. This chapter i s currently in press as Armstrong et a l . (1986). Chapter 3 examines whether an energy-based model can account for t e r r i t o r i a l i t y of a group of breeding male Calliope Hummingbirds ( S t e l l u l a c a l l i o p e ) in the i n t e r i o r of B r i t i s h Columbia. Several descriptive studies have compared breeding and non-breeding t e r r i t o r i e s held by male North American hummingbirds, and have suggested possible differences between them (Pitelka 1951; Legg and Pitelka 1956; Williamson 1956; S t i l e s 1970, 1971). However, rigorous empirical work. on hummingbird t e r r i t o r i a l i t y has so far been confined to the non-breeding season, at which time the immediate reproductive success of birds i s not a confounding factor. Chapter 3 documents an example of breeding t e r r i t o r i a l i t y that c l e a r l y cannot be accounted for solely by energetic considerations. Throughout the 2 month breeding season, flowers blooming on the 6 t e r r i t o r i e s were less p r o f i t a b l e than those on nearby undefended areas. In May, when nectar a v a i l a b i l i t y on the t e r r i t o r i e s was at i t s peak, males did not leave, expand, or s h i f t their t e r r i t o r i e s in response to experimental exclosure of a l l flowers on those t e r r i t o r i e s . Chapter 4 develops a model of optimal t e r r i t o r y size for breeding males based on maximization of immediate reproductive success. This model, which applies to t e r r i t o r i e s with no food resources, suggests that the optimal sizes of t e r r i t o r i e s defended by males are influenced by the rates at which they can obtain energy while foraging away from their t e r r i t o r i e s . An experiment using one t e r r i t o r i a l male did not support t h i s hypothesis, but did suggest that the male became more successful at expelling intruders when provided with an a r t i f i c i a l feeder away from his t e r r i t o r y . On the basis of t h i s observation, I suggest that access to energy may influence the reproductive success of males i f i t a f f e c t s their a b i l i t i e s to es t a b l i s h and hold t e r r i t o r i e s . 7 CHAPTER 2 FORAGING STRATEGIES FOR NECTARIVOROUS BIRDS HOLDING FEEDING TERRITORIES If food resources are l i m i t e d , animals must concentrate t h e i r f o r a g i n g e f f o r t i n areas i n which food i s most a v a i l a b l e i f they are to meet t h e i r e n e r g e t i c and n u t r i t i o n a l requirements. Because the s p a t i a l d i s t r i b u t i o n of t h e i r food resources changes over time, animals may need to s h i f t the s p a t i a l d i s t r i b u t i o n of t h e i r f o r a g i n g . Such s h i f t s i n c l u d e seasonal m i g r a t i o n s spanning vast d i s t a n c e s , but a l s o i n c l u d e short term changes i n a l l o c a t i o n of f o r a g i n g e f f o r t w i t h i n a s i n g l e animal's home range. The s p a t i a l d i s t r i b u t i o n of food i n an animal's home range at any time may p a r t i a l l y r e f l e c t that animal's own a c t i v i t y . Caching behavior, such as that observed i n granivorous rodents and b i r d s , i s an obvious example of animals i n f l u e n c i n g t h e i r food d i s t r i b u t i o n s . However, f o r a g i n g i t s e l f may a l s o a l t e r the d i s t r i b u t i o n , as w e l l as the abundance, of a v a i l a b l e food. When an animal f o r a g e s , i t may cause s i g n i f i c a n t l o c a l d e p r e s s i o n s i n food a v a i l a b i l i t y , and thus the s p a t i a l d i s t r i b u t i o n of i t s food resources may r e f l e c t i t s recent f o r a g i n g h i s t o r y . Given that seed caching t i t s and n u t c r a c k e r s can remember l o c a t i o n s of s e v e r a l hundred seed caches ( S h e t t l e w o r t h 1983), i t seems i n t u i t i v e l y reasonable that at l e a s t some animals might be 8 adept at remembering and avoiding foraging locations that they have recently depleted. As well, i t i s possible that foragers could remember recently v i s i t e d "locations" on more than one spatiotemporal scale (Gass and Montgomerie 1981). Food items are often d i s t r i b u t e d in patches within an animal's home range, and thus an animal might maintain a r e l a t i v e l y long term memory of the last several patches i t has v i s i t e d . While foraging in a patch, i t might maintain a short term memory of which b i t s of that patch i t has already v i s i t e d . A b i t refers to a portion of a patch that may or may not contain a single discrete quantity of food (Green 1984). A b i t , therefore, cannot be further sub-divided, and a forager cannot v i s i t less than a whole b i t . A forager with memory on both of these spatiotemporal scales could be said to have cognit ive maps (Menzel and Wyers 1981) of both the patches in i t s home range and the b i t s in the patch in which i t i s currently foraging. These cognitive maps would consist of the forager's a p r i o r i expectations (Hainsworth and Wolf 1979; Lima 1983) of the amount of food available in individual b i t s , and of the quality of whole patches. If a forager expects that locations i t has v i s i t e d recently w i l l be depleted or nearly depleted, i t should p r e f e r e n t i a l l y v i s i t other locations. If i t does so, i t s pattern of v i s i t i n g locations w i l l be systematic (Kamil 1978). That i s , the number of b i t s r e v i s i t e d per patch w i l l be smaller and the average time in t e r v a l between r e v i s i t s to patches w i l l be longer than would be expected by chance. Although systematic v i s i t a t i o n may be a consequence of a 9 forager maintaining a cognitive map, i t could also be accomplished without such a map. Systematic v i s i t a t i o n both within.and among patches could be achieved by a forager that had no expectations about food a v a i l a b i l i t y i f i t were an e f f i c i e n t  harvester (Pyke 1978b). An e f f i c i e n t harvester i s a forager that sequences i t s foraging movements in such a way that i t rarely crosses i t s path, and therefore generally encounters locations in which food has been replenished since i t s last v i s i t . The common c h a r a c t e r i s t i c shared by e f f i c i e n t harvesters and foragers that maintain cognitive maps i s that they can avoid depleted patches or bi t s of patches prior to encountering them. Consequently, I w i l l , for the sake of brevity, refer to either type of forager as having "memory". Because a forager could not, by d e f i n i t i o n , v i s i t a sub-component of a b i t , any discrimination between depleted and non-depleted b i t s of a patch must be done a p r i o r i , • and therefore constitute " b i t memory". In contrast, a forager could either avoid a patch a p r i o r i ("patch memory"), or choose to leave that patch a p o s t e r i o r i i f i t s i n i t i a l rate of food intake were low. A forager that used only an a p o s t e r i o r i patch-leaving rule, such as the giving-up time rule (Krebs et a_l. 1974; McNair 1982; Ydenberg 1984), might encounter recently v i s i t e d patches frequently. However, i f i t s rule were e f f e c t i v e , i t might spend only a short amount of time in such patches before moving on to new ones. Nevertheless, memory could be b e n e f i c i a l to a forager even i f i t did use an e f f e c t i v e patch-leaving rule. Patch memory could save time spent traveling to depleted patches, and 10 time spent v i s i t i n g empty or nearly empty b i t s before leaving those patches. Bit memory could save time spent r e v i s i t i n g b i t s of the patch in which i t i s currently foraging. Whether or not a forager should use either type of memory depends on whether those benefits outweigh any associated costs. Regardless of whether memory i s achieved by maintaining a cognitive map or by harvesting e f f i c i e n t l y , i t w i l l require storage and processing of information. A long term cost of memory would be involved i f t h i s storage and processing required the animal to maintain additional neural capacity not required for other aspects of i t s behavior. A short term cost would be involved i f t h i s storage and processing reduced the speed and/or accuracy of other functions the animal must perform simultaneously (Gass 1985). For example, i t might become less observant of potential predators (Milinski 1984; Lawrence 1985) or other aspects of i t s environment. It i s l i k e l y that the magnitude of the benefits of memory, and therefore the l i k e l i h o o d that they w i l l exceed the costs, w i l l depend on the c h a r a c t e r i s t i c s of the p a r t i c u l a r animal. I expect that the benefits are most l i k e l y to be s i g n i f i c a n t i f the animal has the following c h a r a c t e r i s t i c s . 1. Its foraging creates l o c a l resource depressions. This can happen i f the animal's rate of food intake i s high in r e l a t i o n to the rate of renewal of i t s food resources. 11 2. Its foraging i s concentrated within a r e l a t i v e l y small home range, so that there is a reasonably high pro b a b i l i t y of returning to a recently depleted area. 3. It maintains f a i r l y exclusive use of food resources in i t s home range, so that i t s own foraging accounts for a large proportion of food removed. 4. It exploits food resources that are f a i r l y immobile. Otherwise, there may be a constant influx of these resources into recently depleted areas from areas of higher abundance. The f i r s t three c h a r a c t e r i s t i c s may be shared, at least to some degree, by a variety of animals that hold feeding t e r r i t o r i e s . However, a group of t e r r i t o r i a l foragers that f i t s the above c h a r a c t e r i s t i c s p a r t i c u l a r l y well i s that composed of members of the four families of nectarivorous birds: hummingbirds, sunbirds, honeycreepers, and honeyeaters. T e r r i t o r i e s of both sunbirds ( G i l l and Wolf 1975) and hummingbirds (Gass et_ a l . 1976; Gass 1979; Kodric-Brown and Brown 1978; Hixon et a l . 1983) contain just enough nectar to support the birds' d a i l y energetic requirements. In a l l cases, birds vigorously defend their t e r r i t o r i e s from intruders, and obtain t h e i r energy from immobile flowers. It has already been found that r e v i s i t s to inflorescences by sunbirds ( G i l l and Wolf 1977) and hummingbirds (Sutherland, in prep.) and r e v i s i t s to flower clu s t e r s by honeycreepers (Kamil 1978) occur less often 12 than would be expected by chance. It isn't clear to what extent th i s i s a result of memory, and to what extent i t i s a result of birds making a p o s t e r i o r i decisions to leave depleted patches of inflorescences or flower c l u s t e r s . G i l l and Wolf (1977) found that sunbirds appeared to be harvesting in that they tended to forage at d i f f e r e n t heights on successive foraging bouts. However, no evidence of harvesting was found for either honeycreepers or hummingbirds. I know of no studies that have d i r e c t l y tested the p o s s i b i l i t y that birds avoid r e v i s i t s on any spatiotemporal scale by maintaining a cognitive map. In t h i s paper, I use a simulation model to predict the nature and extent of the benefits of memory for a t e r r i t o r i a l hummingbird. I therefore hope to provide a the o r e t i c a l background for future studies that examine whether or to what extent nectarivores or other t e r r i t o r i a l foragers do show memory of previously v i s i t e d locations. I modeled t e r r i t o r i a l hummingbirds s p e c i f i c a l l y rather than t e r r i t o r i a l foragers in general for several reasons. F i r s t , for those reasons given above, memory could be p a r t i c u l a r l y important for hummingbirds and other nectarivorous birds. Second, previous studies of hummingbirds (Pitelka 1942; Gass e_t a l . 1976; Gass 1979; Hixon .1980; Hixon et a l . 1983; Paton and Carpenter 1984) have greatly enhanced our understanding of feeding t e r r i t o r i a l i t y in general, and have revealed these birds to be a convenient experimental system. Third, I could base my assumptions on the extensive data that exist for hummingbirds. A l l parameters and functional "relationships in the model are either based on laboratory or 13 f i e l d data for Rufous Hummingbirds or are interpolated from allometric relationships based on a number of hummingbird species (Montgomerie 1979). Fourth, because the predictions of the model apply to a s p e c i f i c system, they can be e a s i l y compared with results of past or future empirical work on that system. In the discussion, I indicate ways in which my assumptions may not f i t the c h a r a c t e r i s t i c s of other types of t e r r i t o r i a l foragers, and discuss how these deviations might affe c t my predictions. The predictions of the model relate to two possible benefits of memory: 1. A decrease in the amount of time per day a hummingbird must forage in order to meet i t s energetic requi rements. 2. A decrease in the minimum amount of nectar a hummingbird's t e r r i t o r y must produce for i t to meet those requirements. I examine the benefits of both patch memory and flower memory, where flowers correspond to b i t s in the model. I have no information to assess either the short term or the long term costs of maintaining memory, and therefore I cannot d i r e c t l y compare the magnitudes of costs and benefits. I do, however, make q u a l i t a t i v e predictions as to the conditions under which the benefits w i l l be highest, and i n t u i t i v e predictions as to 14 whether these benefits are l i k e l y to exceed the costs. The Model The model simulates a hummingbird foraging in i t s t e r r i t o r y over the course of a single day (Fig. 2.1). I assume that 14 h of the day are available for foraging, and that the rest of the time i s spent sleeping. At dawn, model birds have no fat reserves. Each bird i n i t i a t e s i t s f i r s t feeding bout by f l y i n g from a c e n t r a l l y located perch to any of the patches in i t s t e r r i t o r y . Birds remove a l l nectar from each flower they v i s i t (but see Pyke 1978a; Gass and Montgomerie 1981 for a discussion of decisions made at flowers). Those birds with flower memory are able to avoid r e v i s i t i n g at least some flowers. A l l birds use the same a p o s t e r i o r i patch-leaving rule to determine i f a patch i s depleted; i f a b i r d decides that a patch i s depleted, i t f l i e s to a new patch. Birds with patch memory are able to avoid r e v i s i t i n g at least some patches. Model birds regulate their rates of fat storage by adjusting the length of time they rest between feeding bouts. Bouts always terminate when 40 ul of nectar have been harvested. This volume per bout i s t y p i c a l for captive Rufous Hummingbirds (Sutherland, in prep.). However, bouts vary in the amount of energy required to harvest that nectar, and therefore in net energy intake. At the end of each bout, a bi r d returns to i t s perch, and uses at least part of i t s net energy intake to produce fat which i t stores for the coming night. It remains on i t s perch u n t i l any remaining energy i s used up by i t s resting F ly back to same patch no • Se lec t patch • Fly to patch y e s • Se lec t f l o w e r • F ly to f l o w e r Patch depleted? Drink al l n e c t a r in f l o w e r no <^  4 0 ul ha r ve s t ed ye t ? y>— yes • F ly to perch • S to re fat • Perch unt i l rema in ing ene rgy f r om last bout burned off -<( 14 h y e t ? ^-yes Figure 2.1. Flowchart representation of the model. 16 metabolism, and then i n i t i a t e s a new feeding bout by f l y i n g back to the patch in which i t terminated the la s t bout. If they can, model birds store energy at a rate at which the amount of fat accumulated at the end of the day w i l l meet, but not exceed their expected nocturnal requirements (see Hainsworth e_t a l . 1981). One measure of a model bird's success is whether or not i t i s able to meet th i s energy requirement. Those that cannot do so w i l l have negative 24 h energy budgets. A real hummingbird that could not meet i t s energy requirements over a number of days would need to expand i t s t e r r i t o r y , find a new location, or somehow reduce i t s energy expenditure. Another measure of success i s the amount of time that model birds spend foraging over the course of the day. Among model birds that s a t i s f y t h e i r energy requirements, the most successful are those that minimize the amount of time they spend foraging. The success of a model bird depends on the amount and d i s t r i b u t i o n of nectar in i t s t e r r i t o r y and on the effectiveness of i t s foraging t a c t i c s . Flower d i s t r i b u t i o n and nectar production I based model t e r r i t o r i e s on those held by migrating Rufous Hummingbirds in the G r i z z l y Lake area of northwest C a l i f o r n i a during July and August (Gass et a l . 1976; Gass 1979; Gass and Sutherland 1985). These t e r r i t o r i e s averaged 239 red columbine (Aquilegia formosa) flowers, each of which has 5 nectar producing spurs. Flowers were d i s t r i b u t e d in discrete patches, and t e r r i t o r i e s averaged 406 m2 in area. I use a model 17 t e r r i t o r y of 900 flowers. This number both approximates the number of columbine spurs in a real t e r r i t o r y , and allows f l e x i b i l i t y in d i v i d i n g the t e r r i t o r y into d i f f e r e n t numbers of patches. Flowers can be d i s t r i b u t e d among "coarse-grained" t e r r i t o r i e s of few large patches or "fine-grained" t e r r i t o r i e s of many small patches. In a l l cases, t e r r i t o r i e s are square in shape as are the individual patches. I can also vary both the distance between patches and the density of flowers within patches. Regardless of flower spacing, I assume that patches are discrete and d i s t i n c t to the hummingbird. To examine how model birds' foraging t a c t i c s influence the t o t a l nectar production required to support them, I manipulate the nectar production rate per flower rather then manipulating the number of flowers per t e r r i t o r y . I assume that a l l flowers produce nectar at the same rate (but see Feinsinger 1978a, 1983 for- a discussion of v a r i a b i l i t y in nectar production). The model begins at dusk, at which time a l l flowers are empty. If t o t a l nectar production i s at or below the minimum l e v e l required to support a model bird, flowers are also empty 24 h l a t e r . Because model birds consume a l l nectar produced on their t e r r i t o r i e s when nectar production i s at the minimum l e v e l required to support them, the model could be run for several days at that production l e v e l without nectar accumulating and without birds f a i l i n g to meet their energetic requirements. I also examine the consequences of varying two other c h a r a c t e r i s t i c s of nectar production: 18 1. The proportion of nectar produced nocturnally. A higher nocturnal production rate results in a higher standing crop at dawn. 2. The effect of nectar standing crop on nectar production rates. Some flowers, including columbine, decrease their production rates as they f i l l (CA. Redsell, C L . Gass, R.D. Montgomerie, unpublished observations). I simulate t h i s by stopping nectar production at a threshold accumulated volume (equivalent to a threshold f i l l i n g time). I assume that a l l nectar i s 35% sucrose by weight which i s t y p i c a l for columbine (Gass 1974). Hummingbird energetics A l l model birds have i d e n t i c a l energetic requirements. I assume that birds have a constant body weight of 3.5 g, that the temperature i s a constant 15°C, and that the a l t i t u d e i s 2400 m. Using these values, wing morphology measurements from captive Rufous Hummingbirds (Tooze 1984), and Montgomerie's (1979) equations, I estimated that hovering, f l y i n g forward, perching, and sleeping would cost 1.0 Watts (W), 0.5 W, 0.25 W, and 0.125 W, respectively. Duration of forward f l i g h t s i s given by t = 0.80 + 0.11d (Gass 1974), where t i s time (s) and d i s Euclidean distance flown (m) in the model array. Time spent hovering at each flower i s given by t = 1.22 + 0.12v, where v i s nectar 19 volume ( u l ) . T h i s r e l a t i o n s h i p approximates the time r e q u i r e d to handle a columbine spur .(Gass and Sutherland 1985). The i n t e r c e p t i s the time r e q u i r e d f o r a b i r d to p o s i t i o n i t s e l f , and to i n s e r t and withdraw i t s b i l l . T h e r e f o r e , v i s i t s to empty or n e a r l y empty flowers c o s t at l e a s t 1.22 s of hovering time and energy i n a d d i t i o n to t r a v e l c o s t s . Given that s l e e p i n g c o s t s 0.125 W and n i g h t s are 10 h long, model b i r d s need 4.5 kJ worth of f a t to l a s t the n i g h t . I assume t h a t b i r d s spend the whole night s l e e p i n g , and do not become t o r p i d . T h e r e f o r e , i f they are to maintain n e u t r a l 24 h energy budgets, they must harvest enough nectar so that t h e i r net energy gain averages 0.089 W f o r the 14 h they can forage. I assume that c o n v e r s i o n of energy from sugar to f a t i s 100% e f f i c i e n t . T h e r e f o r e , as long as a b i r d ' s net r a t e of energy intake d u r i n g f e e d i n g bouts always exceeds 0.089 W, i t w i l l meet i t s n o c t u r n a l energy requirement. The amount by which a b i r d ' s r a t e of intake exceeds 0.089 W determines the l e n g t h of time i t perches b e f o r e the next bout. I f that r a t e does not exceed 0.089, the b i r d spends 100% of i t s time f o r a g i n g . Foraging t a c t i c s P a t c h - l e a v i n g r u l e . A l l model b i r d s use an a p o s t e r i o r i p a t c h - l e a v i n g r u l e . That i s , they decide when to leave- each patch on the b a s i s of t h e i r nectar i n t a k e r a t e w i t h i n that patch. I f e l t t h a t t h i s was a reasonable assumption s i n c e a wide v a r i e t y of animals have been shown to use t h e i r experience w i t h i n patches to decide when to leave them (Krebs et a l . 20 1983). I assume that a bird w i l l leave a patch i f i t s rate of nectar intake in that patch drops below some givinq-up  threshold. Each bird monitors i t s rate of intake by averaging the nectar volumes i t has obtained from the la s t few flowers v i s i t e d . Cowie (1977) referred to this type of sample as a "memory window"; however, I w i l l use the term sampling window to avoid confusion with patch memory and flower memory. Whenever the average f a l l s below the giving-up threshold, a bi r d moves to another patch. For s i m p l i c i t y , I assume that both the giving-up threshold and the size of the sampling window are constant over the course of the day. Patch memory and flower memory. I wished to examine the benefits of memory, regardless of whether i t involved maintaining a cognitive map or e f f i c i e n t harvesting. However, a complication of the l a t t e r mechanism i s that an animal's foraging route may also influence i t s ov e r a l l tr a v e l costs (Anderson 1983). I wished to manipulate model birds' memories without a l t e r i n g t r a v e l costs. Therefore, in the model, birds with patch and flower memory maintain cognitive maps that indicate those individual locations they have v i s i t e d most recently. They select patches and flowers at random, excluding from consideration those they can remember v i s i t i n g . Perfect patch memory equals one less than the number of patches in the t e r r i t o r y . Therefore, birds with perfect memory v i s i t patches in the same sequence repeatedly. S i m i l a r l y , perfect flower memory equals one less than the number of flowers per patch. I assume that birds retain their memory of flowers in a patch only 21 u n t i l t h ey v i s i t a n o t her p a t c h . However, when a b i r d i n i t i a t e s a new f e e d i n g bout a f t e r p e r c h i n g , i t r e t u r n s t o the p a t c h i n which i t ended the l a s t bout and r e t a i n s i t s memory of the f l o w e r s i n t h a t p a t c h . Because model b i r d s do not choose new pat c h e s or f l o w e r s w i t h r e s p e c t t o t h e i r c u r r e n t l o c a t i o n s , the average t r a v e l time between p a t c h e s and between f l o w e r s w i t h i n p a t c h e s i s not a f f e c t e d by changes i n f o r a g i n g t a c t i c s . The b e n e f i t s of memory a r e t h a t they save time and energy spent f l y i n g t o d e p r e s s e d p a t c h e s and f l y i n g t o and h a n d l i n g empty or n e a r l y empty f l o w e r s . I e x p l o r e t h e s e b e n e f i t s i n the next s e c t i o n . S i m u l a t i o n R e s u l t s A d j u s t i n g the p a t c h - l e a v i n g r u l e The o p t i m a l c o m b i n a t i o n of g i v i n g - u p t h r e s h o l d and sampl i n g window depends on n e c t a r a v a i l a b i l i t y , s i z e of p a t c h e s , and the model b i r d ' s p a t c h and f l o w e r memory. T h e r e f o r e , I d i d not f e e l t h a t I c o u l d d i r e c t l y compare the s u c c e s s of model b i r d s w i t h d i f f e r e n t memory c a p a c i t i e s under a v a r i e t y of c o n d i t i o n s i f I used a s e t c o m b i n a t i o n . I n s t e a d , f o r each s i t u a t i o n , I found the o p t i m a l p a t c h - l e a v i n g r u l e by i t e r a t i n g t h r o u g h runs of the model, c h a n g i n g the g i v i n g - u p t h r e s h o l d and the s i z e of the sa m p l i n g window by 0.2 u l / f l o w e r and one f l o w e r i n c r e m e n t s r e s p e c t i v e l y ( f o r an example, see F i g . 2 . 2 ) . In t h o s e c a s e s i n which b i r d s c o u l d accumulate the n o c t u r n a l f a t requirement of 4 .5 k J by the end of the day, I 22 N O P A T C H P E R F E C T P A T C H M E M O R Y M E M O R Y Size of Sampling Window (flowers) Stored -2.0 0.0 2.0 40 F a t ( k J ) F i g u r e 2 . 2 . Model b i r d s ' energy r e s e r v e s at the end of the day as a f u n c t i o n of t h e i r p a t c h - l e a v i n g r u l e s , and of t h e i r patch and flower memories. The maximum amount of f a t s t o r e d i s 4 . 5 k J . I f the average nectar volume i n the l a s t few flowers a b i r d has v i s i t e d (the sampling window, or "memory window") i s l e s s than the g i v i n g - u p t h r e s h o l d , i t moves to a new patch. In t h i s p a r t i c u l a r example, each flower produces 4 . 3 ul/day at a constant r a t e , and has no volume t h r e s h o l d . A l l flowers i n the t e r r i t o r y are r e g u l a r l y spaced 1 m a p a r t . S i m i l a r r e s u l t s are obtained f o r a v a r i e t y of other c o n d i t i o n s . 23 chose the patch-leaving rule that minimized time spent foraging over the course of the day (to within 2%). If they could not meet the nocturnal requirement, I chose the patch-leaving rule that maximized the amount of fat accumulated (to within 0.2 kJ/day). One generality I observed was that i f birds had either no memory of previously v i s i t e d patches or flowers, or perfect memory of both, the best patch-leaving rule under a l l conditions was to leave a patch after encountering one empty or nearly empty flower. In the next section, I compare only the success of birds with no memory and perfect memory. Therefore, I use a sampling window of 1 flower and a giving-up threshold of 0.4 ul/flower in a l l cases. However, i f model birds had intermediate degrees of either type of memory, other patch-leaving rules sometimes worked better. Figure 2.8 in the t h i r d section was produced with simulations using a number of dif f e r e n t patch-leaving rules, each of which maximized accumulated f a t . The e f f e c t of nectar production c h a r a c t e r i s t i c s For a l l simulations in t h i s section, t e r r i t o r i e s consist of 25 patches of 36 flowers each, and flowers are regularly spaced 1 m apart over the entire t e r r i t o r y . I i n i t i a l l y assumed that flowers had no threshold accumulated volume, and that they continued to accumulate nectar u n t i l emptied by the b i r d . This is the simplest case because d a i l y t e r r i t o r y nectar production is not affected by whether or not the birds keep flowers under the threshold volume. 24 I observed that i f da i l y t e r r i t o r y nectar production was s u f f i c i e n t l y low that model birds spent a large proportion of their time foraging, then they did not meet their energy requirements at the end of the day (Fig. 2.3). If nectar production was below some minimum l e v e l , birds depleted their t e r r i t o r i e s before the end of the day, and thus could not gain energy regardless of how much time they spent foraging. If t e r r i t o r y nectar production was even at the minimum le v e l at which birds could accumulate their 4.5 kJ of f a t , they never spent more than about 25% of the i r time foraging over the course of the day. Therefore, among birds that could meet their nocturnal energy requirement, there was never a large range of difference in time spent foraging. I compared the time spent foraging by a bird with no memory and one with perfect memory at the minimum t o t a l nectar production l e v e l at which a bird with no memory could meet i t s nocturnal requirement (Fig. 2.3). Regardless of r e l a t i v e day and night production rates, the t o t a l number of v i s i t s to flowers over the course of the day was about 6000 for birds with no memory and 1500 for birds with perfect memory, and the absolute difference in time spent foraging was 10-15%. The above comparison assumes that t e r r i t o r y nectar production i s s u f f i c i e n t l y high that a bird with no memory can meet i t s energy requirements. The more pronounced advantage for birds with perfect memory was that the minimum nectar production l e v e l at which they could accumulate their required 4.5 kJ of fat was lower than for birds with no memory (Fig. 2.4). Figure 2.3. The influence of nectar production rate on foraging e f f o r t when (a) nocturnal nectar production rate = 5x daytime production rate, (b) night rate = day rate, and (c) night rate = 20% day rate. In a l l cases, flowers are empty at the previous dusk and have no volume threshold. The proportion of the t o t a l nectar produced that i s available at dawn i s 78%, 42%, and 13% for (a), (b), and (c) respectively. Numbers adjacent to curves indicate the t o t a l nectar produced per flower per day ( u l ) . Solid l i n e s and closed c i r c l e s indicate model birds with no patch memory or flower memory, whereas broken l i n e s and open c i r c l e s indicate birds with perfect memory of both. For a l l lines above the shaded area, birds with no memory are unable to meet the i r nocturnal energy requirement. The shaded area indicates the difference in time spent foraging among birds with d i f f e r e n t memory capacities at the minimum nectar production l e v e l at which a bird with no memory can meet i t s nocturnal energy requirement. In a l l cases, the t e r r i t o r y has 25 patches of 36 flowers each, and flowers are regularly spaced 1 m apart. - I 1 — 1 1 1 - I — 2 4 6 8 10 12 TIME OF DAY (h) 27 Figure 2.4. The effect of memory on a b i l i t y to accumulate energetic reserves, under three nectar production regimes. The regimes shown are the same as for Fig 2.3. The shaded area indicates the range of t o t a l nectar production at which a bird with perfect memory can survive the night, but a bird with no memory cannot. T e r r i t o r y structure as in F i g . 2.3. 28 Therefore, a bird with perfect memory could hold a smaller, less productive t e r r i t o r y . The r e l a t i v e magnitude of day and night production rates had two influences. F i r s t , the minimum t o t a l nectar production required by birds decreased as the proportion of nectar produced overnight (and therefore the standing crop at dawn) increased (Fig. 2.4, F i g . 2.5). Second, when most nectar production was diurnal, even a s l i g h t drop in t o t a l nectar production below the minimum required for 24 h survival resulted in a precipitous drop in d a i l y fat accumulation (Fig. 2.4c). However, regardless of r e l a t i v e day and night production rates, the minimum t o t a l nectar production required to support a bird with perfect memory was about 15% less than that required to .support a bird with no memory (Fig. 2.5). When I placed a threshold accumulated volume on flowers, the benefits of perfect memory increased. For these simulations, I assumed that nectar production rate was i d e n t i c a l during day and night. If flowers f i l l e d in 4 h, and nectar was produced at the minimum rate at which a bird with no memory could meet i t s nocturnal energy requirement, the absolute difference in time spent foraging between birds with perfect memory and those with no memory was 22% (Fig. 2.6). This compares to a difference of 12% in Figure 2.3b. As well, the proportionate difference in the minimum nectar production rate per flower that was required to support a bird with no memory and one with perfect memory increased from 15% when flowers had no threshold volume to 30% when flowers f i l l e d in 4 h (Fig. 2.7). This suggests that i f flowers f i l l in 4 h, a bird with 29 F i g u r e 2 . 5 . T h e e f f e c t o f t e m p o r a l d i s t r i b u t i o n o f n e c t a r p r o d u c t i o n o n t h e m i n i m u m t o t a l p r o d u c t i o n r e q u i r e d t o s u p p o r t a b i r d w i t h n o m e m o r y ( s o l i d l i n e ) a n d o n e w i t h p e r f e c t m e m o r y ( b r o k e n l i n e ) . T e r r i t o r y s t r u c t u r e a s i n F i g . 2 . 3 . 30 2 A 6 8 10 12 T IME OF DAY ( h ) Figure 2.6. The influence of nectar production rate on foraging e f f o r t when empty flowers reach a volume threshold in 4 hours. Numbers adjacent to curves indicate nectar production rates (ul/h) while flowers are producing. These rates are similar during night and day. Because flowers are not always producing, the dai l y average rates w i l l be less than these values. The shaded area indicates the difference in time spent foraging among birds with d i f f e r e n t memory capacities at the minimum nectar production l e v e l required to support a bird with no memory. Compare with F i g . 2.3b. Interpretation of l i n e s and symbols as in F i g . 2.3. Ter r i t o r y structure as in F i g . 2.3. 3 1 O LLl ' 1 1 1 — i -z 4 8 12 16 20 FLOWER FILLING TIME (h) F i g u r e 2 . 7 . T h e e f f e c t o f a f l o w e r v o l u m e t h r e s h o l d o n t h e m i n i m u m n e c t a r p r o d u c t i o n r a t e ( s e e F i g . 6 ) r e q u i r e d t o s u p p o r t a b i r d w i t h n o m e m o r y ( s o l i d l i n e ) a n d o n e w i t h p e r f e c t m e m o r y ( b r o k e n l i n e ) . T e r r i t o r y s t r u c t u r e a s i n F i g . 2 . 3 . 32 perfect memory could survive with a t e r r i t o r y 30% smaller than one with no memory. Because flowers produced nectar only i f they contained less than the volume threshold, the t o t a l produced per day depended not only on the nectar production rate when flowers were producing, but also on how many flowers birds kept under that threshold. Birds with perfect memory could keep more flowers below the threshold volume, and thus their t e r r i t o r i e s produced more nectar than those of birds with no memory. The ef f e c t of t e r r i t o r y structure The previous section i l l u s t r a t e s the advantages that model birds with perfect memory of both patches and flowers within patches have over those with no memory of either. In t h i s section, I compare the r e l a t i v e benefits of patch and flower memory, and determine whether these r e l a t i v e benefits depend on the number and size of patches, or on the distance between patches and between flowers within patches. For s i m p l i c i t y , I assumed that flowers had no accumulated volume threshold and that flowers produced nectar at i d e n t i c a l constant rates during day and night. For a l l simulations, I used a nectar production rate of 4.3 ul/flower.day, which corresponds to 22.9 kJ/territory.day. In nature, feeding t e r r i t o r i e s of Rufous Hummingbirds average about 25 kJ/day (Gass and Montgomerie 1981; Montgomerie and Gass 1981). I chose t h i s rate because birds with no memory could just break even energetically during the day, but could not accumulate any 33 reserves to last the night (Fig. 2.4b). I evaluated the u t i l i t y of incremental increases in flower and patch memory in terms of t o t a l fat accumulated during the day. I f i r s t varied the number and size of patches in t e r r i t o r i e s in which a l l flowers were regularly spaced 1 m apart. That way, I could vary the s p a t i a l grain of t e r r i t o r i e s without changing the distance between any of the flowers. In a l l cases, short term flower memory was much more b e n e f i c i a l to the birds than patch memory (Fig. 2.8a,b,c; see also F i g . 2.2). The r e l a t i v e u t i l i t y of patch memory was greatest when t e r r i t o r i e s were divided into many small patches. However, even when t e r r i t o r i e s consisted of 100 patches of only 9 flowers each (Fig. 2.8c), birds were able to forage quite e f f e c t i v e l y with no patch memory by avoiding only 8 previously v i s i t e d flowers in each patch. On the other hand, birds with no flower memory could not even break even energetically regardless of their patch memory. I increased the distance between patches and decreased the distance between flowers within patches to see i f t h i s would increase the r e l a t i v e u t i l i t y of patch memory. Using a t e r r i t o r y with 25 patches of 36 flowers each, I t r i p l e d the distance between patch centers, from 6 m to 18 m, and reduced the distance between flowers within patches to one-third, from 1 m to 0.33 m. This also increased the t o t a l area 6-fold, from 900 m2 to 5476 m2 which i s nearly twice the t e r r i t o r y area ever observed in two long-term f i e l d studies (Gass et a l . 1976; Kodric-Brown and Brown 1978; Gass 1979). The r e s u l t i n g pattern 34 Figure 2.8. The r e l a t i v e u t i l i t y of patch memory and flower memory when t e r r i t o r i e s have (a) 4 patches of 225 flowers, (b) 25 patches of 36 flowers, (c) 100 patches of 9 flowers ( a l l flowers spaced 1 m apart in each case), and (d) 25 patches of 36 flowers (0.33 m between flowers within patches, 18 m between patch centers). Each flower produces 4.3 ul/day at a similar rate during day and night, and has no volume threshold. In a l l cases, short term flower memory is much more b e n e f i c i a l to model birds than i s patch memory. 35 of fat accumulation as a function of patch and flower memory (Fig. 2.8d) i s very similar to that of Figure 8b. Therefore, the benefits of patch memory were negligible even when the distance between patches was extremely large. Di scussion Although I have dealt with t e r r i t o r i a l hummingbirds as my case example, my predictions may apply to a variety of t e r r i t o r i a l foragers whose feeding patterns produce s i g n i f i c a n t , l o c a l i z e d depressions in food a v a i l a b i l i t y . The degree to which the predictions may be extrapolated depends on how clos e l y the assumptions of the model f i t the c h a r a c t e r i s t i c s of the par t i c u l a r forager. I have made three general assumptions. F i r s t , I assumed that a l l variance among flowers in model hummingbirds' t e r r i t o r i e s was induced by their own foraging a c t i v i t y . Second, I assumed that food was di s t r i b u t e d in patches that were d i s t i n c t to the birds, and that birds foraged within a single patch u n t i l they decided that patch was depleted. Third, I assumed that birds used an e f f e c t i v e patch-leaving rule that allowed them to recognize that the patch in which they were foraging was depleted. I have also made a series of s p e c i f i c assumptions based on laboratory and f i e l d studies of hummingbirds. These dictate the r e l a t i v e energetic costs of model birds' various a c t i v i t i e s and their r e l a t i v e handling times of empty and f u l l flowers. From the simulations, I predict that short term flower memory may be s u f f i c i e n t l y b e n e f i c i a l to outweigh any associated 36 costs. I predict, however, that longer term patch memory w i l l have negligible benefits. I caution that t h i s does not imply, that there i s never any payoff for hummingbirds to retain long term memory of patterns of s p a t i a l v a r i a t i o n in their t e r r i t o r i e s . Real t e r r i t o r i e s may have a great deal of variation in p r o f i t a b i l i t y , both among individual flowers and among patches, that is induced by sources other than owners' foraging. These include differences in nectar concentration and production rate due to differences in plant species and genetic makeup, differences in s o i l q u a l i t y and other a b i o t i c factors, and foraging by intruders. Gass and Sutherland (1985) found that hummingbirds learned and remembered locations of experimentally enriched patches, and that they used th i s information to guide their selection of patches, even on successive days. In the laboratory, hummingbirds learn and remember the c h a r a c t e r i s t i c s of s p a t i a l d i s t r i b u t i o n s of feeders (Gass 1985; Sutherland, in prep.). I predict, however, that there i s no payoff for hummingbirds to retain long term memory of patterns caused by their own foraging. The simulations suggest" that an important consequence of short term memory may be creation and maintenance of patterns of vari a t i o n that allow foragers to e f f e c t i v e l y exploit their t e r r i t o r i e s l a t e r on. If model birds could avoid r e v i s i t i n g flowers while foraging in a patch, they could empty a l l or nearly a l l flowers before foraging in that patch became unprofitable. As a resu l t , they not only achieved a high immediate rate of energy intake, but also created a coarse-37 grained pattern of variation in which the variance in quality among patches was high. High variance among patches should increase the rate of harvesting by any forager that uses i t s experience within patches to decide when to leave them (Green 1984), and model birds used a patch-leaving rule that allowed them to quickly redirect their foraging to p r o f i t a b l e patches. In addition, their energetic cost per time while f l y i n g between patches was only half what i t was while hovering at flowers. Therefore, the cost of v i s i t i n g depleted patches turned out to be n e g l i g i b l e , and thus the benefits of patch memory were also n e g l i g i b l e . This high cost of hovering in comparison to f l y i n g between patches was based on evidence from laboratory studies on several species of hummingbirds (Montgomerie 1979). However, th i s r e l a t i v e l y high cost of foraging observed in hummingbirds may be somewhat a t y p i c a l . For example, most birds (including the other nectarivores) walk, hop, or perch while foraging, and thus the energetic cost of foraging i s less than that of forward f l i g h t . In addition, the distance between patches may be r e l a t i v e l y greater for a number of other animals. Consequently, patch memory may be of r e l a t i v e l y greater value for some other types of animals. For t e r r i t o r i a l hummingbirds, the primary benefit of e f f i c i e n t foraging in general may be that i t allows them to s a t i s f y their energetic requirements in t e r r i t o r i e s that produce less nectar. Hummingbirds may therefore be able to hold smaller t e r r i t o r i e s that are less expensive to defend. The simulations 38 suggest that the magnitude of t h i s benefit should be f a i r l y consistent over a range of t e r r i t o r y structures and nectar production c h a r a c t e r i s t i c s (Fig. 5, F i g . 2.8), although I do predict that i t w i l l increase somewhat i f nectar production rates of flowers decrease as a function of their standing crop (Fig. 2.7). Another factor, however, i s that the intensity of size constraint on hummingbirds' or other animals' t e r r i t o r i e s may vary. D i l l (1978) and Hixon (1980) predicted that a forager's optimal t e r r i t o r y size (in terms of maximizing net energy intake) w i l l decrease as competitor pressure increases, and t h i s effect has been observed in t e r r i t o r i a l sunbirds (Wolf 1975; G i l l and Wolf 1975). Therefore, the benefit of avoiding recently v i s i t e d locations may increase as competitor density increases. S i m i l a r l y , i f we were to experimentally remove potential intruders surrounding an animal's t e r r i t o r y , i t i s possible that i t would expand i t s t e r r i t o r y , and would therefore not need to forage as e f f i c i e n t l y . The costs as well as the benefits of memory may depend on the forager's environment. It seems reasonable that the costs might be proportional to the amount of information that must be stored and processed. Regardless of whether memory i s achieved by maintaining a cognitive map or by e f f i c i e n t harvesting, i t i s l i k e l y that the amount of information required w i l l be an increasing function of the number of locations that must be avoided. On model t e r r i t o r i e s with only 4 large patches (Fig. 2.8a), perfect flower memory consisted of remembering 224 previously v i s i t e d flowers. With the nectar production rate I 39 used, model birds needed to remember more than 100 flowers at one time to meet their energetic requirements. However, on t e r r i t o r i e s with 100 small patches (Fig. 2.8c), they could meet their energy requirements by remembering only 8 previously v i s i t e d flowers in each patch. They could create a pattern of s p a t i a l variation s u f f i c i e n t l y coarse-grained that i t was easy to exploit, and could do so with a minimum of information. Therefore, we might predict that animals w i l l be able to forage e f f e c t i v e l y using less information i f t h e i r t e r r i t o r i e s are divided into many small patches within which they can organize their foraging. For hummingbirds, patches in t h i s sense could refer either to physically separated clumps of flowers or to groups of flowers separated by natural landmarks. In my model, I have assumed that the s p a t i a l organization of foraging behavior i s a d i r e c t function of s t r u c t u r a l features of t e r r i t o r i e s . However, i t i s quite plausible that even in b a s i c a l l y structureless t e r r i t o r i e s , animals organize their foraging such that they create coarse-grained patterns of v a r i a t i o n . For example, during any single feeding bout, hummingbirds do tend to forage in single patches and to approximate nearest-neighbor v i s i t a t i o n sequences within them (Gass and Montgomerie 1981). This t a c t i c may minimize t r a v e l costs. However, i t may also produce f a i r l y homogeneous l o c a l depression. A p o s s i b i l i t y worth investigating i s that hummingbirds' or other animals' foraging t a c t i c s create coarse-grained patterns s t r a t e g i c a l l y in that these patterns allow them to e f f i c i e n t l y exploit their t e r r i t o r i e s l a t e r on. 40 CHAPTER 3 ECONOMICS OF BREEDING TERRITORIALITY IN MALE CALLIOPE HUMMINGBIRDS Food has always played a prominent role ' in theories of t e r r i t o r i a l i t y . Altum (1868; translated by .Mayr 1935) and Howard (1920) both emphasized the importance of an exclusive food supply as a function of t e r r i t o r y defense in nesting bir.ds. Although the existence of hummingbird t e r r i t o r i a l i t y i s recorded in early l i t e r a t u r e (Bullock 1824; Knowlton 1909; Saunders 1936; Aldrich 1939; Woods 1940), Pit e l k a (1942) was the f i r s t author to consider in d e t a i l why hummingbirds defend t e r r i t o r i e s . On the basis of his own observations of breeding male Ruby-throated Hummingbirds (Archilochus c o l u b r i s ) , and previously published accounts for other species during breeding and non-breeding seasons, Pit e l k a concluded that " a l l evidence suggests that t e r r i t o r i a l behavior of male North American hummingbirds centers around a food supply". In his review of avian t e r r i t o r i a l i t y , Hinde (1956) concluded that "while t e r r i t o r i a l behavior i s primarily concerned with food in a few species (e.g. hummingbirds, Pitelka 1942), in most cases the food value i s not s i g n i f i c a n t " . Subsequent observations have indicated that defense of food resources i s common among other nectarivorous birds including sunbirds ( G i l l and Wolf 1975), honeycreepers (Carpenter and 41 MacMillen 1976; Kamil 1978), and honeyeaters (Paton 1979), and is also observed in some other birds such as sandpipers and wagtails (Davies and Houston 1984). Nevertheless, i t s t i l l appears that i t i s rare for birds to defend t e r r i t o r i e s that supply primarily food (Welty 1982). Economics of non-breeding t e r r i t o r i a l i t y Brown's (1964) economic threshold model predicts that an animal w i l l defend a t e r r i t o r y only i f the benefits of that defense outweigh the costs. Theoretically, these benefits could involve access to a variety of resources such as food, shelter, courtship grounds, nesting/oviposit ion s i t e s , or refuges from predators. However, di r e c t comparison of benefits and costs i s most feasible i f both can be expressed in a single currency, and the most e a s i l y quantified currency i s energy. Consequently, the economic threshold model applies p a r t i c u l a r l y well to hummingbirds and other birds that defend energy sources. So far, rigorous empirical work on the economics of t e r r i t o r i a l i t y in nectarivorous birds has been confined to the non-breeding season, at which time i t i s thought the costs and benefits of t e r r i t o r i a l i t y can be indexed solely in terms of energy (Ewald 1980; Hixon 1980). G i l l and Wolf (1975) hypothesized that the benefit to sunbirds of excluding intruders from their t e r r i t o r i e s would be enhancement of nectar a v a i l a b i l i t y , and found nectar a v a i l a b i l i t y to be s i g n i f i c a n t l y higher on t e r r i t o r i e s than on neighboring undefended areas. Carpenter and MacMillen (1976) predicted, on the basis of 42 Brown's (1964) model, that honeycreepers would defend t e r r i t o r i e s only i f enhancement of nectar a v a i l a b i l i t y more than compensated for the energetic cost of that defense, and their data convincingly supported th i s hypothesis. Ewald and Carpenter (1978) and Ewald (1980) also found that t e r r i t o r i a l Anna's Hummingbirds responded to experimental manipulations of energy a v a i l a b i l i t y as predicted by the economic threshold model. Sizes of t e r r i t o r i e s held by non-breeding nectarivorous birds can also be accounted for by energy-based economic models (Schoener 1971, 1983; D i l l 1978; Hixon 1980; Hixon et a l . 1983). In p a r t i c u l a r , the sizes of t e r r i t o r i e s held by migrating Rufous Hummingbirds in mountain meadows are negatively correlated with flower density (Gass e_t §_1. 1 976; Gass 1979; Kodric-Brown and Brown 1978). Further, the amount of energy produced per day by flowers in these t e r r i t o r i e s c l o s e l y matches the t o t a l d a i l y energy requirements of the resident birds (Gass and Montgomerie 1981; Montgomerie and Gass 1981). Individual birds adjust the sizes of their t e r r i t o r i e s in response to both natural (Gass 1979) and experimentally induced (Kodric-Brown and Brown 1978; Hixon et a l . 1983) variations in flower density. Breeding t e r r i t o r i e s of male North American hummingbirds During the breeding season, an important benefit of t e r r i t o r i a l i t y i s improvement in immediate reproductive success (Hixon 1980). Among North American hummingbirds, only males hold t e r r i t o r i e s during the breeding season (Pitelka 1942, 1951; 43 Legg and P i t e l k a 1956; Williamson 1956; S t i l e s 1970). Although females sometimes nest within the boundaries of males' t e r r i t o r i e s ( S t i l e s 1970), there i s generally a f a i r l y clear habitat separation; females nest in wooded areas and males hold t e r r i t o r i e s in open meadows, usually around aggregations of nectar producing flowers (Pitelka 1951; Legg and Pi t e l k a 1956; S t i l e s 1970). Interactions between males and females are most often observed on males' t e r r i t o r i e s , and the few copulations that have been observed have occurred there ( S t i l e s 1982). Except for a few isolated observations, there are no obvious pair bonds formed, and there i s no parental care by males (Johnsgard 1983). Enhancement of nectar a v a i l a b i l i t y on t e r r i t o r i e s could be an important benefit of defense during the breeding season as well as the non-breeding season. Because breeding males are involved in more energetically expensive a c t i v i t i e s ( S t i l e s 1971), energy may be p a r t i c u l a r l y important at that time of year. In addition, enhancement of nectar a v a i l a b i l i t y on their t e r r i t o r i e s could increase males' reproductive success in at least three d i f f e r e n t ways. F i r s t , extra energy could allow males to perform energetically expensive courtship displays (Tamm 1985). Second, high nectar a v a i l a b i l i t y could att r a c t females to t e r r i t o r i e s to feed, where they might subsequently copulate with resident males ( S t i l e s 1970). Third, nectar a v a i l a b i l i t y on t e r r i t o r i e s could act as a secondary sexual c h a r a c t e r i s t i c which females use as an index of the genetic quality of males (Selander 1965). 44 Because a l l the above benefits could result from enhanced nectar a v a i l a b i l i t y , t e r r i t o r i a l i t y that involved only these benefits could be described by an energy-based economic model. However, other benefits could outweigh energetic considerations. F i r s t , by defending their t e r r i t o r i e s from other males, owners could secure exclusive access to any females that entered them. The best locations for encountering females may or may not be those with the highest concentration of nectar producing flowers. Second, exclusive use of t e r r i t o r i e s could allow males to court females without interruption. Third, some quality of males' t e r r i t o r i e s other than nectar a v a i l a b i l i t y could act as a secondary sexual c h a r a c t e r i s t i c , and att r a c t females. In t h i s study, I ask whether breeding t e r r i t o r i a l i t y of a group of male Calliope Hummingbirds can be accounted for solely by an energy-based model. Study Area Location and timing of t e r r i t o r i a l i t y I studied a group of Calliope Hummingbirds in the Ashnola Provincial Forest about 25 km SW of Penticton, B.C., Canada (119° 47' W, 49° 18' N, elevation about 800 m) during the 1985 breeding season. The males I studied a l l held t e r r i t o r i e s within a s t r i p of meadow about 100 m wide (Fig. 3.1) in a valley immediately W of Twin Lakes. Although male Rufous Hummingbirds sometimes hold t e r r i t o r i e s for a few days in the meadow, the only longer term t e r r i t o r i e s are held by male 45 DOUGLAS FIR COVER > 2 m DECIDUOUS COVER > 2 m OPEN MEADOW F i g u r e 3.1. P o s i t i o n s o f t e r r i t o r i e s 1 t h r o u g h 6 on 1 June 1985. T h e s e were h e l d by m a l e s d u r i n g F e m a l e s n e s t i n D o u g l a s f i r , i m m e d i a t e l y N of t h e meadow. See t e x t f o r d e f i n i t i o n o f t e r r i t o r y b o u n d a r i e s . t e r r i t o r i e s most of May and J u n e , c o n i f e r s , p r i m a r i l y 46 Calliopes. Both Rufous and Calliope males also hold t e r r i t o r i e s in meadows on the S slope of the val l e y . Other studies were conducted in thi s area in 1983 and 1984 (Tamm 1985; Tamm et a l . in prep). Calliope males arr i v e in the valley in late A p r i l , and defend t e r r i t o r i e s throughout May and June (Fig. 3.2). Females arrive in early May, and begin interacting with males on their t e r r i t o r i e s soon a f t e r . Seven Calliope nests found in thi s area in 1983 and 1984 were a l l within the Douglas f i r (Pseudotsuga  menziesi i) growth N of the meadow (Fig. 3.1). The average date of egg laying of these 7 nests appeared to be early in June. However, i t i s d i f f i c u l t to estimate when the f i r s t and l a s t clutches were i n i t i a t e d , and therefore when the f i r s t and l a s t matings occurred. I studied the same 6 t e r r i t o r i e s throughout the 1985 breeding season (Fig. 3.1). These were the f i r s t 6 t e r r i t o r i e s in the meadow, and were a l l established by 6 May. T e r r i t o r i e s 1,3, and 6 were each defended by a single c l e a r l y marked male throughout the season. T e r r i t o r i e s 2, 4, and 5 were each defended sequentially by at least 2 di f f e r e n t males, and during mid-May, t e r r i t o r y 5 was divided between at least 2 and sometimes 3 males. 47 5 . 1 5 25 5 15 2 5 M A Y J U N E Figure 3.2. Phenology of t e r r i t o r i a l i t y in the meadow shown in F i g . 3.1, and approximate timing of reproductive a c t i v i t i e s . The influx of additional males during mid-May i s correlated with the peak of the Ribes flowering season. 48 D e f i n i t i o n of t e r r i t o r i e s If t e r r i t o r i e s are considered to be 'defended areas' (Noble 1 939), t e r r i t o r y boundaries should include a l l points from.which owners would expel or attempt to expel intruders. Previous studies on hummingbird t e r r i t o r i a l i t y (Gass et a l . 1976; Gass 1979; Kodric-Brown and Brown 1978; Norton et a l . 1982; Hixon et a l . 1983) have primarily defined t e r r i t o r y boundaries as consisting of the outermost locations at which aggressive interactions were observed. However, unless intrusion rates are high, and well d i s t r i b u t e d around t e r r i t o r y perimeters, t h i s method presents two problems. F i r s t , estimated t e r r i t o r y sizes w i l l increase with increases in observation time. Second, locations that intruders did not enter, but would have been expelled from i f they had, w i l l not be included. In t h i s study, I defined each male's t e r r i t o r y on a given day in terms of the perches he used while surveying his t e r r i t o r y on that day. Of 242 chases of intruding hummingbirds by t e r r i t o r i a l males during the 1985 season, 228 (94%) were i n i t i a t e d when the intruder was within 10 m of the perimeter described by the perches used by the owner on that day. Throughout t h i s study, I used th i s c r i t e r i o n to define t e r r i t o r y boundaries. Sources of nectar Males a r r i v e about a week before the f i r s t nectar producing plants begin to bloom. At t h i s time, the only food males are seen to consume i s small insects (Diptera, Lepidoptera, Neuroptera) that they hawk from their perches. Bushes of Squaw 49 Currant (Ribes cereum) begin blooming in early May. Ribes i s the only source of nectar available to birds throughout May, and is found within a l l t e r r i t o r i e s in the meadow. During mid-May, when the number of t e r r i t o r i e s i s at i t s peak (Fig. 3.2), almost a l l bushes are within or near t e r r i t o r i e s . However, dense aggregations of Ribes bushes are also found on undefended areas both within and around the Douglas f i r growth N of the meadow, and on the slope S of the meadow. Several other nectar producing plants bloom in and around the t e r r i t o r i e s after Ribes dries up in late May. These include Lemonweed (Lithospermum ruderale), Creeping Mahonia (Berberis  repens), Larkspur (Delphinium nuttallianum), Hound's-tongue (Cynoglossum o f f i c i n a l e ) , and Snowberry (Symphoricarpos  oreophilus and S. albus). During preliminary observations in 1984, I saw t e r r i t o r i a l males v i s i t flowers of a l l these species. However, the amount of time I observed birds foraging on these flowers was very small (< 1% of 15 h observation time in June). One plant that is common in the area throughout June, but is not found on the t e r r i t o r i e s I studied, i s Indian Paintbrush ( C a s t i l l e j a miniata). C a s t i l l e j a i s a t y p i c a l ornithophilous plant (Grant and Grant 1968) in that i t s flowers are red, secrete copious nectar, and have a long, tubular shape which makes them accessible to hummingbirds, but not to most insects (Perkins 1977). In contrast, a l l flowers on the t e r r i t o r i e s are shallow, and are accessible to insects as well as birds. Bees (Bombus spp., Apis sp., Emphoropsis spp., Anthophora spp., 50 Andrena spp.) and Hawk Moths (Hemaris d i f f i n i s ) are commonly seen feeding on the t e r r i t o r i e s . C a s t i l l e j a occurs within t e r r i t o r i e s located on the slope S of the valley, in areas that are defended during both May and June. However, the areas of dense C a s t i l l e j a growth that are closest to the meadow are generally undefended. These are located on the steep portion of the slope about 50-100 m S of and 50-100 m above the meadow. 51 PART I. PROFITABILITY AND ENERGY PRODUCTION OF TERRITORIES During both May and June, I repeatedly sampled nectar both on t e r r i t o r i e s and on nearby undefended areas with abundant nectar producing flowers. I did thi s to answer 2 questions. F i r s t , could males obtain energy faster by foraging on their t e r r i t o r i e s than by foraging on the undefended areas? Second, could males obtain enough energy from nectar produced on their t e r r i t o r i e s to meet their metabolic requirements? Methods Sampling design Between 8 and 21 May, I sampled nectar from Ribes flowers on 4 t e r r i t o r i e s ( t e r r i t o r i e s 1,2,4, and 5 in F i g . 3.1) and 2 undefended areas. Because most Ribes bushes in the meadow were either within or near the boundaries of a t e r r i t o r y , I sampled undefended areas close to but outside the meadow. The f i r s t was a series of bushes on the slope about 100 m S of and 100 m above the meadow. The second was a series of bushes within and around the Douglas f i r growth, a l l within 20-50 m N of the meadow. The density of Ribes bushes on both of the undefended areas was approximately equal to that on the t e r r i t o r i e s . During each of the two weeks of Ribes sampling, I sampled each of the 6 areas once. During each of 4 weeks between 27 May and 25 June, I sampled nectar from flowers of a l l plant species that bloomed on 52 the t e r r i t o r i e s after Ribes. Because the density of these flowers was low, I had to treat a l l 6 t e r r i t o r i e s as a single defended area. During each of those same 4 weeks, I sampled C a s t i l l e j a on a single 700 m2 undefended area about 80 m S of and above the meadow. Although there were many isolated patches elsewhere, this was the largest area of f a i r l y contiguous C a s t i l l e j a growth. On 3 June, i t contained 1615 C a s t i l l e j a inflorescences, and t h i s density remained f a i r l y constant throughout most of June. On and before 10 June, I conducted 4 sampling sessions each day sta r t i n g at 06:00, 10:00, 14:00, and 18:00. Because of the lengthening photoperiod, after 10 June I conducted 5 sampling sessions s t a r t i n g at 05:00, 09:00, 13:00, 17:00, and 21:00. I divided each area I sampled into 10 s i t e s , and measured nectar volumes of 3 flowers from each of 3 d i f f e r e n t treatments at each s i t e . The f i r s t treatment was an uncovered branch available to a l l foragers. The second treatment was a branch that had been covered with a p l a s t i c screen bag since the la s t sampling session, and thus had been unavailable to foragers during that time. The t h i r d treatment was a branch covered with a wire bag with 3.2 cm by 2.5 cm hexagonal holes, which allowed insects to enter, but not birds. 53 Sampling techniques I measured nectar volumes in flowers by extracting nectar with glass microcapillary tubes, and measured nectar concentrations using a temperature ca l i b r a t e d sugar refTactometer. Because a minimum volume is required before a concentration reading can be obtained (1-4 u l , depending on l i g h t conditions), I often needed to accumulate nectar from several flowers in order to get a reading. I approximated random sampling by choosing flowers haphazardly with respect to appearance and position. I did not include old, withered flowers in samples. Estimation of p r o f i t a b i l i t y I define the p r o f i t a b i l i t y of an area as the rate at which a bird could obtain energy while foraging on that area over a given time period. In t h i s analysis, I estimate rates at which birds could obtain energy while foraging for 10% of a 16 h day. This represents the amount of time birds were observed to forage on Ribes on their t e r r i t o r i e s during the peak of the Ribes flowering season in mid-May (Fig. 3.9). Instantaneous rate of nectar intake (Watts) at any time i s a product of 3 factors: the nectar volumes of flowers birds v i s i t (ul/flower), the sugar concentration of the nectar ( J / u l ) , and the number of flowers birds v i s i t per time (flowers/s). For each sampling session on the t e r r i t o r i e s , I averaged nectar volumes of unbagged flowers at a l l 10 s i t e s , and multiplied this by the average of a l l concentration readings to obtain a single 54 estimate of the mean energy content per flower. For C a s t i l l e j a , I obtained at least one concentration reading for every second s i t e . Therefore, for each sampling session, I obtained 5 separate estimates of energy content per flower, with each estimate consisting of data averaged for 2 s i t e s . In order to estimate the rate at which birds could obtain this energy, I measured rates at which birds v i s i t e d flowers of each species by timing their foraging with a stopwatch whenever I could observe them at close range. For each t e r r i t o r y or undefended area, I used the resulting estimates of the instantaneous rates at which birds could acquire energy to calculate the amount of energy a bi r d would obtain while foraging for 10% of the day. As long as thi s amount was less than the estimated t o t a l energy production on the area, I assumed that the instantaneous rate was a reasonable estimate of p r o f i t a b i l i t y . This was always the case throughout the Ribes season, and for the C a s t i l l e j a area throughout June. However, on the t e r r i t o r i e s in June, flowers of some species were so sparse that birds could have obtained energy from them at the estimated instantaneous rate for only a few minutes each day. In c a l c u l a t i n g p r o f i t a b i l i t y of the t e r r i t o r i e s at that time, I assumed that birds would spend as much time as possible foraging on the best species on their t e r r i t o r i e s , and would allocate t h e i r remaining time to foraging on the second best species, t h i r d best species, and so on. 55 Estimation of t e r r i t o r y energy production The difference between the average energy content of flowers covered with screen bags and that of unbagged flowers at the same s i t e at the l a s t sampling session provides an estimate of the average energy production per flower over that period. The estimate of 24 h energy production per flower i s the sum of the estimates of production for a l l time periods between samples. The energy produced each day on a t e r r i t o r y i s the product of the average d a i l y energy production per flower and the number of flowers on the t e r r i t o r y . I estimated the number of flowers of each species in each t e r r i t o r y at least once each week. For species other than Ribes, flower density was s u f f i c i e n t l y low that I could i n d i v i d u a l l y count a l l flowers on each t e r r i t o r y . Because Ribes flowers were far too numerous to count i n d i v i d u a l l y , I estimated the number of flowers on each bush in bloom within a t e r r i t o r y on the basis of two indices: the volume of the bush and i t s phenological state. Most Ribes bushes are roughly hemi-ellipsoidal in shape. Therefore, I measured the longest and shortest horizontal axis and the height of each bush, and calculated the volume of a hemi-ellipsoid with these dimensions. I recorded the phenology of each Ribes bush by counting the number of flowers in bloom on the same sample branches twice each week. At the end of the season, I divided the flower count for each date by the maximum number ever counted on that branch, and averaged the values of a l l branches on each bush. Throughout May, I also counted flowers on sectors 56 of 51 randomly selected bushes, with each sector making up 1/16 of the bush volume. The number of flowers (f) counted on 51 bush sectors throughout May was predicted ( r 2 = 0.60) by = 0.4v +2.3p, where v and p are the volume and phenological state of the bush respectively. By summing the predicted values for a l l Ribes bushes on each t e r r i t o r y , I used t h i s equation to estimate the t o t a l number of flowers. Estimation of proportion of nectar removed by insects The t o t a l amount of nectar removed by a l l foragers between sampling sessions i s estimated by the difference in average nectar volumes between flowers covered with screen bags and those l e f t uncovered. The amount removed by insects i s estimated by the difference in nectar volumes between flowers covered with wire bags and those l e f t uncovered. If the rate of nectar harvesting by insects i s not affected by the wire bags, the r e l a t i v e magnitude of the two differences provides an estimate of the proportion of nectar consumed by insects. I tested the assumption that wire bags did not reduce insect foraging by comparing v i s i t a t i o n rates to bagged Ribes branches to rates observed immediately before or after these branches were bagged. Throughout the day of 16 May, I observed 72 branches for 30 minutes each both while bagged and unbagged. Based on logarithms of v i s i t a t i o n rates, I estimated that the r a t i o of v i s i t a t i o n rates to bagged and unbagged flowers was 1.04 (95% confidence i n t e r v a l = 0.65 - 1.67), which indicates that the bags did not have a strong effect on insect v i s i t a t i o n 57 rates. Results Comparative p r o f i t a b i l i t y of defended and undefended areas During both weeks I sampled Ribes during May, flowers on t e r r i t o r i e s contained less nectar on average than those on the two undefended areas (Fig. 3.3). Nectar concentrations were f a i r l y similar on defended and undefended areas (Fig. 3.4). Using these data, and flower v i s i t a t i o n rates for Ribes (Table 3.1), I estimated rates at which birds could obtain energy while foraging on these areas. These estimates suggest that birds could have obtained energy faster by foraging on the undefended areas than by foraging on their t e r r i t o r i e s (Fig. 3.5). Most flowers that bloomed on the t e r r i t o r i e s in June contained very l i t t l e nectar, and far less than that found in the undefended C a s t i l l e j a flowers (Figs. 3.3). Flowers of Delphinium and S. albus on the t e r r i t o r i e s contained approximately the same amount of energy on average as those of C a s t i l l e j a (Fig. 3.3, 3.4). However, there were so few of these flowers on the t e r r i t o r i e s (Table 3.2) that owners could have harvested their 24 h nectar production in no more than 3 to 4 minutes of foraging. Estimates of p r o f i t a b i l i t y on the t e r r i t o r i e s in June (Fig. 3.5) primarily r e f l e c t the low nectar volumes of Lithospermum, Berber i s , Cynoglossum, and S. oreophilus. In order to obtain those estimates, I needed to make some 58 10 20 5 15 25 MAY JUNE Figure 3 . 3 . Nectar volumes of. flowers blooming on (•§• ) and off (-&) t e r r i t o r i e s over the course of the breeding season. Data for May are a l l for Ribes. Date for June are for C a s t i l l e j a off t e r r i t o r i e s and Lithospermum (L), Berber i s (B), Delphinium (D), Cynoglossum (C), S. oreophilus (So), and S. albus (Sa) on t e r r i t o r i e s . Each point indicates the mean nectar volume of flowers at 10 sampling s i t e s , averaged over 4 or 5 times of day. V e r t i c a l bars indicate 95% confidence i n t e r v a l s . Figure 3.4. Concentration of nectar in flowers blooming on (#) and off (•&) t e r r i t o r i e s . Points shown were obtained by c a l c u l a t i n g mean nectar concentrations at each time of day and averaging these. V e r t i c a l bars indicate 95% confidence i n t e r v a l s . / 60 Table 3.1. Flower v i s i t a t i o n r a t e s by male C a l l i o p e Hummingbirds on 4 p l a n t s p e c i e s . Values shown are mean r a t e s ± 95% confidence i n t e r v a l s . No. Bouts Flowers Observed per second Ribes 9 1.0 ± 0.1 Lithospermum 8 0.8 ± 0.05 Delphinium 10 0.7 ± 0.1 C a s t i l l e j a 31 0.6 ± 0.05 6 1 Table 3.2. Total number of flowers of 6 plant species censused on t e r r i t o r i e s each week during June. Underlined numbers indicate that there were i n s u f f i c i e n t flowers of that species to conduct nectar sampling during that week. Date May 27 Lithospermum 1 669 Berberi s 1 068 Delphinium • 0 Cynoqlossum 249 S. oreophilus 0 S. albus 0 June 4 June 11 June 18 1 502 357 38 580 0 0 253 187 22 2180 6051 3853 489 5570 698 0 0 243 62 (a) MAY (b) JUNE Figure 3.5 Comparative p r o f i t a b i l i t y of flowers blooming on (•) and off ( O ) t e r r i t o r i e s at several times of day over the course of the breeding season. P r o f i t a b i l i t y refers to the gross rate at which a bi r d could obtain energy while foraging in a given area, assuming that i t spends 10% of the day foraging. (a) compares p r o f i t a b i l i t y of Ribes on each of 4 t e r r i t o r i e s in May with that on 2 undefended areas N and S of the meadow. (b) compares p r o f i t a b i l i t y of several plant species on the t e r r i t o r i e s in June (see F i g . 3.3) with that of C a s t i l l e j a on the slope S of the meadow. The top of the shaded region i s an approximation of the cost of hovering, based on Montgomerie's (1979) allometric equations. If birds' rates of energy intake were below t h i s value, they would lose energy even while foraging. 63 assumptions. Cynoglossum nectar volumes were so low that I could obtain no concentration readings. I made the l i b e r a l assumption (see F i g . 3.4) that i t s nectar was 40% sugar w/w. I obtained concentration readings for S. oreophilus during only one sampling session. For other sampling sessions, when nectar volumes were ne g l i g i b l e , I assumed that the average concentration was unchanged. Of the 6 species that bloomed on the t e r r i t o r i e s in May, I observed birds foraging on only Lithospermum and Delphinium, and therefore could not measure flower v i s i t a t i o n rates for the other species (Table 3.1). Because the morphologies of S. oreophilus, S. albus, and Berber i s are f a i r l y similar to that of Ribes, I assumed that v i s i t a t i o n rates were s i m i l a r . For Cynoglossum, I used the average rate observed for Lithospermum. For weeks during which there were too few flowers of a species to sample i t , I assumed that nectar volumes and concentrations were equal to that on the closest preceding or succeeding week on which I could (Table 3.2). The resultant estimates of p r o f i t a b i l i t y on the t e r r i t o r i e s for each week in June suggest that birds could never have obtained enough energy even to compensate for the metabolic cost of hovering while foraging (Fig. 3.5). Given these estimates, i t i s not surprising that I observed few instances of birds v i s i t i n g these species. In contrast, estimates of p r o f i t a b i l i t y for C a s t i l l e j a on the slope indicate that birds could have obtained energy f a i r l y rapidly from t h i s species (Fig. 3.5). Throughout June, the b i l l s of a l l 6 t e r r i t o r y residents in the 64 meadow were usually coated with the bright orange pollen c h a r a c t e r i s t i c of C a s t i l l e j a , indicating that they must have used C a s t i l l e j a somewhere off their t e r r i t o r i e s . T e r r i t o r y energy production and metabolic requirements of birds I compared estimates of t e r r i t o r y energy production with estimates of birds' minimum da i l y energy expenditures, which I calculated using both King's ( 1974) and Montgomerie' s ( 1979) allometric equations. Estimates of energy production by Ribes in mid-May are greater than birds' minimum energy requirements (Fig. 3.6). Although insects removed about 60% of t h i s energy (Fig. 3.7), birds may have been able to obtain enough energy from their t e r r i t o r i e s at that time to meet their metabolic requirements. In contrast, estimates of t e r r i t o r y energy production in June were far below birds' minimum requirements (Fig. 3.6), and insects consumed most of th i s energy (Fig. 3.7). I estimated that insects removed more than 75% of the nectar produced by a l l species blooming on the t e r r i t o r i e s in June except Berberis, and th i s o u t l i e r was caused by one flower with an exceptionally high nectar volume out of 360 sampled. Conversely, data for C a s t i l i e j a on the slope confirmed that a l l or nearly a l l nectar produced by t h i s species was removed by hummingbirds (Fig. 3.7). 65 J U N E F i g u r e 3.6. Estimated d a i l y energy p r o d u c t i o n f o r 4 t e r r i t o r i e s d u r i n g May, and f o r 6 t e r r i t o r i e s d u r i n g June. V i r t u a l l y a l l energy p r o d u c t i o n throughout May i s by Ribes. Minimum d a i l y energy expenditure i s based on Montgomerie's (1979) equations, and the assumptions that b i r d s remain perched f o r 16 h at 20°C and s l e e p f o r 8 h at 5°C. King's (1974) a l l o m e t r i c equation, which does not i n c o r p o r a t e temperature, p r e d i c t s a s l i g h t l y lower value of 20.6 kJ, n O fD i-i Ch c\ts> n -a> o 3 fD o CO • H* I Q O O n > in r t TJ 0) < O c 3 Cr fD <D in o • 0) c cn fD o Co iQ 0) i-l cn < I-I n> o i - 1 3 Z O LQ < M-> 3 C — T I S l-h « CO I-I a o rr CT I-I Co O i Q DJ cn cn D fD * fD CU fD 1 l-h fD X O n o g I—' € TJ C fD 0J Qj t-l i-l (5 (fl H-a s — fD 03 3 0) o 3 t—1 3 a o fD cn o s m rt l-l l-l fD 0) c i IT] a 3 <r> o c o < ^ l-h fD fD l-h Q i CO n °" ^ 0) r t O * « I-I a < o i—• c 3 fD >-t 3 fD C O 3 r t 3 c r o p> u m a M cn (D 3 rt 3" a w O i-t 3 O rt cn 03 3 M. O 3 i-h 3 — W O O i-l 3 a o • fD 3 O i-l l-h O n rt H 3 3">< fD W O O cn OJ r t r t O 3 ' Co co 3 r t r t O" fD fD in O 0) 3 C 3 fD cn • s fD TJ ' CO fD O >< 3 V l-h cr 3 cu i O cn cn n —* I-I o fD cn 3 fD (-• 3 O •< r-h CT cr C t->. cu 3 I-I 03 c r OJ cn cu in 03 03 fD fD X 3- a O C I-' 3 l-h C 3 i -a H- o fD 3 S QJ03 fD — CT i-l • 01 n Ch * O in r t 3* r t Cu fD 3 r t o t-> in cr fD 3 fD fD fD O in cn i-h r t fD 3 i-i in f-l fD M- n r t r t O in in O 3 >-' in o rt 3 Cu r t fD fD O cn i-i TJ • I-I T J O ( - " O n Cu O 3 i-l r t r t O cr in r t T J CU fD M- O O 3 P ' H l fD fD OJ in Cu CU IT M-rt H H O •< (D O in 3 3 fD >-•• fD 3 O 03 r t fD 0» t r I-I o r t T J 3" n O o a 3 C O 3 0) r t fD in cr w o >< ^ 3 % O F T O T A L H A R V E S T R E M O V E D B Y I N S E C T S o 2 > -< > K J O •-O D CT • in • O a -A • > • 67 Discussion Throughout the breeding season, flowers blooming on the t e r r i t o r i e s appeared to be less p r o f i t a b l e than those on nearby undefended areas. This result strongly suggests that an energy-based model cannot account for the t e r r i t o r i a l i t y of Calliope males in the meadow. Nevertheless, some caution should be exercised in using data from random samples of flowers to infer rates at which birds could obtain energy on their t e r r i t o r i e s . One factor not considered in such an analysis is that a t e r r i t o r y owner may know which portions of i t s t e r r i t o r y are most productive, and which portions i t has v i s i t e d most recently. Consequently, a b i r d may in r e a l i t y obtain nectar from i t s t e r r i t o r y somewhat faster than i f i t foraged at random ( G i l l and Wolf 1977; Chapter 2). In June, t e r r i t o r i e s were c l e a r l y not an important source of energy. Given that insects removed most of the nectar produced on t e r r i t o r i e s , i t i s extremely unlikely that birds could have obtained energy faster than predicted on the basis of flower sampling. Further, estimates of d a i l y t e r r i t o r y energy production at that time of year were far below birds' minimum dai l y energy expenditures. For May, the results were not as c l e a r . At that time, Ribes was the only nectar source in the area, and was abundant on the t e r r i t o r i e s . I estimated that t e r r i t o r i e s were less p r o f i t a b l e than nearby undefended areas. However, given that birds removed a s i g n i f i c a n t portion of the Ribes nectar produced on their t e r r i t o r i e s , i t i s possible that their true rates of 68 energy a c q u i s i t i o n were h i g h e r than my e s t i m a t e s . E s t i m a t e s of t e r r i t o r y n e c t a r p r o d u c t i o n i n mid-May exceeded c a l c u l a t e d minimum energy e x p e n d i t u r e s , and n e c t a r p r o d u c t i o n on the t e r r i t o r i e s may have matched b i r d s ' energy r e q u i r e m e n t s c l o s e l y a t t h a t t i m e . T h e r e f o r e , even i f the presence of R i b e s bushes on t e r r i t o r i e s cannot i n i t s e l f account f o r t e r r i t o r y d e f e n s e , t h e s e bushes may be an i m p o r t a n t source of energy t o the b i r d s . P a r t I I of t h i s paper r e p o r t s the responses of C a l l i o p e males t o e x p e r i m e n t a l e x c l o s u r e of R i b e s bushes on t h e i r t e r r i t o r i e s i n May. I f t e r r i t o r i a l i t y i s energy-based, one of s e v e r a l responses s h o u l d o c c u r . B i r d s s h o u l d l e a v e t h e i r t e r r i t o r i e s e n t i r e l y , s h i f t or expand them t o i n c o r p o r a t e p e r i p h e r a l bushes, or c h a l l e n g e owners of a d j a c e n t t e r r i t o r i e s . I f t e r r i t o r i a l i t y i s not energy-based, b i r d s s h o u l d remain on t h e i r t e r r i t o r i e s . I f t e r r i t o r i a l i t y i s not energy-based, but R i b e s bushes on t h e i r t e r r i t o r i e s a r e n e v e r t h e l e s s an i m p o r t a n t s o u r c e of energy t o b i r d s , one of two t y p e s of responses s h o u l d o c c u r . B i r d s c o u l d i n c r e a s e the amount of time they spend f o r a g i n g o f f t h e i r t e r r i t o r i e s t o compensate f o r the l o s s of n e c t a r r e s o u r c e s . O t h e r w i s e , they c o u l d reduce t h e i r energy e x p e n d i t u r e by p e r c h i n g i n l e s s exposed l o c a t i o n s , or by r e d u c i n g p a r t i c i p a t i o n i n e n e r g e t i c a l l y c o s t l y a g o n i s t i c or c o u r t s h i p b e h a v i o r . 69 PART I I . RESPONSES OF MALES TO EXPERIMENTAL EXCLOSURE OF TERRITORY NECTAR SOURCES Methods On or before 6 May, I color-marked residents of t e r r i t o r i e s 1 through 6 by catching them in a feeder-baited trap, and painting their breast feathers by hand. I removed feeders from t e r r i t o r i e s immediately after birds were trapped so that the feeders would not influence their t e r r i t o r i a l behavior. Except for periods of a few hours when I placed feeders on t e r r i t o r y 5 on 30 May and t e r r i t o r y 6 on 2 and 16 June (see Chapter 4), there were no feeders on t e r r i t o r i e s after 7 May. On 9, 12, and 14 May, I observed birds on t e r r i t o r i e s 1 through 6 for 90 minutes each. These observations were divided into 3 separate sessions sta r t i n g at 6:30, 11:00, and 15:30. During each session, I started with t e r r i t o r y 1, and proceeded westward u n t i l I had observed, each bird for 30 minutes. During each 30 minute observation session, I recorded the identity of the resident bir d , a l l perches used, and divided the bird's time budget into 5 component a c t i v i t i e s : perching, foraging for nectar, agonistic or courtship behavior, off the t e r r i t o r y , and unaccounted for. If I observed a bird both f l y away from the t e r r i t o r y and return to the t e r r i t o r y , , I considered a l l time in the interim to have been spent off the t e r r i t o r y . Time unaccounted for occurred most frequently when birds flew behind vegetation or perched in inconspicuous locations. I used data on the positions of perches used by each b i r d each day to 70 calculate the sizes and locations of the t e r r i t o r i e s . On the evening of 14 May and throughout 15 May, I covered a l l Ribes bushes on or within 5 m of t e r r i t o r i e s 3 and 6 with transparent p l a s t i c sheeting and secured the sheeting with staples. I repeated the above observation procedure on a l l 6 t e r r i t o r i e s on 18, 20, and 22 May, and compared time budgets of birds on the 2 experimental t e r r i t o r i e s before and after Ribes exclosure. I used the other 4 t e r r i t o r i e s as controls. I conducted 3 further days of observation after the Ribes season on 1, 9, and 15 June, and compared time budgets with those observed in May. Results Both of the birds on experimental t e r r i t o r i e s continued to defend them while their Ribes bushes were covered, and they remained on those t e r r i t o r i e s u n t i l late in June. Of the 4 o r i g i n a l owners of the control t e r r i t o r i e s , one remained throughout the season, and 3 were replaced during May. Throughout most of June, each of the 6 t e r r i t o r i e s was held by a b i r d established by 30 May. Birds did not s h i f t their t e r r i t o r i e s s ubstantially after I covered their Ribes bushes. The per cent overlap with the t e r r i t o r i e s they defended on 9 May never f e l l below 50% on any subsequent day in May for either bird , and th e i r t e r r i t o r i e s did not expand (Fig. 3.8). In addition, neither bird was observed to challenge any other t e r r i t o r y owner. While his Ribes was covered, the owner of t e r r i t o r y 3 frequently entered t e r r i t o r y 2 71 £ 2 EXPERIMENTAL TERRITORIES CONTROL TERRITORIES rsi J 3000-L U M i/> 20004 >-cr o Q : U J 1000-exclosure MAY 10 MAY 20 MAY 10 MAY 20 Figure 3 . 8 . Changes in positions and sizes of t e r r i t o r i e s throughout May. Males continued to defend their t e r r i t o r i e s after I covered a l l Ribes bushes on them. 72 to feed, but was rarely detected by i t s owner. The only components of birds' time budgets that changed s i g n i f i c a n t l y in response to Ribes exclosure were were the amounts of time they spent foraging on their t e r r i t o r i e s and spent off their t e r r i t o r i e s (Fig. 3.9). Both birds spent more time off th e i r t e r r i t o r i e s , and th i s increase closely matched the loss of time foraging on their t e r r i t o r i e s . In contrast, during . the same time period, birds on control t e r r i t o r i e s increased t h e i r amount of time foraging, and decreased their amount of time spent off their t e r r i t o r i e s . In June, the time budgets of a l l 6 birds were very similar to those of the 2 experimental birds in May while Ribes was covered. At t h i s time, birds spent an average of only 0.06% of their time v i s i t i n g flowers on their t e r r i t o r i e s . Di scussion The responses of males to exclosure of their Ribes bushes support the conclusions I reached by sampling nectar on and off t e r r i t o r i e s (Part I ) . The increased time off the t e r r i t o r i e s indicates that these bushes were an important food source to the males, and i t i s possible that t h i s extra time off their t e r r i t o r i e s could have caused them some additional e f f o r t in t e r r i t o r y defense or caused them to lose courtship opportunities. However, the fact that the males retained their t e r r i t o r i e s indicates that their t e r r i t o r i a l i t y cannot be accounted for solely in energetic terms. Ewald (1980) observed that non-breeding Anna's Hummingbirds defended t e r r i t o r i e s 73 15-to U J 10-o o Z> m ui 5-Q m 15-EXPERIMENTA Ribes L TERRITORIES exclosure 6-~_ off "^-<> territory foraging ID-S' CONTROL TERRITORIES foragi i , off territory / MAY 9 - U MAY 18-22 JUNE 1 -15 Figure 3.9. Changes in time budgets of 2 males after I covered a l l Ribes bushes on th e i r t e r r i t o r i e s with p l a s t i c sheeting on 14 and 15 May. I observed similar changes in time budgets of 4 control birds in June after Ribes finished blooming. This r e f l e c t s the fact that there were no p r o f i t a b l e flowers on the t e r r i t o r i e s throughout June. Each point shown i s an average for 2 or 4 birds on 3 d i f f e r e n t days. V e r t i c a l bars indicate 95% confidence i n t e r v a l s based on arcsin vx" transformed data. 74 around a r t i f i c i a l feeders after those feeders were removed, but this period of defense never exceeded 2 days, even i f birds had previously held their t e r r i t o r i e s for 10-30 days. In contrast, the birds in t h i s study defended their t e r r i t o r i e s for 15 days while their Ribes bushes were covered, and for about 25 additional days in June while their t e r r i t o r i e s provided no pro f i t a b l e nectar sources. This study has documented that male North American hummingbirds sometimes defend breeding t e r r i t o r i e s with no pro f i t a b l e energy sources, and may do so even i f undefended s i t e s with abundant flowers are available nearby. However, i t is possible' that t h i s i s a f a i r l y rare phenomenon. The 6 t e r r i t o r i e s I studied were the f i r s t 6 established in the meadow, and these were a l l held throughout the breeding season. During May, however, as many as 5 additional males held t e r r i t o r i e s in the meadow (Fig. 3.2), and t h i s influx of males occurred at the peak of the Ribes flowering season. Defense of Ribes bushes may have played a more important role in the t e r r i t o r i a l i t y of these additional males. As well, I have observed Calliope males in surrounding areas whose t e r r i t o r i e s were centered around aggregations of C a s t i l l e j a inflorescenses. Nevertheless, although i t may not be t y p i c a l for Calliope males to hold t e r r i t o r i e s that do not provide energy, my results indicate that there are other important benefits of t e r r i t o r i a l i t y that sometimes outweigh energetic considerations. T e r r i t o r i e s without p r o f i t a b l e flowers may provide a p a r t i c u l a r l y good system for investigating the nature of these 75 benefits. One p o s s i b i l i t y not yet mentioned i s that t e r r i t o r i a l i t y may insure males access to other types of food. In p a r t i c u l a r , insects are an important component of birds' diets and may constitute their entire diet before Ribes blooms. Defense of insects could account for the frequent displays of males toward insectivorous passerine birds (Tamm 1985; Chapter 4). However, males do not feed on insects in locations where they are p a r t i c u l a r l y concentrated, but instead seem merely to hawk any insects that f l y by their perches. Therefore, i t seems i n t u i t i v e l y unlikely that insect prey are defendable. In addition, in cases in which other hummingbirds have been observed to feed primarily on arthropods (Wolf 1970; Montgomerie and Redsell 1982), they have not been t e r r i t o r i a l at those times. The more plausible hypothesis i s that t e r r i t o r i a l i t y increases males' reproductive success, and that t h i s increase i s not related to the p r o f i t a b i l i t y of flowers blooming on their t e r r i t o r i e s . During the Ribes season, I have seen females feeding on males' t e r r i t o r i e s . However, these females either remained undetected by males or evaded them immediately after detection. During observation sessions, I recorded only 18 separate courtship encounters between males and females, and thus i t i s impossible to quantit a t i v e l y compare encounter rates at times when t e r r i t o r i e s did and did not provide nectar. Nevertheless, these encounters were spaced f a i r l y evenly over the season, and 2 of the 18 occurred on experimental t e r r i t o r i e s 76 while Ribes was covered. These observations, along with the observation that males did not p r e f e r e n t i a l l y hold t e r r i t o r i e s in areas with the richest flowers, suggest that flowers on t e r r i t o r i e s do not have much eff e c t on reproductive success. If the primary benefit of t e r r i t o r y defense by males i s to maintain areas where they can encounter and court females without interference, there are several plausible explanations for their choice of t e r r i t o r y s i t e s . F i r s t , the t e r r i t o r i e s are d i r e c t l y adjacent to females' nesting areas (Fig. 3.1), so that females have easy access to them. Second, t h i s meadow i s f a i r l y devoid of vegetation except for grasses,.Ribes bushes and a few prominent perches. From these, males can e a s i l y observe intruders or females, and at the same time are v i s i b l e to females. Third, by choosing s i t e s without C a s t i l l e j a , males may reduce intrusion pressure from other males. Given that I observed interference by intruding males during 3 of the 18 observed interactions with females, i t seems reasonable that i t would be important for a male to maintain exclusive use of an area. If t e r r i t o r i e s primarily provide a courtship area, then the meadow can roughly be described as a lekking ground. However, a " c l a s s i c a l " lek consists of a communal display area (Bradbury 1981). Lekking i s common among the hermit hummingbird^ (Phaethorninae) (Nicholson 1931; Snow 1968; Snow 1974, 1977; S t i l e s and Wolf 1979) and may also occur in the North American Broad-tailed Hummingbirds (Selasphorus platycercus) (Barash 1972). Males of these species frequently vocalize and/or 77 display in clear view of one another and sometimes in synchrony. Barash (1972) noted that the 3 lekking Broad-tailed Hummingbirds he observed were each separated by only about 7 m. In contrast, during June in t h i s study, the average distance between centers of adjacent t e r r i t o r i e s held by Calliope males in the meadow was about 130 m. There was generally l i t t l e or no interaction between these males, and thus t h i s t e r r i t o r i a l i t y could not be defined as c l a s s i c a l lek behavior. However, Bradbury (1981) noted that in many species, "exploded leks" or "quasi-leks" occur in which males are barely within sight of each other. The t e r r i t o r i a l i t y of these Calliope males f a l l s best within t h i s category. 78 CHAPTER 4 WHAT DETERMINES THE SIZES OF BREEDING TERRITORIES HELD BY MALE CALLIOPE HUMMINGBIRDS? There are several e x i s t i n g models of optimal t e r r i t o r y size (Schoener 1983 and references therein; Ford 1983; Hixon et a l . 1983; Lima 1984, 1986; Jones and Krummel 1985) which deal s p e c i f i c a l l y with energy-based feeding t e r r i t o r i e s . Consequently, most empirical studies on t e r r i t o r y size have been in t e n t i o n a l l y r e s t r i c t e d to the non-breeding season, at which time i t i s thought the costs and benefits of t e r r i t o r i a l i t y can be expressed solely in terms of energy (Pyke 1979; D i l l et a l . 1981; Myers et a l . 1981; Carpenter et a l . 1983; Hixon et a l . 1983; Davies and Houston 1 984; Houston et a_l. 1985). However, among birds in p a r t i c u l a r , t e r r i t o r i a l i t y i s most prevalent during the breeding season, and the most conspicuous and aggressively defended t e r r i t o r i e s are often held at that time (Welty 1982). It i s l i k e l y that the reproductive success of male hummingbirds i s affected by the sizes of their breeding t e r r i t o r i e s . Davies and O'Donald (1976) and Harper (1985) found that male a r c t i c skuas (Catharacta skua) and robins (Erithacus  rubecula) that held large t e r r i t o r i e s at the beginning of the breeding season were more l i k e l y to obtain mates than males holding smaller t e r r i t o r i e s . In promiscuous breeders such as 79 hummingbirds, the effect of breeding t e r r i t o r y size on males' a b i l i t i e s to obtain mates could be even more pronounced due to the p o t e n t i a l l y great variation in the reproductive success of males. In t h i s chapter, I address the question of what determines the sizes of t e r r i t o r i e s defended by male Calliope Hummingbirds at my study s i t e . I propose a general model of optimal t e r r i t o r y size for a breeding male that obtains a l l i t s energy from outside i t s t e r r i t o r y . This model i s similar to those of energy-based t e r r i t o r i a l i t y (Schoener 1983, and references therein) in that I assume that the cost of t e r r i t o r y defense in time and energy increases with t e r r i t o r y size. It d i f f e r s in that I assume that the relevant currency i s access to females rather than energy, and that the optimal t e r r i t o r y size i s that which maximizes the reproductive success of a male, subject to the constraint that he s a t i s f y his maintenance energetic requirements. The model predicts how this optimal size could be affected by several environmental factors. I performed an experiment on a male Calliope Hummingbird's t e r r i t o r y to test the prediction that a male's t e r r i t o r y size w i l l increase i f his rate of energy intake while foraging away from his t e r r i t o r y increases. 80 The Model Access to females If a male's t e r r i t o r y provides no food, he must spend at least some " minimum • time foraging away from his t e r r i t o r y each day in order to meet his baseline energy requirements. His remaining time can p o t e n t i a l l y be spent courting females. I w i l l assume that a male has sole access to a l l females that enter his t e r r i t o r y , and that he courts a l l females he detects. The f i r s t factor that could l i m i t a male's optimal t e r r i t o r y size i s saturation with available females. Each time a male encounters a female, he spends both time and energy courting that female. To recover energy lost in courtship, the male must spend extra time foraging away from his t e r r i t o r y . The sum of these two time components represents the time during which the male i s unavailable to court other females that enter his t e r r i t o r y . If T = the t o t a l time available per day to court females, F = the number of detectable females entering the t e r r i t o r y during that time, and t c = the t o t a l time spent per female, then the number of females the male can court is approximated by T p T + F t c However, i f F t c « T, t h i s value approaches F (see Appendix for d e t a i l s ) . In 81 h of observations of t e r r i t o r i a l Calliope males on 6 t e r r i t o r i e s in 1985 (Chapter 3), I observed only 18 encounters with females, or one encounter for every 4.5 h on average. Therefore, i t i s unlikely that saturation with females 81 i s an important f a c t o r l i m i t i n g t e r r i t o r y s i z e , and i t i s r e a l i s t i c to assume that a male can attempt c o u r t s h i p with a l l females he d e t e c t s on h i s t e r r i t o r y . The number of females that enter a male's t e r r i t o r y per day, and can be dete c t e d by him i f he i s present, i s l i k e l y to be an i n c r e a s i n g f u n c t i o n of t e r r i t o r y a r e a . Because t h i s r e l a t i o n s h i p i s not n e c e s s a r i l y l i n e a r , I w i l l assume i t to be an a l l o m e t r i c f u n c t i o n of the form z f F = f k, A where f i s d e n s i t y of females i n the area, A i s t e r r i t o r y area, and kf and Zf are c o n s t a n t s . However, i f the owner must defend h i s t e r r i t o r y from i n t r u d i n g males, he cannot spend a l l h i s time surveying h i s t e r r i t o r y , and the number of females he a c t u a l l y encounters w i l l be l e s s than F. The c o s t of defense w i l l l i k e l y a l s o be an i n c r e a s i n g f u n c t i o n of t e r r i t o r y a r ea. Cost of defense Because energy spent c h a s i n g i n t r u d e r s must be recovered through e x t r a time f o r a g i n g , the e n t i r e cost of e x p e l l i n g i n t r u d e r s can be expressed in u n i t s of time. I w i l l assume that the t o t a l temporal c o s t of e x p e l l i n g i n t r u d e r s i s a l s o an a l l o m e t r i c f u n c t i o n of t e r r i t o r y area of the form time lost = ik ;A 2 ' where i = the d e n s i t y of p o t e n t i a l i n t r u d e r s i n the area, and k-, and Z-, are c o n s t a n t s . I f T i s the amount of time p o t e n t i a l l y 82 a v a i l a b l e f o r c o u r t i n g females, t a k i n g i n t o account the b a s e l i n e f o r a g i n g requirement f o r meeting maintenance c o s t s , the number of females the male encounters per day as a f u n c t i o n of t e r r i t o r y s i z e i s f (A) = (T - i k; A Z ) f k (A Z < As long as a l l these parameters are g r e a t e r than zero, t h i s f u n c t i o n i s maximized when A - I" ^ ] Z' iki(zT4-z[) T h e r e f o r e , optimal t e r r i t o r y s i z e i n c r e a s e s with T and Z j , and decreases with i , k;, and Z; . The above equation suggests some f a c t o r s that c o u l d i n f l u e n c e s i z e s of breeding t e r r i t o r i e s defended by males. L i k e energy-based models ( D i l l 1978; Hixon 1980), t h i s model p r e d i c t s that t e r r i t o r y s i z e w i l l decrease i n response t o i n c r e a s e s i n i n t r u d e r p r e s s u r e . The co s t of e x p e l l i n g those i n t r u d e r s c o u l d a l s o vary a c c o r d i n g to h a b i t a t . In a h a b i t a t i n which i n t r u d e r s were d i f f i c u l t t o d e t e c t , t h i s c o s t c o u l d be hig h on average (high k; ) and a c c e l e r a t e s h a r p l y ( Z; >> 1) with d i s t a n c e from the c e n t e r of the t e r r i t o r y , r e s u l t i n g i n a small optimal t e r r i t o r y s i z e . S i m i l a r l y , a sharp decrease with d i s t a n c e i n a male's a b i l i t y t o d e t e c t females ( z f << 1) would l i m i t optimal t e r r i t o r y s i z e . One p r e d i c t i o n p a r t i c u l a r l y amenable to experimental t e s t i n g i s that a male's t e r r i t o r y s i z e w i l l i n c r e a s e i n response t o i n c r e a s e s i n the r a t e at which he can ob t a i n energy 83 w h i l e f o r a g i n g away f r o m h i s t e r r i t o r y . I f a m a l e c o u l d o b t a i n e n e r g y a t a f a s t e r r a t e , i t s h o u l d d e c r e a s e b o t h h i s b a s e l i n e t i m e r e q u i r e d t o o b t a i n m a i n t e n a n c e e n e r g y ( i n c r e a s e d T) a n d h i s t i m e r e q u i r e d t o r e c o v e r e n e r g y l o s t w h i l e e x p e l l i n g i n t r u d e r s ( d e c r e a s e d k ; ) . I f t h e s e c h a n g e s w e r e s i g n i f i c a n t , o p t i m a l t e r r i t o r y s i z e s h o u l d c o n s e q u e n t l y i n c r e a s e . I t e s t e d t h i s p r e d i c t i o n by u s i n g a f e e d e r t o i n c r e a s e t h e r a t e a t w h i c h a t e r r i t o r i a l C a l l i o p e H u m m i n g b i r d c o u l d o b t a i n e n e r g y w h i l e f o r a g i n g away f r o m h i s t e r r i t o r y . M e t h o d s The m a l e I s t u d i e d d e f e n d e d t e r r i t o r y 6 ( F i g . 3 . 1 ) t h r o u g h o u t m o s t o f May a n d J u n e 1 9 8 5 . B e f o r e t h e e x p e r i m e n t , he p r i m a r i l y u s e d 3 p e r c h e s w i t h i n 10 m o f one a n o t h e r a t t h e S e n d o f t h e t e r r i t o r y . F o r t h i s e x p e r i m e n t , I p l a c e d a 3 m h i g h m e t a l p e r c h i n t h a t a r e a , w h i c h he u s e d a l m o s t e x c l u s i v e l y t h e r e a f t e r , a n d m e a s u r e d t h e d i s t a n c e N on t h i s p e r c h o v e r w h i c h he e x p e l l e d i n t r u d e r s ( F i g . 4 . 1 ) . On 2 J u n e , I p l a c e d a c o n s p i c u o u s l y c o l o r e d f e e d e r c o n t a i n i n g a 30% w/w s u c r o s e s o l u t i o n on t h e t e r r i t o r y . A f t e r 1 h , by w h i c h t i m e t h e o w n e r h a d b e g u n t o u s e t h e f e e d e r , I r e p l a c e d i t w i t h a n i n c o n s p i c u o u s c l e a r g l a s s b o t t l e c o n t a i n i n g a s i m i l a r s o l u t i o n . I p e r i o d i c a l l y moved t h i s f e e d e r b y i n c r e m e n t s o f a b o u t 5 m u n t i l i t was l o c a t e d w e l l o f f t h e t e r r i t o r y a b o u t 30 m SW o f t h e m e t a l p e r c h i n a g r o v e o f t r e e s . A t t h i s l o c a t i o n , t h e f e e d e r was v i s i t e d f r e q u e n t l y by t h e t e r r i t o r y o w n e r , b u t was n e v e r d i s c o v e r e d by a n y o t h e r b i r d . 84 INCONSPICUOUS METAL PERCH gravel road 0 20 m DOUGLAS FIR COVER > 2 m DECIDUOUS COVER > 2 m x DECOY FEEDER Figure 4.1. Design of experiment to examine the e f f e c t of energy a v a i l a b i l i t y on the size of t e r r i t o r y defended by a male Calliope Hummingbird. The male perched primarily on a metal perch provided, and defended the area N of that perch. Intruders entered the t e r r i t o r y to sample conspicuous decoy feeders containing either water or a r t i f i c i a l sweetener. On 5 of the 10 mornings on which the experiment was conducted, the male had access to an inconspicuous feeder outside his t e r r i t o r y containing a 30% w/w sucrose solution. 85 On 2 June, I also placed 6 feeders containing a 20% w/w sucrose solution on the opposite side of the gravel road N of the t e r r i t o r y (Fig. 4.1). These feeders were discovered and used by several male and female Calliope Hummingbirds and a few Rufous Hummingbirds. On 7 June, I replaced 4 of these with decoy feeders, 2 containing pure water and 2 containing a r t i f i c i a l sweetener (Sucaryl; Abbott Laboratories) of equivalent sweetness to the sugar solution. I subsequently shuffled the locations of these feeders every few hours in order to t r a i n these birds to continually sample the decoys. I used the a r t i f i c i a l sweetener simply to create another category of decoy feeders the birds needed to sample; birds e a s i l y distinguished i t from the real sucrose solution. I conducted the experiment from 06:30 to 09:00 on 10 mornings from 11-14 and 17-22 June. I measured t e r r i t o r y size by placing decoy feeders 5, 15, 25, 35, and 45 m N of the metal perch (Fig. 4.1), and observing the proportion of intruders sampling each of these feeders that were chased or displayed to by the owner. I compared the p r o b a b i l i t i e s of response at each distance on mornings when the inconspicuous feeder was and was not a vailable to determine i f the owner increased his t e r r i t o r y size when he had access to his feeder. The experiment consisted of 5 pairs of days, with th i s feeder available on one randomly selected day of each p a i r . On mornings on which his feeder was avail a b l e , he began v i s i t i n g i t at about 05:00, and therefore had been feeding from i t for about 1 1/2 h before the experiment began. On other mornings, the feeder was gone when he awoke. 86 At 09:00 each day, I replaced the owner's inconspicuous feeder i f i t had been removed the night before the experiment. I also moved a l l decoy feeders N of the gravel road, and f i l l e d two of them with sucrose solution. After dark each night, I replaced these sucrose containing feeders with decoys, placed 6 decoys in the positions shown in F i g . 4.1, and covered a l l of them with opaque p l a s t i c bags u n t i l 06:30 the next morning. On 16 June, when I didn't conduct observations, I placed 2 sucrose containing feeders and 3 decoys on the t e r r i t o r y from 06:30 to 08:30. This was to prevent intruders from learning that feeders in those positions never contained sucrose. No sucrose containing feeders were placed on the t e r r i t o r y at any other time during the experiment. Results The presence of the owner's feeder did not have a noticeable e f f e c t on the size of t e r r i t o r y he defended (Fig. 4.2). The data indicate f a i r l y c l e a r l y that there was not much difference in the owner's p r o b a b i l i t y of responding to an intruding male at any distance when his feeder was and was not available (Fig. 4.2a). For 8 of 481 v i s i t s to decoy feeders by intruders, I could not i d e n t i f y the species and/or sex of the b i r d , but the results were not noticeably affected by the inclusion or exclusion of these data. There were too few intrusions by females to obtain reasonable estimates of the owner's pr o b a b i l i t y of responding to 87 5 15 25 35 45 DISTANCE OF INTRUDER FROM PERCH (m) F i g u r e 4.2. Comparison of t e r r i t o r y d e f e nse when the male d i d and d i d not have a c c e s s t o the a r t i f i c i a l f e e d e r o u t s i d e h i s t e r r i t o r y . V e r t i c a l b a r s r e p r e s e n t 95% c o n f i d e n c e i n t e r v a l s f o r p r o b a b i l i t i e s of r e s p o n s e . These d a t a i l l u s t r a t e t h a t a v a i l a b i l i t y of the fee d e r d i d not s i g n i f i c a n t l y a f f e c t t e r r i t o r y s i z e . Responses t o females p r o b a b l y c o n s t i t u t e d a t t e m p t e d c o u r t s h i p r a t h e r than t e r r i t o r y d e f e n s e . 88 them at each distance. It is possible that his p r o b a b i l i t i e s of responding to males and females were quite similar (Fig. 4.2b). The natures of the responses, however, were quite d i f f e r e n t . The owner chased males in 83 of 84 encounters, but only chased females in 7 of 27 encounters. He dive-displayed at females in 21 of those 27 encounters, but never dive-displayed at males at a l l . He began dive ascents 5 to 10m before reaching females, and continued to dive at them and perform other displays u n t i l they perched in inconspicuous locations or flew away from the t e r r i t o r y . This type of behavior probably constituted attempted courtship rather than aggression. Although the presence of the inconspicuous feeder did not noticeably a f f e c t the owner's t e r r i t o r y size, i t did s i g n i f i c a n t l y a f f e c t other aspects of his behavior. When the inconspicuous feeder was available, he performed many more dive displays toward birds not v i s i t i n g decoy feeders (p = 0.008; Mann-Whitney U test; F i g . 4.3a). Most of these dives were directed at passerine birds including flycatchers (Empidonax sp.), Nashville Warblers (Vermivora r u f i c a p i l l a ) , Rufous-sided Towhees ( P i p i l o erythrophthalmus), and American Robins (Turdus  migratorius). This result indicates that the presence of the feeder did influence the owner's energetic state, and that at least some aspects of his*behavior were normally energy limited. In addition, when the feeder was available, there were fewer chases of Calliope males not v i s i t i n g decoy feeders (p = 0.008; Mann-Whitney U test; F i g . 4.3b). 8 9 F i g u r e 4 . 3 . D i f f e r e n c e s i n t h e n u m b e r o f ( a ) d i v e d i s p l a y s a n d ( b ) c h a s e s b y t h e t e r r i t o r y o w n e r w h e n h e h a d a c c e s s t o a f e e d e r . M o s t d i v e d i s p l a y s w e r e d i r e c t e d a t p a s s e r i n e b i r d s r a t h e r t h a n h u m m i n g b i r d s . C h a s e s n o t e d h e r e a r e t h o s e o f i n t r u d i n g m a l e s n o t v i s i t i n g d e c o y f e e d e r s . T h e s e i n t r u s i o n s , w h i c h m a y h a v e a l l b e e n b y a s i n g l e m a l e , a p p e a r e d t o c o n s t i t u t e c h a l l e n g e s f o r t h e t e r r i t o r y . 90 Di scussion Given that the experiment was performed on only one t e r r i t o r y , extrapolation of the results should be done with caution. Nevertheless, the results do suggest insights into the nature of t e r r i t o r i a l i t y of at least that one male. The result that improved access to energy did not af f e c t the owner's t e r r i t o r y s i z e , but did influence other aspects of his behavior raises two questions. F i r s t , could the changes in behavior after energy manipulation have influenced his reproductive success? Second, what factors did determine the size of his t e r r i t o r y ? Does energy effect males' reproductive success? Tamm (1985) also observed that Calliope males at the same s i t e increased their frequency of dive displays when given access to a feeder. However, given that most of the dives observed in both studies were at passerines, i t i s not clear i f or how males benefit from t h i s energy expenditure. Perhaps passerines provide stimuli similar to but weaker than those of intruding hummingbirds, so that responses occur only i f t e r r i t o r y owners' energetic constraints are reduced. The decreased number of chases of intruding males not v i s i t i n g decoy feeders may be more indicative of an effect on reproductive success. Most of these chases occurred after an intruder flew within 1 m of the owner and appeared to challenge him. The owner appeared to expel intruders more quickly and vigorously when his inconspicuous feeder was av a i l a b l e . 91 Intruders may consequently have been less persistent on those days, resulting in the lower frequency of chases. If a t e r r i t o r i a l male's energetic state a f f e c t s his a b i l i t y to dominate intruders, i t may a f f e c t his a b i l i t y to es t a b l i s h and hold a t e r r i t o r y . Therefore, although the results of the experiment suggest that energy a c c e s s i b i l i t y does not normally l i m i t t e r r i t o r y size, i t could nevertheless be an important determinant of a male's reproductive success. What does determine t e r r i t o r y size? Other than access to energy, possible factors influencing t e r r i t o r y size suggested by the model were intruder pressure and intruder d e t e c t a b i l i t y . The results of the experiment suggest the p o s s i b i l i t y that the size of the t e r r i t o r y was limited only by the owner's a b i l i t y to detect intruders. This hypothesis accounts for the gradual decrease in his responsiveness with distance and the f a i r l y similar p r o b a b i l i t i e s of his responding to males and females. A b i l i t y to detect intruders may generally impose an absolute upper l i m i t on t e r r i t o r y s i z e . Given that the t e r r i t o r i e s defended by Calliope males at th i s study s i t e are probably larger than t y p i c a l for hummingbirds (Fig. 3 . 8 ) , i t should perhaps not be surprising i f their sizes are limited only by detection a b i l i t y . Time and energy constraints may be more important for species such as the hermit hummingbirds, which hold small t e r r i t o r i e s on " c l a s s i c a l " leks. However, given that male hermits generally hold t e r r i t o r i e s in densely wooded areas 92 where v i s i b i l i t y i s poor (Skutch 1964), i t may be impossible for them to defend anything but very small t e r r i t o r i e s . As well, because male hermits are t i g h t l y packed on leks, t e r r i t o r y size may be primarily determined by inter-lek spacing and the number of males on each lek (Bradbury 1981). Energy manipulation experiments similar to that reported in t h i s chapter could be used to d i s t i n g u i s h between these p o s s i b i l i t i e s . 93 Appendix Female s a t u r a t i o n T = the l e n g t h of time a v a i l a b l e per day f o r pe r c h i n g F = the number of d e t e c t a b l e females e n t e r i n g the t e r r i t o r y d u r i n g that time C = the number of females that the male c o u r t s t c = the amount of pe r c h i n g time the male l o s e s per female he c o u r t s Because the male spends t c u n i t s of time c o u r t i n g each of c females, the p r o p o r t i o n of h i s time that he spends c o u r t i n g i s Assuming that the p r o b a b i l i t y of a female e n t e r i n g h i s etc T t e r r i t o r y i s independent of whether he i s busy c o u r t i n g another female, the number of l o s t c o u r t s h i p o p p o r t u n i t i e s w i l l be Fct c F - c = — -T h e r e f o r e c = FT _ TF , Ft c T + Ft c 1 - — As F approaches co , c approaches J L . As e i t h e r t c or F approach 0, c approaches F. 94 I n t r u d e r p r e s s u r e A = t e r r i t o r y area f = d e n s i t y of females f k f A Z < = the number of females the male e n c o u n t e r s per a v a i l a b l e time T = p o t e n t i a l p e r c h i n g t ime per day i = d e n s i t y of i n t r u d i n g males i k ; A Z | = t ime spent c h a s i n g i n t r u d e r s or f o r a g i n g to r e c o v e r energy l o s t w h i l e c h a s i n g i n t r u d e r s The amount of time a v a i l a b l e to c o u r t females i s T - i k , A T h e r e f o r e , the number of females e n c o u n t e r e d as a f u n c t i o n of t e r r i t o r y s i z e i s f ( A ) = ( T - i k , A ) f k « A *m = Z f f k ^ A ^ ^ z ^ ^ i k . - f k f A 2 ^ 2 ' - 1 • A 1 i f d f ( A > - 0 ^en A = d A T h e r e f o r e , t h e r e i s a s i n g l e i n f l e c t i o n p o i n t which i s d e f i n e d as l o n g as z ; * 0. i k i ( z T + - z ; ) 95 d f(A) _ dA = f k f A Z f " 2 ^ z r 1 ^ z fT - ^ z + + z f - i ^ z , + Z f jikj A2 S u b s t i t u t i n g t h e v a l u e of Az, a t t h e i n f l e c t i o n p o i n t y i e l d s d f * A ) = -z,z f k f fTA dA B e c a u s e a l l t h e component p a r a m e t e r s a r e a l w a y s p o s i t i v e , t h i s v a l u e i s a l w a y s n e g a t i v e . T h e r e f o r e , t h e v a l u e o f f(A) a t i t s i n f l e c t i o n p o i n t i s a l w a y s a maximum, and t h e v a l u e of a t t h a t p o i n t i s t h e o p t i m a l t e r r i t o r y a r e a . 96 CHAPTER 5 CONCLUDING REMARKS The research presented in t h i s thesis extends e a r l i e r work on t e r r i t o r i a l behavior of North American hummingbirds. The results in turn suggest further questions about t e r r i t o r i a l i t y of hummingbirds in p a r t i c u l a r , and about t e r r i t o r i a l i t y , foraging behavior, and mating systems in general. In this chapter, I b r i e f l y review the primary results of each study, and discuss p r o f i t a b l e directions for further research. The simulations in Chapter 2 suggest that a hummingbird foraging on an energy-based feeding t e r r i t o r y could benefit by avoiding flowers v i s i t e d recently during a foraging bout, but would not benefit s i g n i f i c a n t l y by avoiding patches v i s i t e d on previous bouts. This result provides a plausible explanation for the observation that, while hummingbirds r e v i s i t flowers less often than would be expected by chance, there i s no apparent pattern to the locations at which they i n i t i a t e foraging bouts (Sutherland, in prep.). Further empirical work on systematic foraging of hummingbirds should therefore concentrate on observations of within-bout foraging movements. The simulations suggest that short-term avoidance of flowers would not only allow a higher immediate rate of energy intake to a b i r d , but would allow i t to create a coarse-grained s p a t i a l d i s t r i b u t i o n of nectar a v a i l a b i l i t y that i t could exploit e a s i l y later on. Although i t has been acknowledged in the foraging theory l i t e r a t u r e that coarse-grained d i s t r i b u t i o n s 97 of food a v a i l a b i l i t y can be exploited more e f f i c i e n t l y (Green 1984), I know of no previous studies that have dealt with the p o s s i b i l i t y that creation of such d i s t r i b u t i o n s may be an important component of foraging strategies. Further theoret i c a l developments might p r o f i t a b l y address this issue, as well as the cl o s e l y related issue of whether the foraging strategies that provide the highest immediate rate of energy intake are the best strategies over a longer time scale. The results of Chapter 3 confirm the suggestion (Ewald 1980; Hixon 1980) that purely energy-based models do not account for the behavior of t e r r i t o r i a l hummingbirds during the breeding season. Although th i s study indicates that other benefits of t e r r i t o r i a l i t y must sometimes outweigh energetic considerations, i t only s u p e r f i c i a l l y deals with the issues of what those benefits are, and what therefore determines the preferred locations of t e r r i t o r i e s . Because t e r r i t o r i e s were situated around prominent perches adjacent to females' nesting areas, i t is plausible that locations with these c h a r a c t e r i s t i c s may be p a r t i c u l a r l y good for a t t r a c t i n g and courting females. Given that males readily use a r t i f i c i a l perches, t h i s hypothesis might be addressed by attempting to manipulate q u a l i t y of existing t e r r i t o r i e s and to create t e r r i t o r i e s in previously unused locations by strategic location of such perches. This approach would be analogous to manipulating quality of energy-based non-breeding t e r r i t o r i e s using feeders (Ewald and Carpenter 1978; Ewald 1980, 1985). Chapter 4 suggests possible factors determining the sizes 98 rather than the locations of t e r r i t o r i e s . Results of an experiment performed on one male's t e r r i t o r y suggest that t e r r i t o r y size might simply be limited by males' a b i l i t i e s to detect intruders. However, repetition of t h i s experiment i s needed to determine the generality of the conclusion that t e r r i t o r y size i s not limited by the time and energy required to expel intruders. It would also be useful to perform comparative experiments on male hermit hummingbirds, some of which defend much smaller breeding t e r r i t o r i e s containing no energy sources (Skutch 1964; Snow 1968; Snow 1974; S t i l e s and Wolf 1979). Although hummingbird t e r r i t o r i a l behavior i s probably more complex during the breeding season than at other times, I f e e l that research conducted during the breeding season may ultimately prove the most rewarding. At present, more research is needed in order to understand the proximate factors determining preferred s i t e s for t e r r i t o r i e s and sizes of t e r r i t o r i e s . It should be possible to obtain t h i s information by observing the behavioral responses of t e r r i t o r i a l males to manipulations of their environments, as I have described above. Understanding of these proximate factors w i l l lead to two further questions. F i r s t , what determines which males hold t e r r i t o r i e s , and which males hold t e r r i t o r i e s on preferred sites? Second, i s a male's reproductive success affected by whether or not he holds a t e r r i t o r y and/or by the size and location of his t e r r i t o r y ? Given that observed encounters between male and female hummingbirds are infrequent, measurements of the reproductive 99 s u c c e s s of males w i l l p r o b a b l y be d i f f i c u l t t o o b t a i n . However, such measurements w i l l a l l o w d i r e c t i n v e s t i g a t i o n of the p o s s i b i l i t y t h a t n a t u r a l s e l e c t i o n t a k e s p l a c e among males on the b a s i s of t h e i r t e r r i t o r i a l b e h a v i o r . T h i s would be an e x c i t i n g avenue of i n v e s t i g a t i o n , and one not c l e a r l y open t o s t u d i e s of non- b r e e d i n g t e r r i t o r i a l i t y . 100 LITERATURE CITED Ald r i c h , E.C. 1939. 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