Food Intake versus ability to flee among birds, particularly the hummingbird?

Food Intake versus ability to flee among birds, particularly the hummingbird?

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Logically speaking, if a hummingbird drinks too much nectar, it will be temporarily overweight and less able or unable to fly to escape danger. However if the same hummingbird doesn't drink enough nectar, it will suffer the same problem of not being able to flee danger, but for the different reason of it wouldn't have enough energy to do so. Hummingbirds are incredibly small, so I would assume they would have the most problem with this issue due to the fact it would have very little margin for error. I am not sure how much that margin is though or the marginal percent of body weight, so I'll ask that question too.

What mechanisms do (humming)birds have to regulate and control their body weight and their energy needs and scouting and timing the acquisition of their next potential food source? What is their margin for error and how do they meet it and how did they meet it in the past?

EDIT: I want a more concise question, so hopefully this is answerable:

Alternatively and optionally, Can you describe to me a general day in the life of a Hummingbird? I want to know what good decisions it makes over the course of its "perfectly average" day to survive. Such things as what it does to avoid dangers, and how it finds its time to eat and how much it eats and at what intervals, and what it does with the rest of its time?


  • 1 Behavioural Biology, Institute of Biology Leiden and Leiden Institute for Brain and Cognition, Leiden University, Leiden, Netherlands
  • 2 Amsterdam Brain and Cognition, Institute for Logic Language and Computation, University of Amsterdam, Amsterdam, Netherlands

While humans can easily entrain their behavior with the beat in music, this ability is rare among animals. Yet, comparative studies in non-human species are needed if we want to understand how and why this ability evolved. Entrainment requires two abilities: (1) recognizing the regularity in the auditory stimulus and (2) the ability to adjust the own motor output to the perceived pattern. It has been suggested that beat perception and entrainment are linked to the ability for vocal learning. The presence of some bird species showing beat induction, and also the existence of vocal learning as well as vocal non-learning bird taxa, make them relevant models for comparative research on rhythm perception and its link to vocal learning. Also, some bird vocalizations show strong regularity in rhythmic structure, suggesting that birds might perceive rhythmic structures. In this paper we review the available experimental evidence for the perception of regularity and rhythms by birds, like the ability to distinguish regular from irregular stimuli over tempo transformations and report data from new experiments. While some species show a limited ability to detect regularity, most evidence suggests that birds attend primarily to absolute and not relative timing of patterns and to local features of stimuli. We conclude that, apart from some large parrot species, there is limited evidence for beat and regularity perception among birds and that the link to vocal learning is unclear. We next report the new experiments in which zebra finches and budgerigars (both vocal learners) were first trained to distinguish a regular from an irregular pattern of beats and then tested on various tempo transformations of these stimuli. The results showed that both species reduced the discrimination after tempo transformations. This suggests that, as was found in earlier studies, they attended mainly to local temporal features of the stimuli, and not to their overall regularity. However, some individuals of both species showed an additional sensitivity to the more global pattern if some local features were left unchanged. Altogether our study indicates both between and within species variation, in which birds attend to a mixture of local and to global rhythmic features.

5| Resource Acquisition and Allocation

Ecological events and their outcomes, such as growth, reproduction, photosynthesis, primary production, and population size, are often regulated by the availability of one or a few factors or requisites in short supply, whereas other resources and raw materials present in excess may go partially unused. This principle has become known as the " law of the minimum" (Liebig 1840). For instance, in arid climates, primary production (the amount of solar energy trapped by green plants) is strongly correlated with precipitation (Figure 5.1) here water is a " master limiting factor." Of many different factors that can be limiting, frequently among the most important are various nutrients, water, and temperature.

When considering populations, we often speak of those that are food-limited, predator-limited, or climate-limited. Populations may be limited by other factors as well for example, density of breeding pairs of blue tits (Parus caeruleus) in an English woods was doubled by the addition of many new nesting boxes (Lack 1954, 1966), providing an indication that nest sites were limiting. However, limiting factors are not always so clear-cut but may usually interact so that a process is limited simultaneously by several factors, with a change in any one of them resulting in a new equilibrium. For instance, both increased food availability and decreased predation pressures might result in a larger population size.

A related concept, developed by Shelford (1913b), is now known as the " law of tolerance." Too much or too little of anything can be detrimental to an organism. In the early morning, a desert lizard finds itself in an environment that is largely too cold, whereas later in the day its environment is too hot. The lizard compensates somewhat for this by spending most of its time during the early morning in sunny places, whereas later on most of its activities take place in the shade. Each lizard has a definite optimal range of temperature, with both upper and lower limits of tolerance. More precisely, when measures of performance (such as fitness, survivorship, or foraging efficiency) are plotted against important environmental variables, bell-shaped curves usually result (for examples, see Figures 5.2 and 5.8).

Organisms can be viewed as simple input-output systems, with foraging or photosynthesis providing an input of materials and energy that are in turn "mapped" into an output consisting of progeny. Fairly extensive bodies of theory now exist both on optimal foraging and reproductive tactics (see next chapter). In optimal foraging theory, the "goal" usually assumed to be maximized is energy uptake per unit time (successful offspring produced during an organism's lifetime would be a more realistic measure of its foraging ability, but fitness is exceedingly difficult to measure). Similarly, among organisms without parental care, reproductive effort has sometimes been estimated by the ratio of calories devoted to eggs or offspring over total female calories at any instant (rates of uptake versus expenditure of calories have unfortunately not yet infiltrated empirical studies of reproductive tactics). To date, empirical studies of resource partitioning have been concerned largely with "input" phenomena such as overlap in and efficiency of resource utilization and have neglected to relate these to "output" aspects. In contrast, empirical studies of reproductive tactics have done the reverse and almost entirely omitted any consideration of foraging. Interactions and constraints between foraging and reproduction have barely begun to be considered. A promising area for future work will be to merge aspects of optimal foraging with optimal reproductive tactics to specify rules by which input is translated into output optimal reproductive tactics ("output" phenomena) surely must often impose substantial constraints upon "input" possibilities and vice versa.

Any organism has a limited amount of resources available to devote to foraging, growth, maintenance, and reproduction. The way in which an organism allocates its time and energy and other resources among various conflicting demands is of fundamental interest because such apportionments provide insight into how the organism copes with and conforms to its environment. Moreover, because any individual has finite resource and energy budgets, its capacity for regulation is necessarily limited. Organisms stressed along any one environmental variable are thus able to tolerate a lesser range of conditions along other environmental variables. Various tolerance and performance curves (Figure 5.2) are presumably subject to certain constraints. For example, their breadth (variance) usually cannot be increased without a simultaneous reduction in their height and vice versa (Levins 1968). This useful notion of trade-offs, known as the principle of allocation, has proven to be quite helpful in interpreting and understanding numerous ecological phenomena.

As an example of allocation, imagine an animal of a given size and mouth-part anatomy. A certain size of prey item is optimal, whereas other prey are suboptimal because they are either too large or too small for efficient capture and swallowing. Any given animal has its own "utilization curve" that indicates the actual numbers of prey of different sizes taken per unit time under particular environmental conditions. In an idealized, perfectly stable, and infinitely productive environment, a utilization curve might become a spike with no variance, with the organism using only its most optimal prey resource type. In actuality, limited and changing availabilities of resources, in both time and space, result in utilization curves with breadth as well as height. In terms of the principle of allocation, an individual with a generalized diet adapted to eat prey of a wide range of available sizes presumably is not so effective at exploiting prey of intermediate size as another, more specialized, feeder. In other words, a jack-of-many-trades is a master of none. We will consider this subject in more detail later.

Time, matter, and energy budgets vary widely among organisms. For example, some creatures allot more time and energy to reproduction at any instant than do others. Varying time and energy budgeting is a potent means of coping with a changing environment while retaining some degree of adaptation to it. Thus, many male songbirds expend a great deal of energy on territorial defense during the breeding season but little or none at other times of the year. Similarly, in animals with parental care, an increasing amount of energy is spent on growing offspring until some point when progeny begin to become independent of their parents, whereupon the amount of time and energy devoted to them decreases. Indeed, adult female red squirrels, Tamiascurus, at the height of lactation consume an average of 323 kilocalories of food per day compared with an average daily energy consumption of a similar-sized adult male of only about 117 kilocalories (C. Smith 1968). The time budgets of these squirrels also vary markedly with the seasons.

In a bad dry year, many annual plants "go to seed" while still very small, whereas in a good wet year, these plants grow to a much larger size before becoming reproductive presumably more seeds are produced in good years, but perhaps none (or very few) would be produced in a bad year if individuals attempted to grow to the sizes they reach in good years.

An animal's time and energy budget provides a convenient starting point for clarifying some ways in which foraging influences reproduction and vice versa. Any animal has only a certain finite period of time available in which to perform all its activities, including foraging and reproduction. This total time budget, which can be considered either on a daily basis or over the animal's lifetime, will be determined both by the diurnal rhythm of activity and by the animal's ability to " make time" by performing more than one activity at the same time (such as a male lizard sitting on a perch, simultaneously watching for potential prey and predators while monitoring mates and competing males). Provided that a time period is profitable for foraging (expected gains in matter and energy exceed inevitable losses from energetic costs of foraging), any increase in time devoted to foraging clearly will increase an animal's supply of matter and energy. However, necessarily accompanying this increase in matter and energy is a concomitant decrease in time available for nonforaging activities such as mating and reproduction. Thus, profits of time spent foraging are measured in matter and energy while costs take on units of time lost. Conversely, increased time spent on nonforaging activities confers profits in time while costs take the form of decreased energy availability. Hence, gains in energy correspond to losses in time, while dividends in time require reductions in energy availability. (Of course, risks of foraging and reproduction also need to be considered.)

The preceding arguments suggest that optimal allocation of time and energy ultimately depends on how costs in each currency vary with profits in the opposite. However, because units of costs and profits in time and energy differ, one would like to be able to convert them into a common currency. Costs and profits in time might be measured empirically in energetic units by estimating the net gain in energy per unit of foraging time. If all potential foraging time is equivalent, profits would vary linearly with costs under such circumstances, the loss in energy associated with nonforaging activities would be directly proportional to the amount of time devoted to such activity. Optimal budgeting of time and energy into foraging versus nonforaging activities is usually profoundly influenced by various circadian and seasonal rhythms of physical conditions, as well as those of predators and potential prey. Clearly, certain time periods favorable for foraging return greater gains in energy gathered per unit time than other periods. Risks of exposure to both harsh physical conditions and predators must often figure into the optimal amount of time to devote to various activities. Ideally, one would ultimately like to measure both an animal's foraging efficiency and its success at budgeting time and energy by its lifetime reproductive success, which would reflect all such environmental "risks."

Foraging and reproductive activities interact in another important way. Many organisms gather and store materials and energy during time periods that are unfavorable for successful reproduction but then expend these same resources on reproduction at a later, more suitable, time. Lipid storage and utilization systems obviously facilitate such temporal integration of uptake and expenditure of matter and energy. This temporal component greatly complicates the empirical measurement of reproductive effort.

Prey density can strongly affect an animal's time and energy budget. Gibb (1956) watched rock pipits, Anthus spinoletta, feeding in the intertidal along the English seacoast during two consecutive winters. The first winter was relatively mild the birds spent an average of 6-1/2 hours feeding, 1-3/4 hours resting, and 3/4 hour fighting in defense of their territory (total daylight slightly exceeded 9 hours). The next winter was much harsher and food was considerably scarcer the birds spent 8-1/4 hours feeding, 39 minutes resting, and only 7 minutes on territorial defense! Apparently the combination of low food density and extreme cold (endotherms require more energy in colder weather) demanded that over 90 percent of the bird's waking hours be spent feeding and no time remained for frivolities. This example also illustrates that food is less defendable at lower densities, as indicated by reduced time spent on territorial defense. Obviously, food density in the second year was near the lower limit that would allow survival of rock pipits. When prey items are too sparse, encounters may be so infrequent that an individual cannot survive. Gibb (1960) calculated that to balance their energy budget during the winter in some places, English tits must find an insect on the average once every 2-1/2 seconds during daylight hours.

Time and energy budgets are influenced by a multitude of other ecological factors, including body size, mode of foraging, mode of locomotion, vagility, trophic level, prey size, resource density, environmental heterogeneity, rarefaction, competition, risks of predation, and reproductive tactics.

Leaves take on an almost bewildering array of sizes and shapes: some leaves are deciduous, others evergreen some are simple, others compound and their actual spatial arrangement on a given plant differs considerably both within and between species (Figure 5.3).

Some leaves are much more costly to produce and maintain than others (elementary economic considerations dictate that any given leaf must pay for itself plus generate a net energetic profit). Presumably, this great diversity of leaf tactics is a result of natural selection maximizing the lifetime reproductive success of individual plants under diverse environmental conditions. Leaf tactics are influenced by many factors that include light, water availability, prevailing winds, and herbivores. When grown in the shade, individuals of many species grow larger, less dissected leaves than when grown in the sun. Similarly, shade-tolerant plants of the understory usually have larger and less lobed leaves than canopy species. Similar types of leaves often evolve independently in different plant lineages subjected to comparable climatic conditions at different geographic localities, especially among trees (Bailey and Sinnot 1916 Ryder 1954 Stowe and Brown 1981). Compound leaves, thought to conserve woody tissue, with small leaflets are found in hot dry regions, whereas those with larger leaflets occur under warm moist conditions. Lowland wet tropical rain forest trees have large evergreen leaves with nonlobed or continuous margins, chaparral plants tend to have small sclerophyllous evergreen leaves, arid regions tend to support leafless stem succulents such as cacti or plants with entire leaf margins (especially among evergreens), plants from cold wet climates often have notched or lobed leaf margins, and so on. Such repeated patterns of leaf size and shape suggest that a general theory of leaf tactics is possible.

Several models for optimal leaf size under differing environmental conditions have been developed. Efficiency of water use (grams of carbon dioxide assimilated per gram of water lost) was the measure of plant performance maximized by Parkhurst and Loucks (1971). A similar model for size and shape of vine leaves was developed by Givnish and Vermeij (1976). Even these relatively simple models predict several observed patterns in leaf size, such as large leaves in warm, shady, wet places and small leaves in colder areas or warmer and sunnier locales (Figure 5.4).

The evergreen versus deciduous dichotomy can be approached similarly using cost-benefit arguments (Orians and Solbrig 1977 Miller 1979). In considering leaf tactics of desert plants, Orians and Solbrig contrast leaf types along a continuum ranging from the relatively inexpensive deciduous " mesophytic" leaf to the more costly evergreen " xerophytic" leaf. Mesophytic leaves photosynthesize and transpire at a rapid rate and hence require high water availability (low " soil water potential"). In deserts, such plants grow primarily along washes. In contrast, xerophytic leaves cannot photosynthesize as rapidly when abundant water is available, but they can extract water from relatively dry soil. Each plant leaf tactic has an advantage either at different times or in different places, thereby promoting plant life form diversity. During wet periods, plants with mesophytic leaves photosynthesize rapidly, but under drought conditions, they must drop their leaves and become dormant. During such dry periods, however, the slower photosynthesizers with xerophytic leaves are still able to function by virtue of their ability to extract water from dry soils. Of course, all degrees of intermediate leaf tactics exist, each of which may enjoy a competitive advantage under particular conditions of water availability (Figure 5.5). In a predictable environment, net annual profit per unit of leaf surface area determines the winning phenotype. Even a relatively brief wet season could suffice to give mesophytic leaves a higher annual profit (which accounts for the occurrence of these plant life forms in deserts).

In an interesting discussion of leaf arrangement and forest structure, Horn (1971, 1975a, 1976) distinguished " monolayers" from " multilayers." Each plant in the multilayer of a forest (usually sunnier places such as the canopy) has leaves scattered throughout its volume at several different levels, whereas monolayer plants have essentially a single blanket or shell of leaves. Plants in the multilayer gain from a geometry that allows some light to pass through to their own leaves at lower levels. Horn points out that lobing facilitates passage of light and that such plants do well in the sun (in the shade, inner leaves may respire more than they photosynthesize). In contrast, the optimal tree design in the shade is a monolayer in which each leaf typically intercepts as much light as possible (leaves are large and seldom lobed). Moreover, slow-growing monolayered plants eventually outcompete fast-growing multilayered plants that persist by regular colonization of newly vacated areas created by continual disturbance (Horn 1976).

Foraging tactics involve the ways in which animals gather matter and energy. As explained above, matter and energy constitute the profits gained from foraging, in that they are used in growth, maintenance, and reproduction. But foraging has its costs as well a foraging animal may often expose itself to potential predators, and much of the time spent in foraging is rendered unavailable for other activities, including reproduction. An optimal foraging tactic maximizes the difference between foraging profits and their costs. Presumably, natural selection, acting as an efficiency expert, has often favored such optimal foraging behavior. Consider, for example, prey of different sizes and what might be termed "catchability." How great an effort should a foraging animal make to obtain a prey item with a given catchability and of a particular size (and therefore matter and energy content)? Clearly, an optimal consumer should be willing to expend more energy to find and capture food items that return the most energy per unit of expenditure upon them. Moreover, an optimal forager should take advantage of natural feeding routes and should not waste time and energy looking for prey either in inappropriate places or at inappropriate times. What is optimal in one environment is seldom optimal in another, and an animal's particular anatomy strongly constrains its optimal foraging tactic. Evidence is considerable that animals actually do attempt to maximize their foraging efficiencies, and a substantial body of theory on optimal foraging tactics exists.

Numerous aspects of optimal foraging theory are concisely summarized in an excellent chapter, "The Economics of Consumer Choice," by MacArthur (1972). He makes several preliminary assumptions: (a) Environmental structure is repeatable, with some statistical expectation of finding a particular resource (such as a habitat, microhabitat, and/or prey item). (b) Food items can be arranged in a continuous and unimodal spectrum, such as size distributions of insects (Schoener and Janzen 1968 Hespenhide 1971). (This assumption is clearly violated by foods of some animals, such as monophagous insects or herbivores generally, because plant chemical defenses are typically discrete see Chapter 15) (c) Similar animal phenotypes are usually closely equivalent in their harvesting abilities an intermediate phenotype is thus best able to exploit foods intermediate between those that are optimal for two neighboring phenotypes (see Chapter 13). Conversely, similar foods are gathered with similar efficiencies a lizard with a jaw length that adapts it to exploit 5-mm-long insects best is only slightly less efficient at eating 4- and 6-mm insects. (d) The principle of allocation applies, and no one phenotype can be maximally efficient on all prey types improving harvesting efficiency on one food type necessitates reducing the efficiency of exploiting other kinds of items. (e) Finally, an individual's economic "goal" is to maximize its total intake of food resources. (Assumptions b, c, and d are not vital to the argument.)

MacArthur (1972) then breaks foraging down into four phases: (1) deciding where to search (2) searching for palatable food items (3) upon locating a potential food item, deciding whether or not to pursue it and (4) pursuit itself, with possible capture and eating. Search and pursuit efficiencies for each food type in each habitat are entirely determined by the preceding assumptions about morphology (assumption c) and environmental repeatability (assumption a) moreover, these efficiencies dictate the probabilities associated with the searching and pursuing phases of foraging (2 and 4, respectively). Thus, MacArthur considers only the two decisions: where to forage and what prey items to pursue (phases 1 and 3 of foraging).

Clearly, an optimal consumer should forage where its expectation of yield is greatest -- an easy decision to make, given knowledge of the previous efficiencies and the structure of its environment (in reality, of course, animals are far from omniscient and must make decisions based on incomplete information). The decision as to which prey items to pursue is also simple. Upon finding a potential prey item, a consumer has only two options: either pursue it or go on searching for a better item and pursue that one instead. Both decisions end in the forager beginning a new search, so the best choice is clearly the one that returns the greatest yield per unit time. Thus, an optimal consumer should opt to pursue an item only when it cannot expect to locate, catch, and eat a better item (i.e., one that returns more energy per unit of time) during the time required to capture and ingest the first prey item.

Many animals, such as foliage-gleaning insectivorous birds, spend much of their foraging time searching for prey but expend relatively little time and energy pursuing, capturing, and eating small sedentary insects that are usually easy to catch and quickly swallowed. In such "searchers," mean search time per item eaten is large compared to average pursuit time per item hence, the optimal strategy is to eat essentially all palatable insects encountered. Other animals ("pursuers") that expend little energy in finding their prey but a great deal of effort in capturing it (such as, perhaps, a falcon or a lion) should select prey with small average pursuit times (and energetic costs). Hence, pursuers should generally be more selective and more specialized than searchers. Moreover, because a food-dense environment offers a lower average search time per item than does a food-sparse area, an optimal consumer should restrict its diet to only the better types of food items in the former habitat. To date, optimal foraging theory has been developed primarily in terms of the rate at which energy is gathered per unit of time. Limiting materials such as nutrients in short supply and the risks of predation have so far been largely neglected.

Carnivorous animals forage in extremely different ways. In the " sit-and-wait" mode, a predator waits in one place until a moving prey item comes by and then "ambushes" the prey in the " widely foraging" mode, the predator actively searches out its prey (Pianka 1966b Schoener 1969a, 1969b). The second strategy normally requires a greater energy expenditure than the first. The success of the sit-and-wait tactic usually depends on one or more of three conditions: a fairly high prey density, high prey mobility, and low predator energy requirements. The widely foraging tactic also depends on prey density and mobility and on the predator's energy needs, but here the distribution of prey in space and the predator's searching abilities assume paramount importance. Although these two tactics are endpoints of a continuum of possible foraging strategies (and hence somewhat artificial), foraging techniques actually employed by many organisms are rather strongly polarized. The dichotomy of sit-and-wait versus widely foraging therefore has substantial practical value. Among snakes, for example, racers and cobras forage widely when compared with boas, pythons, and vipers, which are relatively sit-and-wait foragers. Among hawks, accipiters such as Cooper's hawks and goshawks often hunt by ambush using a sit-and-wait strategy, whereas most buteos and many falcons are relatively more widely foraging. Web-building spiders and sessile filter feeders such as barnacles typically forage by sitting and waiting. Many spiders expend considerable amounts of energy and time building their webs rather than moving about in search of prey those that do not build webs forage much more widely. Some general correlates of these two modes of foraging are listed in Table 5.1.

Table 5.1 Some General Correlates of Foraging Mode

Sit-and-Wait Widely Foraging

Prey type Eat active prey Eat sedentary and unpre- dictable (but clumped or
large) prey

Volume prey captured/dayLow Generally high, but low
in certain species

Daily metabolic expense Low High

Types of predators Vulnerable primarily Vulnerable to both sit-
to widely foraging and-wait and to widely
predators foraging predators

Rate of encountersProbably lowProbably high
with predators

MorphologyStocky (short tails)Streamlined (generally
long tails)

Probable physiologicalLimited enduranceHigh endurance capacity

Relative clutch mass High Low

Sensory modeVisual primarily Visual or olfactory

Learning abilityLimitedEnhanced learning and
memory, larger brains

Source: Adapted from Huey and Pianka (1981).

Similar considerations can be applied in comparing herbivores with carnivores. Because the density of plant food almost always greatly exceeds the density of animal food, herbivores often expend little energy, relative to carnivores, in finding their prey (to the extent that secondary chemical compounds of plants, such as tannins, and other antiherbivore defenses reduce palatability of plants or parts of plants, the effective supply of plant foods may be greatly reduced). Because cellulose in plants is difficult to digest, however, herbivores must expend considerable energy in extracting nutrients from their plant food. (Most herbivores have a large ratio of gut volume to body volume, harbor intestinal microorganisms that digest cellulose, and spend much of their time eating or ruminating -- envision a cow chewing its cud.) Animal food, composed of readily available proteins, lipids, and carbohydrates, is more readily digested carnivores can afford to expend considerable effort in searching for their prey because of the large dividends obtained once they find it. As would be expected, the efficiency of conversion of food into an animal's own tissues ( assimilation) is considerably lower in herbivores than it is in carnivores.

Many carnivores have extremely efficient prey-capturing devices (see Chapter 15) often the size of a prey object markedly influences this efficiency. Using simple geometry (Figure 5.6), Holling (1964) estimated the diameter of a prey item that should be optimal for a praying mantid of a particular size. He then offered hungry mantids prey objects of various sizes and recorded percentages attacked (Figure 5.7). Mantids were noticeably reluctant to attack prey that were either much larger or much smaller than the estimated optimum. Hence, natural selection has resulted in efficient predators both by producing efficient prey-capturing devices and by programming animals so that they are unlikely to attempt to capture decidedly suboptimal items. Larger predators tend to take larger prey than smaller ones (see Figure 12.12). It may in fact be better strategy for a large predator to overlook prey below some minimal size threshold and to spend the time that would have been spent in capturing and eating such small items in searching out larger prey (see also above). Similarly, the effort a predator will expend on any given prey item is proportional to the expected return from that item (which usually increases with prey size). Thus, a lizard waiting on a perch will not usually go far for a very small prey item but will often move much greater distances in attempts to obtain larger prey.

Because small prey are generally much more abundant than large prey, most animals encounter and eat many more small prey items than large ones. Small animals that eat small prey items encounter prey of suitable size much more frequently than do larger animals that rely on larger prey items as a result, larger animals tend to eat a wider range of prey sizes. Because of such increased food niche breadths of larger animals, size differences between predators increase markedly with increasing predator size (MacArthur 1972).

The concern of environmental physiology, or ecophysiology, is how organisms function within, adapt and respond to, and exploit their physical environments. Physiological ecologists are interested primarily in the immediate functional and behavioral mechanisms by which organisms cope with their abiotic environments. Physiological mechanisms clearly must reflect ecological conditions moreover, mutual constraints between physiology and ecology dictate that both must evolve together in a synergistic fashion.

A fundamental principle of physiology is the notion of homeostasis, the maintenance of a relatively stable internal state under a much wider range of external environmental conditions. Homeostasis is achieved not only by physiological means but also by appropriate behavioral responses. An example is temperature regulation in which an organism maintains a fairly constant body temperature over a considerably greater range of ambient thermal conditions (homeostasis is never perfect). Homeostatic mechanisms have also evolved that buffer environmental variation in humidity, light intensity, and concentrations of various substances such as hydrogen ions (pH), salts, and so on. By effectively moderating spatial and temporal variation in the physical environment, homeostasis allows organisms to persist and be active within a broad range of environmental conditions, thereby enhancing their fitness. The subject of environmental physiology is vast some references are given at the end of this chapter.

Physiological Optima and Tolerance Curves

Physiological processes proceed at different rates under different conditions. Most, such as rate of movement and photosynthesis, are temperature dependent (Figure 5.8). Other processes vary with availability of various materials such as water, carbon dioxide, nitrogen, and hydrogen ions (pH). Curves of performance, known as tolerance curves (Shelford 1913b), are typically bell shaped and unimodal, with their peaks representing optimal conditions for a particular physiological process and their tails reflecting the limits of tolerance. Some individuals and species have very narrow peaked tolerance curves in others these curves are considerably broader. Broad tolerance curves are described with the prefix eury- (e.g., eurythermic, euryhaline), whereas steno- is used for narrow ones (e.g., stenophagous). An organism's use of environmental resources such as foods and microhabitats can profitably be viewed similarly, and performance can be measured in a wide variety of units such as survivorship, reproductive success, foraging efficiency, and fitness.

Performance curves can sometimes be altered during the lifetime of an individual as it becomes exposed to different ambient external conditions. Such short-term alteration of physiological optima is known as acclimation (Figure 5.8). Within certain design constraints, tolerance curves clearly must change over evolutionary time as natural selection molds them to reflect changing environmental conditions. However, very little is known about the evolution of tolerance most researchers have merely described the range(s) of conditions tolerated or exploited by particular organisms. Tolerance curves are often taken almost as given and immutable, with little or no consideration of the ecological and evolutionary forces that shape them.

Performance or tolerance is often sensitive to two or more environmental variables. For example, the fitness of a hypothetical organism in various microhabitats might be a function of relative humidity (or vapor pressure deficit), somewhat as shown in Figure 5.9a. Assume that fitness varies similarly along a temperature gradient (Figure 5.9b). Figure 5.9c combines humidity and temperature conditions to show variation in fitness with respect to both variables simultaneously (a third axis, fitness, is implicit in this figure). The range of thermal conditions tolerated is narrower at very low and very high humidities than it is at intermediate and more optimal humidities. Similarly, an organism's tolerance range for relative humidity is narrower at extreme temperatures than it is at more optimal ones. The organism's thermal optimum depends on humidity conditions (and vice versa). Fitness reaches its maximum at intermediate temperatures and humidities. Hence, temperature tolerance and tolerance of relative humidities interact in this example. The concept of a single fixed optimum is in some ways an artifact of considering only one environmental dimension at a time.

Some of the food ingested by any animal passes through its gut unused. Such egested material can be as high as 80 to 90 percent of the total intake in some caterpillars (Whittaker 1975). Food actually digested is termed assimilation: A fraction of this must be used in respiration to support maintenance metabolism and activity. The remainder is incorporated into the animal concerned as secondary productivity and ultimately can be used either in growth or in reproduction. These relationships are summarized below:

Assimilation = Productivity + Respiration

Productivity = Growth + Reproduction

The total amount of energy needed per unit time for maintenance increases with increasing body mass (Figure 5.10). However, because small animals have relatively high ratios of body surface to body volume, they generally have much higher metabolic rates and hence have greater energy requirements per unit of body weight than larger animals (Figure 5.11). Animals that maintain relatively constant internal body temperatures are known as homeotherms those whose temperatures vary widely from time to time, usually approximating the temperature of their immediate environment, are called poikilotherms. These two terms are sometimes confused with a related pair of useful terms. An organism that obtains its heat from its external environment is an ectotherm one that produces most of its own heat internally by means of oxidative metabolism is known as an endotherm. All plants and the vast majority of animals are ectothermic the only continuously endothermic animals are found among birds and mammals (but even some of these become ectothermic at times). Some poikilotherms (large reptiles and certain large fast-swimming fish such as tuna) are at times at least partially endothermic. Certain ectotherms (many lizards and temperate-zone flying insects) actually regulate their body temperatures fairly precisely during periods of activity by appropriate behavioral means. Thus, ectotherms at times can be homeotherms! An active bumblebee or desert lizard may have a body temperature as high as that of a bird or mammal (the layman's terms "warm-blooded" and "cold-blooded" can thus be quite misleading and should be abandoned). Because energy is required to maintain a constant internal body temperature, endotherms have considerably higher metabolic rates, as well as higher energy needs (and budgets), than ectotherms of

the same body mass. There is a distinct lower limit on body size for endotherms -- about the size of a small hummingbird or shrew (2 or 3 grams). Indeed, both hummingbirds and shrews have very high metabolic rates and hence rather precarious energetic relationships they depend on continual supplies of energy-rich foods. Small hummingbirds would starve to death during cold nights if they did not allow their body temperatures to drop and go into a state of torpor.

Body size, diet, and movements are complexly intertwined with the energetics of metabolism. Energy requirements do not scale linearly with body mass, but instead as a fractional exponent: E = k m 0.67 where k is a taxon-specific constant and m is body mass. Large animals require more matter and energy for their maintenance than small ones, and in order to obtain it they usually must range over larger geographical areas than smaller animals with otherwise similar food requirements. Food habits also influence movements and home range size. Because the foods of herbivorous animals that eat the green parts of plants (such as grazers, which eat grasses and ground-level vegetation, and browsers, which eat tree leaves) are usually quite dense, these animals usually do not have very large home ranges. In contrast, carnivores and those herbivores that must search for their foods (such as granivores and frugivores, which eat seeds and fruits, respectively) frequently spend much of their foraging time and energy in search, ranging over considerably larger areas. McNab (1963) termed the first group " croppers" and the latter " hunters." Croppers generally exploit foods that occur in relatively dense supply, whereas hunters typically utilize less dense foods. Hunters are often territorial, but croppers seldom defend territories. Croppers and hunters are not discrete but in fact grade into each other (Figure 5.12). A browser that eats only the leaves of a rare tree might be more of a hunter than a granivore that eats the seeds of a very common plant. However, such intermediates are uncommon enough that separation into two categories is useful for many purposes. Figure 5.13 shows the correlation between home range size and body weight for a variety of mammalian species, here separated into croppers and hunters. Analogous correlations, but with different slopes and/or intercepts, have been obtained for birds and lizards (Schoener 1968b Turner et al. 1969). Very mobile animals, like birds, frequently range over larger areas than less mobile animals such as terrestrial mammals and lizards. In areas of low productivity (for example, deserts), most animals may be forced to range over a greater area to find adequate food than they would in more productive regions. Large home ranges or territories usually result in low densities, which in turn markedly limit possibilities for the evolution of sociality. Thus, McNab (1963) points out that complex social behavior has usually evolved only in croppers and/or among exceptionally mobile hunters.

The metabolic cost of movement varies with both an animal's body size and its mode of locomotion. The cost of moving a unit of body mass some standard distance is actually less in larger animals than in smaller ones (Figure 5.14). Terrestrial locomotion is the most expensive mode of transportation, flight is intermediate in cost, and swimming is the most economical means of moving about -- provided body shape is fusiform and buoyancy is neutral (Figure 5.14).

Physiologists have documented numerous consistent size-related trends in organs and metabolic properties. For example, among mammals, heart mass is always about 0.6 percent of total body mass, whereas blood volume is almost universally about 5.5 percent of body mass over a great range of body sizes (these organ systems are thus directly proportional to size). Other physiological attributes, such as lung surface in mammals, vary directly with metabolic rate rather than with size. However, some organ systems, such as the kidney and liver, do not scale directly with either size or metabolic rate (Schmidt-Nielsen 1975). Such " physiological rules" apparently dictate available avenues for physiological change, thereby constraining possible ecological adaptations.

Organisms are adapted to their environments in that, to survive and reproduce, they must meet their environment's conditions for existence. Evolutionary adaptation can be defined as conformity between an organism and its environment. Plants and animals have adapted to their environments both genetically and by means of physiological, behavioral, and/or developmental flexibility. The former includes instinctive behavior and the latter learning. Adaptation has many dimensions in that most organisms must conform simultaneously to numerous different aspects of their environments. Thus, for an organism to adapt, it must cope not only with various aspects of its physical environment, such as temperature and humidity conditions, but also with competitors, predators, and escape tactics of its prey. Conflicting demands of these various environmental components often require that an organism compromise in its adaptations to each. Conformity to any given component takes a certain amount of energy that is then no longer available for other adaptations. The presence of predators, for example, may require that an animal be wary, which in turn is likely to reduce its foraging efficiency and hence its competitive ability.

Organisms can conform to and cope with highly predictable environments relatively easily, even when they change in a regular way, as long as they are not too extreme. Adaptation to an unpredictable environment is usually more difficult adapting to extremely erratic environments may even prove impossible. Many organisms have evolved dormant stages that allow them to survive unfavorable periods, both predictable and unpredictable. Annual plants everywhere and brine shrimp in deserts are good examples. Brine shrimp eggs survive for years in the salty crust of dry desert lakes when a rare desert rain fills one of these lakes, the eggs hatch, the shrimp grow rapidly to adults, and they produce many eggs. Some seeds known to be many centuries old are still viable and have been germinated. Changes in the environment that reduce overall adaptation are collectively termed the " deterioration of environment" such changes cause directional selection resulting in accommodation to the new environment.

A simple but elegant model of adaptation and undirected environmental deterioration was developed by Fisher (1930). He reasoned that no organism is "perfectly adapted" -- all must fail to conform to their environments in some ways and to differing degrees. However, a hypothetical, perfectly adapted organism can always be imagined (actually this reflects the environment) against which existing organisms may be compared. Fisher's mathematical argument is phrased in terms of an infinite number of "dimensions" for adaptation (only three are used here for ease of illustration).

Imagine an adaptational space of three coordinates representing, respectively, the competitive, predatory, and physical environments (Figure 5.15). An ideal "perfectly adapted" organism lies at a particular point (say A) in this space, but any given real organism is at another point (say B), some distance, d, away from the point of perfect adaptation. Changes in the position of A correspond to environmental changes making the optimally adapted organism different changes in B represent changes in the organisms concerned, such as mutations. The distance between the two points, d, represents the degree of conformity between the organism and environment, or the level of adaptation. Fisher noted that very small undirected changes in either organism or environment have a 50:50 chance of being to the organism's advantage (i.e., reducing the distance between A and B). The probability of such improvement is inversely related to the magnitude of the change (Figure 5.16).

Very great changes in either organism or environment are always maladaptive because even if they are in the correct direction, they "overshoot" points of closer adaptation. (Of course, it is remotely possible that such major environmental changes or "macromutations" could put an organism into a completely new adaptive realm and thereby improve its overall level of adaptation.) Fisher makes an analogy with focusing a microscope. Very fine changes are as likely as not to improve the focus, but gross changes will almost invariably throw the machine further out of focus. Organisms may be thought of as " tracking" their environments in both ecological and evolutionary time, changing as their environments change thus, as point A shifts because of daily, seasonal, and long-term environmental fluctuations, point B follows it. Such environmental tracking may be physiological (as in acclimation), behavioral (including learning), and/or genetic (evolutionary), depending on the time scale of environmental change. Reciprocal counterevolutionary responses to other species (prey, competitors, parasites, and predators) constitute examples of such evolutionary tracking, 1 and have been termed coevolution (see Chapter 15). Individual organisms with narrow tolerance limits, such as highly adapted specialists, generally suffer greater losses in fitness due to a unit of environmental deterioration than generalized organisms with more versatile requirements, all else being equal. Thus, more specialized organisms and/or those with restricted homeostatic abilities cannot tolerate as much environmental change as generalists or organisms with better developed homeostasis (Figure 5.16). Fisher's (1930) model applies only to nondirected changes in either party of the adaptational complex -- such as mutations and perhaps certain climatic fluctuations, or other random events. However, many environmental changes are probably nonrandom. Changes in other associated organisms, especially predators and prey, are invariably directed so as to reduce an organism's degree of conformity to its environment thus, they constitute a deterioration of that organism's environment. Directed changes in competitors can either increase or decrease an organism's level of adaptation, depending on whether they involve avoidance of competition or improvements in competitive ability per se. Directed changes in mutualistic systems would usually tend to improve the overall level of adaptation of both parties.

When averaged over a long enough period of time, heat gained by an organism must be exactly balanced by heat lost to its environment otherwise the plant or animal would either warm up or cool off. Many different pathways of heat gains and heat losses exist (Figure 5.17). The notion of a heat budget is closely related to the concept of an energy budget balancing a heat budget requires very different adaptations under varying environmental conditions. At different times of day, ambient thermal conditions may change from being too cold to being too warm for a particular organism's optimal performance. Organisms living in hot deserts must avoid overheating by being able to minimize heat loads and to dissipate heat efficiently in contrast, those that live in colder places such as at high altitudes or in polar regions must avoid overcooling -- hence they have evolved efficient means of heat retention, such as insulation by blubber, feathers, or fur, that reduce the rate of heat exchange with the external environment.

As seen in previous chapters, environmental temperatures fluctuate in characteristic ways at different places over the earth's surface, both daily and seasonally. In the absence of a long-term warming or cooling trend, environmental temperatures at any given spot remain roughly constant when averaged over an entire annual cycle. Recall that the range in temperature within a year is much greater at high latitudes than it is nearer the equator. An organism could balance its annual heat budget by being entirely passive and simply allowing its temperature to mirror that of its environment. Such a passive thermoregulator is known as a thermoconformer (Figures 5.18 and 5.19). Of course, it is also an ectotherm. Another extreme would be to maintain an absolutely constant body temperature by physiological and/or behavioral means, dissipating (or avoiding) excess bodily heat during warm periods but retaining (or gaining) heat during cooler periods (in endotherms, energy intake is often increased during cold periods and more metabolic heat is produced to offset the increased heat losses).

Organisms that carefully regulate their internal temperatures are called thermoregulators, or homeotherms. (Recall that both endotherms and ectotherms may regulate their body temperatures.) There is, of course, a continuum between the two extremes of perfect conformity and perfect regulation (see Figure 5.22). Homeostasis, remember, is never perfect. Because regulation clearly has costs and risks as well as profits, an emerging conceptual framework envisions an optimal level of regulation that depends on the precise form of the constraints and interactions among the costs and benefits arising from a particular ecological situation (Huey and Slatkin 1976). Thermoregulation often involves both physiological and behavioral adjustments as an example of the latter, consider a typical terrestrial diurnal desert lizard. During the early morning, when ambient temperatures are low, such a lizard locates itself in warmer microclimates of the environmental thermal mosaic (e.g., small depressions in the open or on tree trunks), basking in the sun with its body as perpendicular as possible to the sun's rays and thereby maximizing heat gained. With the daily march of temperature, ambient thermal conditions quickly rise and the lizard seeks cooler shady microhabitats. Individuals of some species retreat into burrows as temperatures rise others climb up off the ground into cooler air and orient themselves facing into the sun's rays, thereby reducing heat load. Many lizards change colors and their heat reflectance properties, being dark and heat absorbent at colder times of day but light and heat reflectant at hotter times. Such adjustments allow individual lizards to be active over a longer period of time than they could be if they conformed passively to ambient thermal conditions presumably, they are also more effective competitors and better able to elude predators as a result of such thermoregulatory behaviors.

Hot, arid regions typically support rich lizard faunas, whereas cooler forested areas have considerably fewer lizard species and individuals. Lizards can enjoy the benefits of a high metabolic rate during relatively brief periods when conditions are appropriate for activity and yet can still become inactive during adverse conditions. By facilitating metabolic inactivity on both a daily and a seasonal basis, poikilothermy thus allows lizards to capitalize on unpredictable food supplies. Ectotherms are low-energy animals one day's food supply for a small bird will last a lizard of the same body mass for a full month! Most endothermic diurnal birds and mammals must wait out the hot midday period at considerable metabolic cost, whereas lizards can effectively reduce temporal heterogeneity by retreating underground, becoming inactive, and lowering their metabolic rate during harsh periods (some desert rodents estivate when food and/or water is in short supply). Poikilothermy may well contribute to the apparent relative success of lizards over birds and mammals in arid regions. Forests and grasslands are probably simply too shady and too cold for ectothermic lizards to be very successful because these animals depend on basking to reach body temperatures high enough for activity in contrast, birds and mammals do quite well in such areas partly because of their endothermy.

Because water conservation is a major problem for desert organisms, their physiological and behavioral adaptations for acquisition of water and for economy of its use have been well studied. These interesting adaptations are quite varied. Like energy and heat budgets, water budgets must balance losses must be replaced by gains. For examples of water acquisition mechanisms, consider rooting strategies. Desert plants may usually invest considerably more in root systems than plants from wetter areas one study showed that perennial shrubs in the Great Basin desert allocate nearly 90 percent of their biomass to underground tissues (Caldwell and Fernandez 1975), whereas roots apparently represent a much smaller fraction (only about 10 percent) of the standing crop biomass of a mesic hardwood forest.

The creosote bush Larrea divaricata has both a surface root system and an extremely deep tap root that often reaches all the way down to the water table. This long tap root provides Larrea with water even during long dry spells when surface soils contain little moisture. Cacti, in contrast, have an extensive but relatively shallow root system and rely on water storage to survive drought. Many such desert plants have tough sclerophyllous xerophytic leaves that do not allow much water to escape (they also photosynthesize at a low rate as a consequence). Mesophytic plants occur in deserts too, but they photosynthesize rapidly and grow only during periods when moisture is relatively available they drop their leaves and become inactive during droughts. Plants also reduce water losses during the heat of midday by closing their stomata and drooping their leaves ( wilting). Many desert plants and animals absorb and use atmospheric and/or substrate moisture most can also tolerate extreme desiccation.

Camels do not rely on water storage to survive water deprivation, as is commonly thought, but can lose as much as a quarter of their body mass, primarily as water loss (Schmidt-Nielsen 1964). Like many desert organisms, camels also conserve water by allowing their temperature to rise during midday. Moreover, camels tolerate greater changes in plasma electrolyte concentrations than less drought-adapted animals. In deserts, small mammals like kangaroo rats survive without drinking by relying on metabolic water derived from the oxidation of their food (here, then, is an interface between energy budgets and water budgets). Most desert rodents are nocturnal and avoid using valuable water for heat regulation by spending hot daytime hours underground in cool burrows with high relative humidity, thereby minimizing losses to evaporation (most desert organisms resort to evaporative cooling mechanisms such as panting only in emergencies). The urine of kangaroo rats is extremely concentrated and their feces contain little water (Schmidt-Nielsen 1964). Most other desert animals minimize water losses in excretion, too. Birds and lizards produce solid uric acid wastes rather than urea, thereby requiring little water for excretion. Desert lizards also conserve water by retreating to burrows and lowering their metabolic rate during the heat of the day.

Numerous other materials, including calcium, chloride, magnesium, nitrogen, potassium, and sodium, may be in short supply for particular organisms and must therefore be budgeted. Neural mechanisms of animals depend on sodium, potassium, and chloride ions, which are sometimes available in limited quantities. Because many herbivorous mammals obtain little sodium from their plant foods (plants lack nerves and sodium is not essential to their physiology), these animals must conserve sodium and/or find supplemental sources at salt licks -- indeed, Feeny (1975) suggests that plants may actually withhold sodium as an antiherbivore tactic. Similarly, amino acids are in short supply for many insects, such as in Heliconius butterflies, which supplement their diets with protein-rich pollen (Gilbert 1972).

An organism's nutrient and vitamin requirements are strongly influenced by the evolution of its metabolic pathways likewise, these same pathways may themselves determine certain of the organism's nutritional needs. To illustrate: Almost all species of vertebrates synthesize their own ascorbic acid, but humans and several other primate species that have been tested cannot they require a dietary supplement of ascorbic acid, known as vitamin C. Of thousands of other species of mammals, only two -- the guinea pig and an Indian fruit-eating bat -- are known to have lost the ability to synthesize their own ascorbic acid. A few species of birds must supplement their diets with ascorbic acid, too. Thus, a frog, a lizard, a sparrow, or a rat can make its own ascorbic acid, but we cannot. Why should natural selection favor the loss of the ability to produce a vital material? Pauling (1970) suggests that species of animals that have lost this capacity evolved in environments with ample supplies of ascorbic acid in available foods. It might actually be advantageous to dismantle a biochemical pathway in favor of another once it becomes redundant. Conversely, natural selection should favor evolution of the ability to synthesize any necessary materials that cannot be predictably obtained from available foods where this is possible (clearly organisms cannot synthesize elements -- herbivores cannot make sodium).

Animals vary tremendously in their perceptive abilities. Most (except some cave dwellers and deep-sea forms) use light to perceive their environments. But visual spectra and acuity vary greatly. Some, such as insects, fish, lizards, and birds, have color vision, whereas others (most mammals, except squirrels and primates) do not. Ants, bees, and some birds can detect polarized light and exploit this ability to navigate by the sun's position pigeons have poorly understood backup systems that enable them to return home remarkably well even when their vision is severely impaired with opaque contact lenses. Many temperate zone species of plants and animals rely on changes in day length to anticipate seasonal changes in climatic conditions. This, in turn, requires an accurate " biological clock." (Some organisms may also use barometric pressure to anticipate climatic changes.)

Certain snakes, such as pit vipers and boas, have evolved infrared receptors that allow them to locate and capture endothermic prey in total darkness. Most animals can hear, of course, although response to different frequencies varies considerably (some actually perceive ultrasonic sounds). Bats and porpoises emit and exploit sonar signals to navigate by echolocation. Similarly, nocturnal electric fish perceive their immediate environments by means of self-generated electrical fields. Certain bioluminescent organisms, such as " fireflies" (actually beetles), produce their own light for a variety of purposes, including attraction of mates and prey as well as (possibly) predator evasion (in some cases a mutualistic relationship is formed with a bioluminescent bacteria). Certain deep-sea fish probably use their "headlights" to find prey in the dark depths of the ocean. Pigeons can detect magnetic fields. Although a few animals have only a relatively feeble sense of smell (birds and humans, for example), most have keen chemoreceptors and/or olfactory abilities. Certain male moths can detect exceedingly dilute pheromones released by a female a full kilometer upwind, allowing these males to find females at considerable distances. Similarly, dung beetles use a zigzag flight to "home in" on upwind fecal material with remarkable precision.

Various environmental cues clearly provide particular animals with qualitatively and quantitatively different kinds and amounts of information. Certain environmental cues are useful in the context of capturing prey and escaping predators others may facilitate timing of reproduction to coincide with good conditions for raising young. Some environmental signals are noisier and less reliable than others. Moreover, the ability to process information received from the environment is limited by a finite neural capacity. The principle of allocation and the notion of trade-offs dictate that an individual cannot perceive all environmental cues with high efficiency. If ability to perceive a broad range of environmental stimuli actually requires lowered levels of performance along each perceptual dimension, natural selection should improve perceptual abilities along certain critical dimensions at the expense of other less useful ones. Clearly, echolocation has tremendous utility for a nocturnal bat, whereas vision is relatively much less useful. In contrast, the values of these two senses are reversed for a diurnal arboreal squirrel. Within phylogenetic constraints imposed by its evolutionary history, an animal's sensory capacities can be viewed as a bioassay of the importance of particular perceptual dimensions and environmental cues in that animal's ecology.

A basic point of this chapter is that any given organism possesses a unique coadapted complex of physiological, behavioral, and ecological traits whose functions complement one another and enhance that organism's reproductive success. Such a constellation of adaptations has been called an optimal design (Rosen 1967) or an adaptive suite (Bartholomew 1972).

Consider the desert horned lizard Phrynosoma platyrhinos (Figure 5.20). Various features of its anatomy, behavior, diet, temporal pattern of activity, thermoregulation, and reproductive tactics can be profitably interrelated and interpreted to provide an integrated view of the ecology of this interesting animal (Pianka and Parker 1975a). Horned lizards are ant specialists and usually eat essentially nothing else. Ants are small and contain much undigestible chitin, so that large numbers of them must be consumed. Hence, an ant specialist must possess a large stomach for its body size. When expressed as a proportion of total body mass, the stomach of this horned lizard occupies a considerably larger fraction of the animal's overall body mass (about 13 percent) than do the stomachs of all other sympatric desert lizard species, including the herbivorous desert iguana Dipsosaurus dorsalis (herbivores typically have lower assimilation rates and larger stomachs than carnivores). Possession of such a large gut necessitates a tanklike body form, reducing speed selection has favored a spiny body form and cryptic behavior rather than a sleek body and rapid movement to cover (as in most other species of lizards), decreasing the lizard's ability to escape from predators by flight. As a result, natural selection has favored a spiny body form and cryptic behavior rather than a sleek body and rapid movement to cover (as in most other species of lizards).

Risks of predation are likely to be increased during long periods of exposure while foraging in the open. A reluctance to move, even when actually threatened by a potential predator, could well be

advantageous movement might attract attention of predatorsand negate the advantage of concealing coloration and contour. Such decreased movement doubtless contributes to the observed high variance in body temperature of Phrynosoma platyrhinos, which is significantly greater than that of all other species of sympatric lizards.

Phrynosoma platyrhinos are also active over a longer time interval than any sympatric lizard species. Wide fluctuations in horned lizard body temperatures under natural conditions presumably reflect both the long activity period and perhaps their reduced movements into or out of the sun and shade (most of these lizards are in the open sun when first sighted). More time is thus made available for activities such as feeding. A foraging anteater must spend considerable time feeding. Food specialization on ants is economically feasible only because these insects usually occur in a clumped spatial distribution and hence constitute a concentrated food supply. To make use of this patchy and spatially concentrated, but at the same time not overly nutritious, food supply, P. platyrhinos has evolved a unique constellation of adaptations that include a large stomach, spiny body form, an expanded period of activity, and "relaxed" thermoregulation ( eurythermy). The high reproductive investment of adult horned lizards is probably also a simple and direct consequence of their robust body form. Lizards that must be able to move rapidly to escape predators, such as racerunners (Aspidoscelis formerly Cnemidophorus), would hardly be expected to weight themselves down with eggs to the same extent as animals like horned lizards that rely almost entirely upon spines and camouflage to avoid their enemies.

Energetics of metabolism of weasels provide another, somewhat more physiological, example of a suite of adaptations (Brown and Lasiewski 1972). Due to their long, thin body shape, weasels have a higher surface-to-volume ratio than mammals with a more standard shape, and as a consequence, they have an increased energy requirement. Presumably, benefits of the elongate body form more than outweigh associated costs otherwise natural selection would not have favored evolution of the weasel body shape. Brown and Lasiewski (1972) speculate that a major advantage of the elongate form is the ability to enter burrows of small mammals (weasel prey), which results in increased hunting success and thus allows weasels to balance their energy budgets (Figure 5.21). A further spin-off of the elongate shape is

the evolution of a pronounced sexual dimorphism in body size, which allows male and female weasels to exploit prey of different sizes and hence reduces competition between the sexes (related mustelids such as skunks and badgers do not have the marked sexual size dimorphism characteristic of weasels).

Most biologists are acutely aware that possible evolutionary pathways are somehow constrained by basic body plans. Although natural selection has "invented," developed, and refined a truly amazing variety of adaptations, 2 selection is clearly far from omnipotent. Wheels might be a desirable solution to certain environmental contingencies and yet they have not been evolved. Such " design constraints" are usually elusive and not easily demonstrable. Students of thermoregulation have often noted an apparent upper thermal limit of about 40°C for most of the earth's eukaryotic creatures (most plants, invertebrates, and vertebrates). This thermal "lid" has frequently been used as evidence for some extremely archaic and inflexible fundamental physiological process (perhaps an enzyme basic to life processes, such as a dehydrogenase, denatures). The major exceptions are certain heat-tolerant bacteria and blue-green algae, inhabitants of hot springs and oceanic volcanic vents. These prokaryotic organisms may well have arisen before the origin of the heat-sensitive metabolic pathway that seems to limit the eukaryotes.

An example of such a physiological design constraint involves the thermal relationships of vertebrates, spanning classes from reptiles to mammals (Pianka 1985, 1986a). Detailed consideration of behavioral thermoregulation in lizards enables a fairly accurate prediction of the active body temperatures of mammalian homeotherms. A provocative biological "constant" can thus be identified that suggests a substantial degree of physiological inertia.

An intriguing hypothesis for the evolution of homeothermy was offered by Hamilton (1973), who suggested that homeothermy is a by-product of advantages gained from maintaining maximum body temperatures in the face of such an innate physiological ceiling. Ecologically optimal temperatures need not coincide with physiological optima.

Remember that not all homeotherms are endotherms many ectotherms have attained a substantial degree of homeothermy by means of behavioral thermoregulation. Typically, such organisms actively select thermally suitable microhabitats, orient their bodies (or parts thereof) to control heat exchange, and/or shuttle between sun and shade as necessary to maintain a more-or-less constant internal body temperature.

Thermoregulation in lizards is not nearly as simple as it might appear to be at first glance, but rather encompasses a wide diversity of very different thermoregulatory tactics among species ranging from ectothermic poikilothermy to and including ectothermic homeothermy. Even a casual observer quickly notices that various species of desert lizards differ markedly in their times and places of activity. Some are active early in the morning, but other species do not emerge until late morning or midday. Most geckos and pygopodids and some Australian skinks are nocturnal. Certain species are climbers, others subterranean, while still others are strictly surface dwellers. Among the latter, some tend to be found in open areas whereas others frequent the edges of vegetation. Thermal relations of active lizards vary widely among species and are profoundly influenced by their spatial and temporal patterns of activity. Body temperatures of some diurnal heliothermic species average 38°C or higher, whereas those of nocturnal thigmothermic species are typically in the mid-twenties, closely paralleling ambient air temperatures.

Interesting interspecific differences also occur in the variance in body temperature as well as in the relationship between body temperatures and air temperatures. For example, among North American lizards, two arboreal species (Urosaurus graciosus and Sceloporus magister) display narrower variances in body temperature than do terrestrial species. Presumably, arboreal habits often facilitate efficient, economic, and rather precise thermoregulation. Climbing lizards have only to shift position slightly to be in the sun or shade or on a warmer or cooler substrate, and normally do not move through a diverse thermal environment. Moreover, arboreal lizards need not expend energy making long runs as do most ground dwellers, and thus climbing species do not raise their body temperatures metabolically to as great an extent as do terrestrial lizards.

Such differences in temporal patterns of activity, the use of space, and body temperature relationships are hardly independent. Rather, they complexly constrain one another, sometimes in intricate and obscure ways. For example, thermal conditions associated with particular microhabitats change in characteristic ways in time a choice basking site at one time of day becomes an inhospitable hot spot at another time. Perches of arboreal lizards receive full sun early and late in the day when ambient air temperatures tend to be low and basking is therefore desirable, but these same tree trunks are shady and cool during the heat of midday when heat-avoidance behavior becomes necessary. In contrast, the fraction of the ground's surface in the sun is low when shadows are long early and late, but reaches a maximum at midday.

Terrestrial heliothermic lizards may thus experience a shortage of suitable basking sites early and late in the day moreover, during the heat of the day, their movements through relatively extensive patches of open sun can be severely curtailed. Hence, ground-dwelling lizards encounter fundamentally different and more difficult thermal challenges than do climbing species.

Radiation and conduction are the most important means of heat exchange for the majority of diurnal lizards, although the thermal background in which these processes occur is strongly influenced by prevailing air temperatures. Ambient air temperatures are critical to nocturnal lizards as well as to certain very cryptic diurnal species.

In an analysis of the costs and benefits of lizard thermoregulatory strategies, Huey and Slatkin (1976) identified the slope of the regression of body temperature against ambient environmental temperature as a useful indicator (in this case, an inverse measure) of the degree of passiveness in regulation of body temperature. On such a plot of active body temperature versus ambient temperature, a slope of one indicates true poikilothermy or totally passive thermoconformity (a perfect correlation between air temperature and body temperature results), whereas a slope of zero reflects the other extreme of perfect thermoregulation. Lizards span this entire thermoregulation spectrum. Among active diurnal heliothermic species, regressions of body temperature on air temperature are fairly flat (for several species, including some quite small ones, slopes do not differ significantly from zero) among nocturnal species, slopes of similar plots are typically closer to unity. Various other species (nocturnal, diurnal, and crepuscular), particularly Australian ones, are intermediate, filling in this continuum of thermoregulatory tactics.

A straight line can be represented as a single point in the coordinates of slope versus intercept these two parameters are plotted for linear regressions of body temperatures on air temperatures among some 82 species of lizards in Figure 5.22.

Each data point represents the least-squares linear regression of body temperature against air temperature for a given species of desert lizard. Interestingly enough, these data points fall on yet another, transcendent, straight line. The position of any particular species along this spectrum reflects a great deal about its complex activities in space and time. The line plotted in Figure 5.22 thus offers a potent linear dimension on which various species can be placed in attempts to formulate general schemes of lizard ecology (Pianka 1985, 1986a, 1993). Various other ecological parameters, including reproductive tactics, can be mapped on to this emergent spatial temporal axis.

The intriguing "intercept" of the intercepts (38.8°C) approximates the point of intersection of all 82 regression lines and presumably represents an innate design constraint imposed by lizard physiology and metabolism. It is presumably not an accident that this value also corresponds more or less to the body temperature of homeotherms, particularly mammals!

Birds, which maintain slightly higher body temperatures than mammals (Hamilton 1973), descended from another reptilian stock, the archosaurs, represented today by the crocodilians. Would a comparable study of crocodilian thermoregulation yield a higher intercept of the intercepts? (This prediction could be doomed to failure by the mere fact that crocodilians are aquatic and very large -- yet they obviously thermoregulate when out of the water.) Although most insects are so small that convective heat exchange prevents them from attaining body temperatures much higher than that of ambient air, some, such as bumblebees and butterflies, do exhibit behavioral thermoregulation would a plot for insects show more scatter and a different intercept?

Limiting Factors and Tolerance Curves

Ehrlich and Birch (1967) Errington (1956) Hairston, Smith, and Slobodkin (1960) Lack (1954, 1966) Liebig (1840) Murdoch (1966a) Odum (1959, 1963, 1971) Shelford (1913b) Terborgh (1971) Walter (1939).

Electronic supplementary material is available online at

Published by the Royal Society. All rights reserved.


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Circulatory Delivery of Sugars

Because they are both transported via the circulatory system, many of the adaptations in the “oxygen transport cascade” that enhance oxygen delivery simultaneously enhance the delivery of glucose, and potentially fructose (80). Rates of oxygen and sugar delivery to tissues are a function of cardiac output and blood oxygen or sugar levels, and are enhanced by higher capillary volume densities, which reduce diffusion or transport distances. Hummingbird heart rates during flight range between 480 and 1,200 beats/min (BPM) (18, 41), and their cardiac output is approximately five times their body weight per minute (33). Hematocrit, an indirect measure of oxygen-carrying capacity, is also high, at 56.3% (34). Bats generally also exhibit enhanced cardiac output and oxygen-carrying capacities. Frugivorous tent-making bat (Uroderma bibobatum) heart rates have been recorded reaching upward 900 BPM during flight (60). Egyptian fruit bats (Rousettus aegypticus) exhibit hematocrit values as high as 55%, greater than in similarly sized non-flying mammals such as shrews (39–50% Refs. 35, 73). Both hummingbirds (6) and nectar bats (25 mM Ref. 39) exhibit exceptionally high postprandial blood glucose levels compared with similarly sized terrestrial mammals. Electron micrograph analysis of hummingbird flight muscle reveals a two to six times higher capillary volume density compared with mammals (50), and although unreported in nectar bats, capillary volume density is high in insectivorous bats (51). Collectively, it is clear that glucose delivery to tissues is highly enhanced in these aerial nectarivores. Frustratingly, blood fructose levels are unreported in any of these groups. Thus similar conclusions about fructose delivery capacity remain elusive.

Oxygen and the carbon in dietary sugars converge in the mitochondria of aerobically active tissues. Thus the mitochondria, as end consumers of both oxygen and sugar carbon, play a key role in establishing the overall flux of each. Unsurprisingly, both nectar bats and hummingbirds exhibit exceptionally high activities of mitochondrial enzymes such as citrate synthase (83). Both structural and enzymatic properties of hummingbird mitochondria contribute to the increased rate of substrate utilization observed (50). Hummingbird mitochondria occur at densities near theoretical physiological maximums, comprising 35% of overall muscle fiber volume (81). Although not yet directly demonstrated in nectar bats, high mitochondrial abundance is unsurprisingly the case in bats in general (51), since they all employ energetically expensive flight to forage.

Data and analyses

We compiled data on avian resting metabolism, evaporative cooling, Tb and heat tolerance for one species of quail (Smith et al., 2015), five caprimulgids (O'Connor et al., 2017 Talbot et al., 2017), six columbids (McKechnie et al., 2016b Smith et al., 2015), two owls (Talbot et al., 2018), two parrots (McWhorter et al., 2018), one sandgrouse (McKechnie et al., 2016a), one cuckoo and one roller (Smit et al., 2018) and 29 passerines (Czenze et al., 2020 Kemp and McKechnie, 2019 McKechnie et al., 2017 Smit et al., 2018 Smith et al., 2017 Whitfield et al., 2015) from recent literature (Table S1). In addition, we included unpublished data for one species of each of the following: owl, sandgrouse, barbet, swift, mousebird, kestrel, thick-knee and passerine (Table S1).

In brief, all these data were collected using flow-through respirometry under conditions of low chamber humidity (dewpoints typically ∼0°C) maintained using higher-than-typical flow rates (for details, see Whitfield et al., 2015). Birds were held in the dark and exposed to stepped profiles of increasing Ta in increments of 2°C when Ta>40°C, spending 10–30 min at each Ta value until stable Tb, EWL and RMR were reached. These conditions cannot be considered steady-state and the experimental protocol is analogous to the sliding cold exposure protocol used to elicit summit metabolism (Swanson et al., 1996). Steady-state measurements similar to those when quantifying parameters such as basal metabolic rate, where birds typically experience a single Ta value for 6–8 h, are not feasible when Ta is well above Tb and EWL may exceed 5% Mb h −1 . Measurements ended when birds showed a loss of balance, lack of coordination or thermoregulatory failure, after which they were allowed to recover with ad libitum access to water and food before being released at their sites of capture. One study in which individuals were monitored for several weeks after release revealed no obvious adverse effects of the experimental protocol (Kemp and McKechnie, 2019).

From each study we obtained minimum values for Tb, EWL and RMR at thermoneutrality (typically 30–35°C), inflection Ta values above which each variable increased, the slopes of relationships at Ta above inflections and maximum values associated with thermal endpoints for calm birds, which were taken in all the studies as the heat tolerance limit (HTL), the Ta associated with loss of balance, coordination or rapid, uncontrolled increases in Tb, or sudden decreases in EWL or RMR (Whitfield et al., 2015). In these studies, the relationship between EWL and Ta was modelled using linear models at Ta above an inflection point. Although a number of authors have argued that the increase in EWL at high Ta is exponential rather than linear (e.g. Weathers, 1981, 1997), comparisons of the explanatory power of linear and polynomial models suggest little difference (Whitfield et al., 2015), and linear models greatly simplify comparisons among and within species.

Correlations between functional traits of passerines

A recent comparison of interspecific differences in thermal physiology between regularly drinking and non-drinking passerines from southern Africa revealed that HTL is correlated with evaporative scope, the ratio of maximum EWL to minimum EWL at thermoneutrality (Czenze et al., 2020). To test whether this correlation holds among passerines more broadly, we tested for significant relationships between evaporative scope and residual HTL (HTL scales significantly with Mb Fig. 2) and between the maximum ratio of evaporative heat loss (EHL) to metabolic heat production (MHP). To evaluate relationships between Tuc and increases in EWL above minimal levels and the onset of panting, we also fitted linear models to residual Tuc and inflection Ta for EWL, and residual Tuc and the Ta associated with the onset of panting. We restricted these analyses to the 30 passerines in our data set to avoid the potentially confounding effects of EHL via gular flutter or rapid cutaneous evaporation that predominates in several non-passerine orders.

Scaling of avian maximum body temperature and heat tolerance limits. (A) Maximum body temperature (Tb) during acute heat exposure decreases with increasing body mass (Mb, g) among passerines, with a best-fit model of Tb=−0.814log10Mb+45.734. (B) Difference between maximum Tb and normothermic daytime Tb under thermoneutral conditions (ΔTb) scales negatively among passerines (ΔTb=−1.374log10Mb+5.956) but positively among columbids (ΔTb=2.646log10Mb−2.525). (C) Heat tolerance limit (HTL, i.e. the maximum air temperature tolerated) scales positively among all species in our data set (HTL=4.867log10Mb+43.040) as well as within passerines (HTL=3.873log10Mb+43.107). All regressions are phylogenetically independent models generated using phylogenetic least squares regressions. See ‘Data and analyses’ section for details.

Scaling of avian maximum body temperature and heat tolerance limits. (A) Maximum body temperature (Tb) during acute heat exposure decreases with increasing body mass (Mb, g) among passerines, with a best-fit model of Tb=−0.814log10Mb+45.734. (B) Difference between maximum Tb and normothermic daytime Tb under thermoneutral conditions (ΔTb) scales negatively among passerines (ΔTb=−1.374log10Mb+5.956) but positively among columbids (ΔTb=2.646log10Mb−2.525). (C) Heat tolerance limit (HTL, i.e. the maximum air temperature tolerated) scales positively among all species in our data set (HTL=4.867log10Mb+43.040) as well as within passerines (HTL=3.873log10Mb+43.107). All regressions are phylogenetically independent models generated using phylogenetic least squares regressions. See ‘Data and analyses’ section for details.

Potential error associated with use of allometrically predicted values

To quantify the potential error associated with predicting ecologically relevant parameters related to risk of lethal dehydration during extreme weather events on the basis of allometrically predicted rates of EWL rather than species-specific empirical data, we compared cumulative 6 h water loss and time to lethal dehydration [cumulative EWL >15% of Mb, following Albright et al. (2017) and Conradie et al. (2020)] using both approaches. We modeled evaporative water requirements using a Ta profile corresponding to an extremely hot day with a Ta maximum of ∼48°C (data from, for each of 27/30 passerines in our data set. We excluded curve-billed thrasher (Toxostoma curvirostre) on account of an atypically high EWL inflection Ta (Smith et al., 2017) and white-browed sparrow-weaver (Plocepasser mahali) and sociable weaver (Philetairus socius) on account of EWL inflection Ta values not being reported in the original study (Whitfield et al., 2015). For each species, we modelled cumulative EWL during the 6 h period between 09:00 and 15:00 h using the actual slope of EWL against Ta, and then using the slope predicted from a regression model fitted to all passerine data in our data set. We took the actual and predicted survival times for each species as the period over which cumulative EWL remained ≤15% Mb. We used linear regressions forced through the origin to model relationships between predicted and actual values, and calculated 95% prediction intervals for these models following Cooper and Withers (2006).

Scaling analyses

To quantify relationships between physiological variables and Mb and to test for correlations between variables, we initially fitted linear regression models in R ( For variables that scaled significantly with Mb, we used the R package ape (Paradis and Schliep, 2018) to test for phylogenetic signal using the parameter λ (Freckleton et al., 2002). We used a consensus phylogenetic tree generated from 1000 trees downloaded from (Jetz et al., 2012) using the Hackett et al. (2008) phylogeny as a backbone. From these trees, a 50% majority-rule consensus tree was calculated using the consensus function in ape, as recommended by Rubolini et al. (2015). As significant phylogenetic signal was present for all variables examined, we present phylogenetically informed models based on phylogenetic least squares regressions using the ‘gls’ function in ape. All phylogenetic analyses were performed following Garamszegi (2014). Coefficients are presented with standard error of the mean (s.e.m.) and sample sizes (N) refer to number of species.

Food Intake versus ability to flee among birds, particularly the hummingbird? - Biology

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Concentration-Dependent Sugar Preferences of the Malachite Sunbird (Nectarinia famosa)

Mark Brown, * Colleen T. Downs, 1,* Steven D. Johnson 1

1 School of Biological and Conservation Sciences, University of KwaZulu-Natal, Private Bag X01, Scotts

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Sugar-type preferences of nectarivores may be an important selective factor in the evolution of sugar composition in floral nectar. We investigated sugar preferences of the Malachite Sunbird (Nectarinia famosa), using experiments in which birds were offered paired choices between energetically equivalent solutions over a range of sugar concentrations. The birds preferred hexose at low (5%) concentration and sucrose at high (25%) concentration they showed no preference at 10%, 15%, and 20% concentrations. The birds regulated energy intake by adjusting volumetric consumption, except on a 5% concentration diet, where they failed to maintain energy balance. They also exhibited a strong preference for concentrated solutions, given a choice between 10%, 15%, 20%, and 25% sucrose solutions. We discuss the significance of these results in terms of the nectar composition of sunbird-pollinated plants.

© 2010 by The American Ornithologists' Union. All rights reserved. Please direct all requests for permission to photocopy or reproduce article content through the University of California Press's Rights and Permissions website,

Mark Brown , Colleen T. Downs , and Steven D. Johnson "Concentration-Dependent Sugar Preferences of the Malachite Sunbird (Nectarinia famosa)," The Auk 127(1), 151-155, (1 January 2010).

Received: 5 August 2008 Accepted: 1 July 2009 Published: 1 January 2010

Food Intake versus ability to flee among birds, particularly the hummingbird? - Biology


1 Department of Ecology & Evolutionary Biology, University of Arizona, Tucson, AZ 85721
USA, e-mail: [email protected]

2 Departamento de Ecología, Facultad de Ciencias Biológicas, P. Universidad Católica de
Chile, Casilla 114-D, Santiago, Chile, e-mail: [email protected]

Balance between energy acquisition and expense is critical for the survival and reproductive success of organisms. Energy budgets may be limited by environmental factors as well as by animal design. These restrictions may be especially important for small endotherms such as hummingbirds, which have exceedingly high energy demands. Many nectar-feeding bird species decrease food intake when sugar concentration in food is increased. This feeding response can be explained by two alternative hypotheses: compensatory feeding and physiological constraint. The compensatory feeding hypothesis predicts that if birds vary intake to maintain a constant energy intake to match energy expenditures, then they should increase intake when expenditures are increased. Broad-tailed hummingbirds ( Selasphorus platycercus ) and Green-backed fire crown hummingbirds ( Sephanoides sephaniodes ) were presented with diets varying in energy density and exposed to various environmental temperatures. Birds decreased volumetric food intake in response to sugar concentration. However, when they were exposed to lower environmental temperatures, and hence increased thermoregulatory demands, they did not increase their rate of energy consumption and lost mass. These results support the existence of a physiological constraint to the energy budgets of hummingbirds. Digestive and peripheral organ function limitations may impose severe challenges to the energy budgets of these small endotherms, and therefore play a significant role in determining their distribution, ecology, and natural history.

Key words: energetics, digestion, feeding behavior, hummingbirds, nectarivory.

El balance entre la adquisición y el uso de energía es crítico para la reproducción y sobrevivencia. Los presupuestos energéticos de los organismos pueden estar limitados tanto por factores ambientales como por su fisiología. Estas restricciones pueden ser especialmente importantes para pequeños endotérmos como los colibríes (picaflores) que tienen costos energéticos altos por unidad de masa. Muchas especies de aves nectarívoras reducen el consumo de alimento cuando la concentración de azúcar aumenta. Esta respuesta puede ser explicada por dos hipótesis alternativas: compensación alimenticia y restricciones fisiológicas. La primera hipótesis predice que las aves varían el consumo para mantener la ingesta de alimento ajustada a sus gastos energéticos. Por ende, cuando los gastos energéticos aumentan, el consumo debe aumentar. Colibríes vibradores ( Selasphorus platycercus ) y picaflores ( Sephanoides sephaniodes ) fueron alimentados con dietas de contenido energético variable y expuestos a varias temperaturas ambientales. Las aves redujeron el volumen consumido en respuesta a un incremento en la concentración de azúcar. Sin embargo, cuando fueron expuestos a bajas temperaturas, y por lo tanto a mayores demandas de termoregulación, no aumentaron su consumo de energía y perdieron masa corporal. Estos resultados indican la existencia de una limitante fisiología que restringe a los presupuestos energéticos de los colibríes. Limitaciones funcionales (digestivas o periféricas) pueden imponer seríos dilemas para los presupuestos de energía de estos pequeños endotérmos y por lo tanto jugar un papel significativo en su distribución, ecología, e historia natural.

Palabras clave: energética, digestión, conducta de alimentación, picaflores, nectarivoría.

Nectar feeding animals provide physiological ecologists with relatively simplified systems in which to study the interaction of diet, physiology, and ecology. Hummingbirds are among the most intriguing subjects because they are among the smallest endothermic vertebrates and have extremely high mass-specific metabolic rates (Pearson 1950, Lasiewski 1963, Bartholomew & Lighton 1986). The energetic cost of hovering flight employed by foraging hummingbirds (Suarez 1992) sets them apart from other nectarivores and in combination with their small size makes them especially sensitive to energy stress (Tooze & Gass 1985, McNab 1988). In addition to confronting the problems of endothermy at small body sizes, hummingbirds often face large fluctuations in energy availability and energetic demands (Gass & Lertzman 1980, Montgomerie & Gass 1981). Furthermore, many species of hummingbirds that breed in temperate, high latitude areas face the additional energetic cost of migrating long distances between breeding and wintering grounds (see for example Calder 1993). The ability of the digestive system to obtain energy to meet demands and peripheral organs to transform energy to work must be tightly coupled in hummingbirds. The simultaneous regulation of energy intake and energy use has the potential to limit physiological, behavioral and ecological capacities in these animals (Beuchat et al. 1990, McWhorter & Martínez del Río 1999).

Although hummingbirds are able to modify their behavior (Ewald & Carpenter 1978, Gass 1978, Tiebout 1991) and utilize energy saving strategies, such as torpor, to enhance their ability to deal with energetically adverse conditions (Calder 1994 and references therein), they still appear to live teetering on the edge of the chasm of negative energy balance. What factors influence the energy budgets of small endotherms such as hummingbirds? In addition to potential ecological constraints on energy budgets (i.e. resource availability and competition), the idea that physiological limitations may restrict the energy budgets of animals has gained support over the past decade (Weiner 1992, Hammond & Diamond 1997). Physiological constraints include limits to both rates of energy acquisition (foraging, food ingestion, digestion and absorption) and energy expenditure (work, heat production and tissue growth, Weiner 1992). Animals may maintain energy balance by dynamically regulating nutrient uptake capacity and energy expenditure (i.e. changing the relative importance of central versus peripheral limitations) based on the conditions they experience. Despite the considerable flexibility that hummingbirds exhibit in their energy management, physiological constraints may be important in determining their life histories.

In this paper we review the interplay of diet, physiological constraints, and ecology as determinants of food intake. Specifically, we examine some of our recent research on the physiological and behavioral responses of hummingbirds to manipulation of environmental energy availability and energetic demands. In addition, the modeling of gut function based on chemical reactor theory is presented as a tool to understand the digestive physiology of nectar-feeding animals. We argue that adopting an integrative, mechanistic approach to the study of the physiological ecology of hummingbirds is key to understanding their behavior, ecology and distribution.

A major goal in physiological ecology is to understand the factors that may influence the ecological roles and abilities of animals. For hummingbirds, energy budgets and constraints thereof are undoubtedly among the most important influences. Because their nectar diets are relatively energy dilute and their mass-specific metabolic rates so high, physiological limitations to energy acquisition and energy utilization may be equally important. We are going to begin to examine the factors that influence the energy budgets of hummingbirds by introducing a behavioral feeding pattern and its ecological correlates. We will then introduce a series of experiments designed to differentiate between possible explanations for this pattern and determine the nature of potential physiological constraints.

Effects of sugar concentration on hummingbird feeding and energy use

The energy content of food and its spatial and temporal availability determine both the net energy that a foraging hummingbird can obtain and how it manages its daily energy budget (López-Calleja et al. 1997). Nectar sugar concentration, therefore, probably has a strong effect on hummingbird foraging behavior. Indeed, foraging time and resource removal rates are functions of feeding rate, which is dictated by digestive capacities and ultimately the energy demands of the animal (Karasov 1990). López-Calleja et al. (1997) experimentally varied nectar sugar concentration and investigated the effect on feeding patterns and energy use in hummingbirds, using captive Green-backed firecrowns ( Sephanoides sephaniodes ). Their work tested the assumptions and predictions of a model of hummingbird feeding that assumes gut processing rates are linearly correlated with sugar concentration in food (Martínez del Río & Karasov 1990). The model makes several predictions about how hummingbirds should respond to sugar concentration if their goal is to maximize energy gain. The predictions examined by López-Calleja et al. (1997) are the following: (a) Hummingbirds should assimilate the sugars in their diets essentially completely, regardless of sugar concentration (b) Increased sugar concentration should lead to increased rates of energy intake and (c) Meal retention times, and hence inter-meal intervals, should increase linearly with sugar concentration. Note that the second prediction in particular follows from the assumption that hummingbirds behave to maximize their rate of energy intake.

The feeding behavior and digestive performance of hummingbirds supported several of the predictions of the model (López-Calleja et al. 1997). Hummingbirds assimilated the sugars in their food almost completely, regardless of sugar concentration. This pattern is common to all of the hummingbird species that have been examined thus far (Karasov et al. 1986, Hainsworth 1988, Martínez del Río 1990b, McWhorter 1997) and suggests that assimilation efficiency is independent of sugar concentration (López-Calleja et al. 1997). Processing time index (PTI), proposed by Martínez del Río (1990b) as an indirect measurement of meal retention time, increased with sugar concentration. Inter-meal intervals also increased linearly with sugar concentration. Energy assimilation was not, however, correlated with sugar concentration as predicted. Despite a ten-fold variation in food intake between 0.25 and 0.75 M sucrose solutions, energy assimilation remained constant at about 35 kJ/day (López-Calleja et al. 1997). This result falsified perhaps the most important prediction of Martínez del Río and Karasov’s (1990) model, which is that energy intake would be positively correlated with sugar concentration. This can be interpreted either as evidence that hummingbirds do not function as "energy maximizers" (sensu Schoener 1971) at the temporal scale of a day, or that gut processing rates somehow constrain the rate of energy assimilation (Karasov et al. 1986, Levey & Martínez del Río 1999). Many observations have suggested that at the temporal scale of a day hummingbirds regulate energy intake at a relatively constant level (Hainsworth 1978, 1981, Hainsworth & Wolf 1983). Discerning whether hummingbirds are defending a constant rate of energy assimilation or are constrained to a maximal rate of energy assimilation requires that they be exposed to environmental conditions that force them to increase their rate of energy expenditure (López-Calleja et al. 1997). Such conditions include low temperature (Kendeigh et al. 1969), unpredictable resource availability or temperature (Caraco et al. 1990, Elkman & Hake 1990), and long distances to food sources (Tiebout 1991). The next section describes experiments designed to differentiate between these possible explanations using acute exposure to low ambient temperatures.

Does gut function limit hummingbird food intake?

Hummingbirds respond to experimentally increased sugar concentration in food by decreasing volumetric intake (Fig. 1, see also López-Calleja et al. 1997, McWhorter 1997). This inverse relationship between intake and sugar concentration is common to many nectar-feeding birds (Collins 1981, Downs 1997, Lotz & Nicolson 1999). Similar reciprocal relationships between nutrient/energy density and food intake have been described in a variety of animals (Montgomery & Baumgardt 1965, Batzli & Cole 1979, Simpson et al. 1989, Nagy & Negus 1993, Castle & Wunder 1995). The widespread occurrence of such intake-response patterns has often been attributed to compensatory feeding (Simpson et al. 1989). This explanation supposes that animals regulate food intake to maintain a constant flux of assimilated energy or nutrients (Montgomery & Baumgardt 1965, Slansky & Wheeler 1992). Animals compensate for decreased energy density in food by increasing intake. An alternative explanation is that intake is constrained by the ability of animals to assimilate the nutrients contained in food (see above, Karasov et al. 1986, Levey & Martínez del Río 1999). McWhorter and Martínez del Río (in press) address the question of whether the intake-response relationship observed in hummingbirds is the result of compensatory feeding or a digestive constraint to energy assimilation. Animals must be exposed to environmental conditions that acutely increase their energetic demand in order to discern between these possibilities, because chronic cold exposure in endotherms is often accompanied by increased digestive and metabolic capacities (Konarzewski & Diamond 1994 and references therein).

Relación entre la ingesta volumétrica de alimento y la concetración de azucar en picaflores y mieleros-serranos. La relación recíproca es común a una amplia variedad de animales y se ha atribuido a alimentación compensatoria. Los datos se describen por una función potencial con pendientes que varían entre -0,71 y -0,95. Interesantemente,la pendiente es significativamente menor que uno y en algunos casos no está correlacionada con los taxa. La ingesta (I) disminuye significativamente con un aumento en la concentración de sacarosa en la dieta ( C) de la siguiente manera: Selasphorus plalycercus I = 1502,0 C -0.77 Archilochus alexandri I = 1582, 7 C -0.75 Eugenesfulgens I = 1697,3 C -0.76 Lampornis clemenciael = 1606,2 C -0.71 Sephanoides sephaniodes I = 4638,6 C -0.95 Diglossa baritula I = 3789,9 C -0.92 .

The resting metabolic rate of Broad-tailed hummingbirds ( Selasphorus platycercus ) is considerably higher at 10°C than at 20°C (Bucher & Chappell 1988). Based on this observation McWhorter and Martínez del Río (in press) hypothesized that for a given food energy density, birds exposed to lower temperatures would show increased food intake. An increase in sugar intake under energetically demanding conditions would support the compensatory feeding explanation. Conversely, the opposite result would provide evidence that a physiological process limits sugar assimilation. Broad-tailed hummingbirds were exposed to 10°C and 22°C and fed diets ranging in sugar concentration from 292 to 1168 mmol/L sucrose. Birds exhibited the expected reciprocal relationship between intake and food energy density, but did not significantly increase food consumption when exposed to low environmental temperatures (McWhorter & Martínez del Río in press). This failure to increase food intake when acutely challenged by cold temperatures was interpreted as evidence for the existence of a physiological constraint to energy assimilation. The conclusion that broad-tailed hummingbirds were unable to increase their food intake to meet increased energetic demands was supported by two additional observations. First, birds lost significantly more body mass at the lower temperature. Second, birds exposed to 10°C were often observed emerging from torpor in the morning and exhibited behaviors commonly associated with energy conservation (ptiloerection, decreased flying time, feet held close to body in flight, Gass & Montgomerie 1981, Udvardy 1983). Regardless of any energy conserving mechanisms employed, it appeared that acutely cold-exposed hummingbirds could not process energy fast enough to compensate for their higher energy demands. Increased torpor use by cold-exposed hummingbirds highlights the subtle interrelation of their digestive and metabolic traits. Balancing their precarious energy budget may require hummingbirds to use energy conserving strategies when energetic demands are increased and energy acquisition is constrained (McWhorter & Martínez del Río in press).

The apparent inability of hummingbirds to increase energy assimilation when subjected to higher energetic demands led McWhorter & Martínez del Río (in press) to speculate about the factors potentially imposing an upper limit to food intake. Physiological processes that determine rates of sugar assimilation are important potential limiting factors because the vast majority of energy acquired by hummingbirds comes from dietary sugars. Sugar ingestion can be limited by rates of sucrose hydrolysis or transport of the resulting monosaccharides (Karasov et al. 1986, Martínez del Río 1990a), and by rates of sugar catabolism or biosynthetic processes (Suarez et al. 1988, Suarez et al. 1990). McWhorter & Martínez del Río (in press) focused on the potential role of digestive processes in limiting energy assimilation. Because previous methods developed to compare the capacity of the intestine to hydrolyze and absorb nutrients with ingested loads appear to overestimate digestive capacity, an alternative model of sucrose hydrolysis in hummingbird guts was developed. This method relies on modeling the intestine of hummingbirds as a plug-flow chemical reactor (Penry & Jumars 1987), and was described in detail by McWhorter & Martínez del Río (in press). Sucrase activity measurements in vitro, sugar assimilation rates and intestinal morphology were used to predict intake rates for four experimental sucrose concentrations. The intake rates predicted using this model slightly overestimated observed intake rates, but there was a remarkable qualitative resemblance between the model’s output and bird behavior. The safety factors (defined as the ratio of capacity to load) estimated using this method are considerably lower than those predicted by integrating the maximum capacity of intestinal hydrolases along the length of the intestine as proposed by Diamond and Hammond (1992). Because the model developed by McWhorter & Martínez del Río (in press) includes greater physiological detail than previous methods, it may lead to a less biased estimate of hydrolytic capacity. Most significantly, the model takes into account the decline in sucrose concentration along the gut that accompanies hydrolysis. The lower safety factors predicted by the model indicate that broad-tailed hummingbirds ingested as much sucrose as they had the ability to process. Consequently, when they were faced with increased energetic demands, they were unable to increase energy assimilation to meet them.

The cold exposure experiments performed by McWhorter & Martínez del Río (in press) were specifically designed to differentiate between compensatory feeding and constraints to energy acquisition. Cold exposure was acute in these experiments because chronic exposure to increased energy demands leads to increased intake and is typically accompanied by increased digestive and metabolic capacities (Konarzewski & Diamond 1994). For example, Hammond et al. (1994) demonstrated that the higher intake shown by cold-acclimated mice is accompanied by hypertrophy of the gastrointestinal tract. It would make sense that hummingbirds are similarly capable of increasing intake and assimilation. McWhorter & Martínez del Río (in press) showed that the physiological capacities of hummingbirds are well matched to the loads that they experience normally. When energy demands were increased, birds were unable to match them and lost body mass. Based on these results, we hypothesized that chronic cold exposure would lead to up-regulation of the ability to assimilate energy and to a new match between demands and capacities. If this hypothetical scenario is correct, it leads to an important ecological consequence of the tight matching of physiological capacities and ecological demands. The energetic savings provided by not having a large spare digestive capacity could come at the cost of short-term behavioral flexibility. In hummingbirds, such tight matches between the ability to assimilate energy and the normal energetic demands of the environment can result in periods during which the animals lose mass. In the next section, we describe experiments that explore the factors accounting for the regulation of energy budgets when hummingbirds are chronically exposed to low environmental temperatures and energy dilute diets.

What factors impose a ceiling to the energy budget of hummingbirds?

Physiological constraints to the energy budgets of animals may include limits to either the energy-supplying physiological machinery (central limitation hypothesis), the energy-consuming machinery (peripheral limitation hypothesis), or both (Kirkwood 1983, Petersen et al. 1990, Koteja 1996a, 1996b). Central limitations include aspects directly related to the assimilation of nutrients and energy. Digestive capacities, such as nutrient hydrolysis and uptake rates, influence food ingestion rate and ultimately foraging behavior (Karasov 1990, Martínez del Río 1990a). Peripheral limitations involve pathways through which absorbed nutrients are converted to work, heat production and growth (Weiner 1992). Limitations to the catabolism of absorbed sugars and/or shunting into biosynthetic pathways has the potential to limit feeding rates (Suarez et al. 1988, Suarez et al. 1990). Physiological limitations are undoubtedly of primary importance to small endothermic vertebrates such as hummingbirds. The studies that we have previously described focus mainly on establishing the existence of physiological constraints, and to some extent exploring the factors responsible for those constraints. We believe that peripheral limitations, which these studies did not explore, may be as important as central limitations for hummingbirds.

López-Calleja & Bozinovic (pers. comm.) explored the influence of energy acquisition and expenditure on the energy and time budgets of captive S. sephaniodes . Their study was designed to provide a quantitative assessment of the factors (central versus peripheral limitation) responsible for regulating and limiting the energy budgets of hummingbirds. Birds were tested using two experimental diets (high and low energy density) and two environmental temperatures (within their thermoneutral zone and low temperature), and were acclimated to these conditions for 15 days before experiments began. Volumetric food intake, body mass, time budgets and metabolic rates were measured during the experimental period. After experiments, birds were killed in order to measure organ masses and fat content. In agreement with other studies on hummingbirds (López-Calleja et al. 1997, McWhorter 1997, McWhorter & Martínez del Río in press), volumetric food intake was negatively correlated with sugar concentration, independent of thermal conditions (López-Calleja & Bozinovic pers. comm.). Birds in their thermoneutral zone feeding on the high quality diet (higher quality defined as higher energy density HQ-TNZ) maintained body mass throughout the experimental period. Birds challenged with lower quality diets and cold temperatures (LQ-LT) decreased their body mass. Birds in the remaining two treatment groups (HQ-LT and LQ-TNZ) showed slight decreases, but body mass stabilized toward the end of the acclimation period. Since rates of sugar assimilation are limiting when hummingbirds are subjected to increased energetic demands over the short term (McWhorter & Martínez del Río in press), these decreases in body mass make functional sense. If the input side of an energy budget cannot be increased, then the output side must be decreased. Reduced body mass is accompanied by lower net energy demands. The observation that birds lost mass when challenged with energy-dilute food and/or cold temperatures chronically confirms a physiological constraint to their energy budgets. A closer look at patterns of energy use and changes in organ mass was necessary, however, to discern whether the limitation is central or peripheral.

Fat free carcass mass (including the flight muscles, which may compose up to a third of a hummingbird’s body mass) increased significantly in cold-exposed birds, as did heart and lung mass (López-Calleja & Bozinovic pers. comm.). In addition, significant increases in intestinal nominal area and kidney mass were detected in birds fed the low quality diet. The overall decrease in body mass observed in cold-exposed birds was presumably due to decreased fat stores. Daily energy expenditure (DEE) and the proportion of energy used for thermoregulation increased significantly in cold-exposed birds (López-Calleja & Bozinovic pers. comm.). The time budgets of birds also changed as a consequence of energy challenges. Cold-exposed birds spent less time flying and feeding and used torpor much more frequently and for longer periods than birds at milder temperatures (López-Calleja & Bozinovic pers. comm.).

What do these observations say about physiological constraints to the energy budgets of hummingbirds? Changes in the time budgets of birds, such as decreased flying time and feeding frequency, and increased torpor use indicate the existence of an energetic constraint, but not where it may lie. The increase in energy-consuming organs (flight muscles, heart, lungs) may reveal that the higher metabolic rates observed in cold-exposed birds required a concomitant increase in organ size (Konarzewski & Diamond 1995). It is conceivable that the combined energetic demands of hovering flight and increased thermoregulatory costs exceeded the capacity of the energy-consuming organs to produce work and heat, which indicates a peripheral limitation. The increase in the absorptive surface area of the intestine, on the other hand, indicates a central limitation. It appears that both central and peripheral limitations are important influences on the energy budgets of hummingbirds.

The energy supplying and energy consuming physiological machinery of hummingbirds are without doubt closely matched. Hummingbirds are nevertheless subject to rapid and unpredictable fluctuations in environmental temperatures and resource availability (Gass & Lertzman 1980, Montgomerie & Gass 1981). Such tight matches between the ability to assimilate energy and the normal energetic demands of the environment result in periods during which birds are in negative energy balance. The energetic savings provided by not having a large spare digestive capacity indeed appeared to come at the cost of short-term behavioral flexibility. Birds subjected to low temperatures and energy dilute foods utilized torpor to a much greater extent than other birds, but the energy savings provided by this strategy were not adequate to prevent negative energy balance and significant mass loss (López-Calleja et al. 1997, McWhorter & Martínez del Río in press, López-Calleja & Bozinovic pers. comm.). Chronic cold exposure, however, led to a new balance between energetic demands and the ability to assimilate and utilize energy. We propose that the relative importance of central or peripheral limitations changes dynamically, based on the conditions experienced by the animal. The considerable flexibility that hummingbirds exhibit in their energy management over the long term is critical for their survival and reproductive success, and greatly broadens the ecological role that they may occupy.


Interest in physiological constraints to the energy budgets of animals stems from the conjecture that many animals routinely operate at near maximum intensity (Weiner 1992). Kirkwood (1983) computed an allometric equation that predicts the maximum metabolizable energy input for a variety of animals. The predictions of this allometry imply that the energy budgets of animals are limited, often to levels equal to or only slightly higher than rates of energy expenditure observed in the field (Nagy 1987). Apparently, some animals operate with little safety margin between energetic load and capacity. Physiological limitations may therefore be more important than environmental constraints, such as resource availability, for the energy budgets of animals (Weiner 1992). Indeed, many authors have suggested that knowledge of the digestive and metabolic physiology of birds is a crucial, albeit neglected, component in understanding their behavior and feeding ecology (Karasov et al. 1986, Karasov 1990, Petersen et al. 1990, Weiner 1992, Martínez del Río & Restrepo 1993, Martínez del Río 1994, Karasov 1996, Sabat et al. 1998). The observation of sucrose avoidance in passerines in the Sturnidae-Muscicapidae lineage that lack the enzyme sucrase (Martínez del Río et al. 1988, Karasov & Levey 1990, Martínez del Río 1990a) is an excellent example of how physiological traits determine behavior and resource utilization in birds. Previous research on hummingbirds has emphasized the regulation of energy budgets in the face of changing energy demands and availability without directly examining the underlying physiological mechanisms involved (Calder 1975, Hainsworth 1978, Hainsworth 1981, Hainsworth & Wolf 1983, Calder 1994). We argue that avoiding such "black box" approaches by asking broad, integrative questions about the physiology of hummingbirds can lead to a greater understanding of the factors that determine their behavior and ecology.

Hummingbirds are perhaps the most specialized nectarivorous vertebrates. They exhibit remarkably high rates of sucrose hydrolysis (Martínez del Río 1990a) and the highest rates of carrier-mediated glucose transport reported among vertebrates (Karasov et al. 1986). Their digestive systems appear extremely well suited to digest and absorb a sucrose rich diet. Likewise, their energy consuming metabolic machinery is well matched to their energetically demanding lifestyle. Hummingbirds have high lung oxygen diffusing capacities, cardiac outputs, mitochondrial volume densities, cristae surface densities and concentrations of enzymes involved in energy metabolism (Suarez 1998 and references therein). Although it is clear that hummingbirds are impressively equipped for their energetically demanding lifestyles, the specific factors responsible for imposing a ceiling to their energy budgets were previously unclear. The studies we have reviewed in this paper provide support for the notion that both central and peripheral limitations are significant influences on the energy budgets of hummingbirds (López-Calleja et al. 1997, McWhorter & Martínez del Río in press, López-Calleja & Bozinovic pers. comm.). The concept of symmorphosis would argue that all structures of an organism are precisely tuned to one another, so that the functional capacity of one structure does not exceed any other (Weibel et al. 1991, Weiner 1992). Although we agree that the functional capacities at each step in linear pathways are probably well matched (i.e. that there is not a single rate limiting step, Suarez 1998), we suggest that the relative importance of central or peripheral limitations changes dynamically. Regardless of the specific limitations in effect in any given situation, the putative effects of physiological limitations to energy budgets define the ecological capacities of hummingbirds, and undoubtedly contribute to the establishment of the lower size limit for endothermic homeotherms.

The integrative approaches adopted by the studies reviewed in this paper provide a mechanistic bridge between ecological patterns and physiological capacities at organism, tissue and cellular levels. This type of approach may be particularly useful for identifying the nature of physiological constraints and testing under what conditions these constraints have an ecological function (Karasov 1986). The ongoing process of developing and testing mathematical models of digestive function has been an indispensable tool for understanding the digestive physiology of nectar-feeding animals. The remarkably accurate predictions of sugar intake made by McWhorter & Martínez del Río’s (in press) model highlight the usefulness of this approach. We have made the assumption that the digestive limitations documented for hummingbirds in captivity operate in the field. Models of digestive function lack relevance if their predictions are not testable under natural conditions. Hummingbirds present an unparalleled opportunity to test the usefulness of these models for understanding the ecology and behavior of nectar-feeding animals. Daily energy expenditures can be measured using standard methods (Powers & Nagy 1988, Tiebout & Nagy 1991) and digestive capacities can be estimated from floral nectar composition and the model presented by McWhorter & Martínez del Río (in press). Clearly, a better understanding of the digestive and metabolic traits of nectar-feeding birds, and how these factors influence each other, is necessary. It has been concluded based on previous research that the assumption of energy maximization is probably inappropriate for nectar-feeding animals that are not growing, storing fat, or reproducing (Karasov & Cork 1996, López-Calleja et al. 1997). The understanding of physiological limitations to the energy budgets of these animals may, however, be especially important under just those conditions. Additional laboratory and field studies are necessary to provide a complete picture of how and when physiological constraints are ecologically relevant for hummingbirds. Examination of the physiological traits of nectar-feeding birds can also provide insight into their roles as selective influences on the characteristics of other animals and plants with which they interact (Martínez del Río et al. 1992, Martínez del Río & Restrepo 1993). Further study at all levels, from the biochemical to organismal, as well as continued work towards integration, is necessary to clarify the relationships between capacities and loads in these animals (Suarez 1998). Adopting an integrative approach to the study of the physiological ecology of hummingbirds is key to understanding their behavior, ecology and distribution.

This paper resulted from the enjoyable symposium on avian physiological ecology organized by Francisco Bozinovic and Carlos Martínez del Río at the VI-Neotropical Ornithological Congress. Previous versions of this paper benefited from the critical comments of Carlos Martínez del Río, Donald R. Powers and Jorge E. Schöndube. Jorge E. Schöndube generously shared his unpublised data on flower-piercer food intake. Supported by Fondecyt 3000047 of M.V. López-Calleja.

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Flowers of P. angustifolia in the Rio Abajo Forest Reserve were visited by three species of pollinators with different visitation behaviors (long-billed hummingbird, honeybee, bananaquit). These pollinators were not equally efficient at depositing pollen after one flower visit. However, once their visitation rates were taken into account, all pollinators were equally effective at depositing pollen because flowers on a plant were expected to receive the same amount of pollen grains from each pollinator type over time.

As expected based on floral morphology, A. viridis was the most efficient pollinator per flower visit. With its long bill, A. viridis was the only visitor capable of legitimately reaching the nectar located at the base of the tubular corolla. Interestingly, when one considers only the effective pollinators, the two components of pollination effectiveness (pollination efficiency and visitation rates) were not correlated. Although the long-billed hummingbird was the most efficient visitor, it made many fewer visits per flower-hour-plant than bananaquits or honeybees (Fig. 1c).

There are at least three possible explanations for this incongruence between pollination efficiency and visitation rates by A. viridis. First, our observation periods showed that C. maugaeus, a visitor that acted as a secondary robber, effectively excluded A. viridis at least 17 times from P. angustifolia patches. Hummingbirds have high metabolic demands and thus require high rates of energy intake (Mongomerie and Gass, 1981). Aggressive interactions with other flower visitors may reduce the levels of net energy intake expected by A. viridis from P. angustifolia flowers and prevent these birds from visiting. A second possibility, although, not necessarily mutually exclusive, is that the nectar depletion caused by visits of the two species of nectar robbers (i.e., C. flaveola and C. maugaeus), leads to low visitation rates by long-billed hummingbirds. Given that flower preferences by hummingbirds are at least partially based on nectar availability (Meléndez-Ackerman et al., 1997 Meléndez-Ackerman and Campbell, 1998 Blem et al., 1997 Biernaskie et al., 2002), low visitation rates by long-billed hummingbirds should also be expected in P. angustifolia patches to the extent that nectar robbing reduces the nectar standing crop in this species (Irwin and Brody, 1998). A third alternative is the availability of other local flowering species that may be competing with P. angustifolia for pollinator service. Indeed, at this site long-billed hummingbird visits to flowers of the common timber tree Hibiscus elatus were observed although not quantified (J. J. Fumero-Cabán, personal observation).

Apis mellifera is a generalist forager and visits flowers with different pollination syndromes (Roubik, 1980 Aizen and Feinsinger, 1994). In agreement with other studies, A. mellifera had lower pollination efficiency than the native pollinator (Vaughton, 1996 Gross and Mackay, 1998 Hansen et al., 2002). Nevertheless, they visited flowers much more frequently than did A. viridis. Once visitation rates were taken into account, A. mellifera was as effective as A. viridis at depositing pollen. These results were unexpected given that there is a better morphological correspondence between the bills of A. viridis and P. angustifolia flowers relative to all remaining flower visitors. Moreover, where introduced, Apis mellifera is often considered to be detrimental to populations of native pollinators and thought to disrupt specialized relationships between native bee pollinators and their plants (Roubik, 1980). That was not the case in our study, where the recently introduced A. mellifera (now mostly feral) were found to be good pollinators of P. angustifolia and as effective as the bird pollinators of this species.

Flower visits by C. maugaeus, a secondary nectar robber indeed did not result in pollen transfer (Fig. 1a). Nevertheless, despite its behavior as primary nectar robbers, we found that C. flaveola did have pollination capabilities albeit incidental. We observed that flowers of P. angustifolia bent and struck against the bananaquit's body during the process of nectar robbing and that this bending motion of flowers most likely causes self-pollen to fall on the stigma. On a per visit basis this mode of pollination was much less efficient at pollen deposition than that of legitimate pollinators (i.e., A. viridis and A. mellifera, Fig. 1b). However, due to their relatively high visitation rates, bananaquits are still expected to deposit as much pollen per flower as the legitimate pollinators (Fig. 1c). The end result is that P. angustifolia flowers are visited by three animal species (two natives, one exotic) that are equally effective at depositing pollen even when long-billed hummingbirds can be much more efficient at pollen deposition on a per flower basis.

How do we reconcile the presence of a floral phenotype that seems adaptive to hummingbird pollination but yet maintains multiple pollinators? First, honeybees are a recently introduced species in Puerto Rico (fewer than 400 yr, Cox, 1994). Pitcairnia angustifolia plants are long-lived perennials thus one possibility is that there has not been enough time for honeybees to drive radical evolutionary changes in floral phenotypes. Second, recent models addressing fitness trade-offs between pollinators suggest that simply ranking pollinators by their relative effectiveness on the mean floral phenotype may not be enough to predict floral specialization (Aigner, 2001). These models suggest that factors such as the shape of fitness functions related to pollination service by individual pollinators as well as the strength of fitness interactions among available pollinators could be more important than pollination effectiveness in predicting floral specialization. The models argue that data on the fitness contributions by different pollinators over a variety of floral phenotypes would be required in order to address hypotheses on the potential for floral specialization (Aigner, 2001).

One potential limitation of our study is that we only considered the maternal component of pollination effectiveness (i.e., pollen deposition). Pollinators may also differ in their pollination effectiveness by affecting the rate of pollen transfer among flowers (Thomson and Goodell, 2001). Pollen grooming by pollen-collecting bees may lead to considerable pollen waste from the perspective of plants that depend on animal-mediated pollination (Stanton et al., 1992 Holsinger and Thomson, 1994). Indeed, Apis mellifera has shown lower transfer effectiveness relative to other bee pollinators under certain conditions (Thomson and Goodell, 2001). Similarly, pollination by C. flaveola is indirect and thus they may not be able to effect any pollination if flowers have already been visited and anthers have already been depleted of pollen. Thus, all other things being equal, long-billed hummingbirds could still be more effective pollinators if they circulate larger portions of pollen relative to honeybees and bananaquits.

Recent studies have shown that patterns of flower visitation in pollination systems are often generalized (Waser et al., 1996), especially for native and endemic plants on oceanic islands (Carlquist, 1974 Olesen et al., 2002). Local populations of P. angustifolia were effectively visited by three species (two native, one exotic) that differ functionally, yet no single flower visitor was statistically more effective than the other two (Fig. 1c). For selection to favor a generalized pollination system in P. angustifolia populations, plants must be exposed to consistent conditions of pollen limitation. Under this assumption, honeybee pollination could be favored under conditions of nectar robbing because the bees do not discriminate between robbed and intact nonrobbed flowers (Fumero-Cabán, 2004) they are frequent visitors and are not chased away by competitors. Less efficient but more abundant pollinators may compensate for the lack of main pollinators (Waser, 1979 Fleming et al., 2001 Mayfield et al., 2001 Rivera-Marchand and Ackerman, 2006). Coereba flaveola is a primary nectar robber, yet it still deposits a significant amount of pollen and thus behaves as a robber-like pollinator (Navarro, 2000, 2001). This type of activity can be particularly favorable to flowering plants during periods of low abundance of primary pollinators (Waser, 1979 Navarro, 2000, 2001). Conditions leading to temporal variation in the abundance of pollinators may be common on tropical islands like Puerto Rico that are subjected to frequent hurricanes (Weaver, 1986 Rathcke, 2000). Such large disturbances may also lead to unpredictable changes in the abundance of pollinators and may reduce the abundance of nectarivorous bird populations (Wunderle, 1995 Rathcke, 2000, 2001). To the extent that fluctuations in pollinator abundance are indeed dramatic at this site, a pollination system with multiple pollinators (and even some redundancy) could also be favored over time. Long-term studies are needed to determine the temporal stability of the interaction between P. angustifolia and its pollinators and their long-term role in floral evolution on this plant species.

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