Lecture Notes II - Foraging Behavior

Natural selection may favor 'efficient' foragers, and efficient may mean that

• individuals maximize energy intake or intake of some nutrient, or
• minimize fluctuations in energy intake, or
• maximize energy intake during certain periods . . .

• What types of food to eat?
• Where & how long to search for food?
• What type of search path to use?

For example, let's look at two studies:

• "Preferred length of Neomysis integer eaten by different sizes of 15-spined sticklebacks" (J. Exp. Mar. Biol. Ecol. 25:151-158)

• Selection of flies by Pied Wagtails (Davies 1977)

Given that foragers may want to maximize 'profit', what should they do when less than optimal prey are encountered?

• CLASSICAL MODEL OF PREY CHOICE (also in text):
• Predator - searching for 2 types of prey (1 & 2) that require search times of S1 & S2
• Prey - 2 types that yield E1 & E2 units of 'reward' (e.g., energy) AND take h1 & h2 seconds to handle
• So, their profitabilities = E1/h1 & E2/h2

• Let PREY TYPE 1 be more profitable than PREY TYPE 2:

• Depends on S1 (Search time for Type 1 prey)
• If :
• E2/h2 > E1/S1 + h1 (which would be true if S1 is large), then take both BUT if
• E2/h2 < E1/S1 + h1 (which would be true if S1 is small), then take only Type 1 prey

• Assumptions of this model:
• Prey value is measurable net energy or some other comparable single dimension
• Handling time is fixed
• Handling & searching cannot be done at the same time
• Prey are recognized instantaneously (with no errors)
• Prey are encountered sequentially & randomly
• Energetic costs of handling are the same for different prey
• Predators wish to maximize rate of energy (or some other measure of value) intake

• Predictions of model:
• Most profitable prey should never be ignored
• Less profitable prey should be ignored according to preceding equation
• Exclusion of less profitable prey should be all-or-nothing (depending on direction of inequality)
• Exclusion of less profitable prey does not depend on S2 (when Type 1 prey are sufficiently abundant using time to handle Type 2 prey is not profitable)

Test of the model (Krebs et al. 1977):

• Great Tits (Parus major)
• captive birds presented with 2 different-sized pieces of mealworms (Large = Type 1 prey & Small = Type 2 prey) on a moving belt.
• ‘Search time' for large prey (Type 1 prey) varied by varying distance between successive large prey on the moving belt (to cross the 'threshold' of the model's equations).
• Results ---> Demonstrated absence of 'all-or-nothing' response, i.e., partial preferences

Extra payoff for specializing (prey/sec) on large worms rather than taking both (From Fig. 3.6b; Krebs and Davies 1993)

• Possible reasons:
• Discrimination errors
• Runs of 'bad luck'
• Simultaneous encounters
• Need to sample the environment
• Other factors may influence behavior, such as the need to avoid predators, find mates, & so on

Exploitation of patches

Prey availability within a patch decreases as a result of the predator's foraging activity because of:

• Depletion of prey
• Evasive action by prey

As a result, to maximize the rate of gain of a resource, predators should follow the 'marginal value theorem':

If patches vary in quality, each patch should be exploited until the gain rate within the patch drops to the average for the environment:

Assumptions of the Marginal Value Theorem:

                1 - Each patch type is recognized instantaneously
                2 - Travel time between patches is known by the predator
                3 - Gain curve is smooth, continuous, & decelerating
                4 - Travel time between & searching within a patch have equal energy costs

Predictions of the Marginal Value Theorem:

                1 - If travel time & the gain curve are known, then Topt can be predicted
                2 - If there is more than one patch type in an environment, all should be reduced to the same gain rate
 

Tests of the Marginal Value Theorem:

Great Tits foraging in large aviary for pieces of mealworm hidden in sawdust-filled plastic cups on the 'branches' of artificial trees (Cowie 1977):

• Predictions:
• When average feeding rate in the aviary 'environment' was high, the birds should spend less time at each patch (plastic cup)
• If travel time between 'patches' increases, then birds should spend more time at each 'patch'
• TO TEST PREDICTION 1 ---> Six Great Tits foraged individually in aviary for 2 10-min trials each:

• TO TEST PREDICTION 2 ---> Travel time was increased by placing a top on each cup, which took about 15 sec to remove (so, 'travel time' increased from about 5 sec to about 20 sec):

Tests of the MVT often show qualitative but not quantitative support. Why?

• Other factors important besides energy (e.g., predation risk)
• 'Rich' patches = increased competition with others (= smaller loads?)
• Animals may need to 'sample' the environment

Foraging for young located in a nest or den: Central Place Foraging

Assume a diminishing energy gain with increasing load size (e.g., a bird with a beakful of insects) or increasing time in patch:

• The optimal load size (energy delivered to young/unit time) may be influenced by the time it takes to travel between a 'central place' (nest or den) & a feeding area
• Test of Central Place Foraging model using House Martins (Bryant and Turner 1982):

Cumulative food gain within patches for an average House Martin (open circles). The straight lines show maximum overall rates of food gain within bouts for foraging near the nest (Tn), at the mean observed distance from the nest (Tm), & far from the nest (Td). The Bryant and Turner (1982) model yields a different value for optimal bolus size (Bopt) for each travel time.

House Martin (Delichon urbica)

Effect on foraging behavior when a predator requires as particular nutrient?

• Nutrient quality - more important to herbivores because plants often lack essential nutrients & careful selection is required for a balanced diet
• Example = Moose diet & need for sodium & energy

- What is the optimal mixture?

• Example - Feeding patterns of Mantled Howler Monkeys (Glander 1981):

Photo source: http://www.primatesofpanama.org/howler.htm

Howlers - feed on fruits, flowers, & leaves of trees (96 species present in study area)

Conclusions:

• Howlers obtain most food from relatively rare trees
• Howlers maximize intake of protein, water, & most amino acids
• Howlers minimize intake of crude fiber & plant secondary compounds (e.g., alkaloids & tannins)

Stochastic foraging models

Assume that travel times & patch quality vary in an unpredictable way. Possible consequences:

• Animals might respond to the risk of doing badly or well in a particular patch or with a particular prey
• Animals might have a strategy for assessing patch quality & acquiring information by sampling

• Yellow-eyed Juncos (Junco phaeonotus; Caraco et al. 1980) - offered a choice between 2 feeding sites in an aviary (with the other site no longer available after a choice is made):
• Site 1 = constant reward (e.g., 4 mealworms)
• Site 2 = unpredictable reward (e.g., 0 or 8 mealworms but a mean of 4 mealworms)
• AFTER 1 HOUR STARVATION, juncos preferred the predictable site BUT AFTER 4 HOURS STARVATION, juncos preferred the unpredictable site.

• After 1 hour of deprivation:
• Constant site - provided enough food to meet energy requirements
• Variable site - 50% chance of providing more than enough & 50% chance of not providing enough
• After 4 hours of deprivation:
• Constant site - NO chance of providing enough food
• Variable site - 50% chance of providing enough food

Effect of 'information' on foraging behavior

• A forager acquiring information about a patch should, on average, stay longer than predicted by the marginal value theorem because extra time may reveal that the patch is better than the 'current' estimate. In other words, it may pay to 'sacrifice' the maximum intake rate to gain extra information.
• Do foragers acquire & use 'information'?

• Study in small woodlot in southeastern Michigan
• Patches
• 37-cm length of sapling ash tree, 2.5-3 cm in diameter
• 24 holes drilled (0.5 cm deep) & arranged into 6 groups of 4 holes each. Groups were placed at 4-cm intervals & covered with a strip of masking tape
• may or may not be a single sunflower seed in any given hole of a patch
• 60 'patches' (about 4 m apart) in environment
• Downy Woodpeckers - given experience in patch use by providing them with 60 totally full patches (24 seeds in 24 holes) for 14 days
• Downies - then exposed to 3 'environments':
• 'Full' = 36 patches empty & 24 patches full
• 'Half-full' = 36 patches empty & 24 patches half-full (12 seeds in 24 holes)
• 'Quarter-full' = 30 patches empty & 30 patches quarter-full (6 seeds in 24 holes)
• Results:

Day 1 ---> Downies expected only totally full patches & opened almost all holes in empty patches (although no seeds were found)
Days 2 - 8 ---> Downies learned that some patches had seeds & some did not
Days 9 - 11 ---> Downies opened 1.7 holes/empty patch
Day 12 ---> 1st day of half-full environment
Day 13 ---> Downies opened 5 holes/empty patch
Day 23 ---> 1st day of quarter-full environment
Days 29 - 31 ---> Downies opened 6.3 holes/empty patch

CONCLUSIONS:

• Increased uncertainty that patch was empty or had seeds led to increased sampling by woodpeckers before giving a patch up as empty
• In patches with seeds, the woodpeckers' strategy was to open every hole (efficient but suboptimal . . . why??)
• Downies distinguished between patches with seeds & empty patches, & gathered enough information to exploit different environments in a reasonably efficient manner
• Downies responded rather quickly to environmental changes

Foraging & conflicting demands

Behavior of foraging animals may be influenced by need to watch for predators, search for mates, defend territories, defend nest sites, and so on (e.g., Martindale 1982):

• While adult Gila Woodpeckers forage, nestlings are vulnerable to intruders & predators (e.g., other Gila Woodpeckers or Common Flickers attempting to take over the nest site). How does the need for nest defense alter foraging behavior?

Gila Woodpecker

Conclusions:

• Increased risk of predation ---> Defending forager should move closer to the nest, leave patches sooner, & deliver smaller loads
• Males behaved as expected but females didn't

Influence of a predator on the optimal foraging behaviour of sticklebacks (Milinski and Heller 1978):

Search Paths

• Flocks of finches generally move in a way that minimizes path crossing (to reduce chances of returning to areas that have already been 'depleted') (Cody 1971)
• Animals may increase amount of 'turning' in their paths following encounters with prey (possible adaptation for exploiting a patchily-distributed food resource) (Pyke 1978).
• Animals may avoid patches and areas within patches already visited (Zach and Falls 1978):
• Ovenbirds exhibit increasingly tortuous search paths & reduced speed in areas with greater prey densities.

Age-specific foraging behavior (e.g., Wunderle 1991)

• Foraging sites - many (but not all) studies have revealed age- related differences in habitat or patch use.
• Possible explanations:
• Dominant adults displace juveniles from certain foraging sites
• Inability of juveniles to accurately evaluate patch differences
• Diet differences arise from lack of juvenile proficiency for searching, capturing, or handling prey
• Different nutritional requirements
• Search methods & patterns - quantification of searching methods is difficult & few field studies have compared adults & juveniles
• Food recognition & selection - How do juveniles recognize prey?:
• Juveniles may learn from parents
• Juveniles may learn from personal experience
• Juvenile learning is mostly independent of personal experience & is primarily genetically based

• Juveniles are less proficient than adults
• Juveniles are less skilled at some other aspect of foraging (e.g., capturing or handling) & compensate by selecting a different diet
• Juveniles have different nutrient requirements
• Adult dominance influences juvenile diet selection by preventing juveniles from selecting the most profitable prey types

Food handling time & technique:

• Handling time is the time required for a forager to eat a captured food item, and can represent a substantial portion of foraging time in some species.
• Juveniles in a variety of species & with a variety of diet types (piscivores, insectivores, mollusc eaters, scavengers, carnivores, & seed eaters) have been found to be less adept at handling food items
• lack of food handling proficiency can have major implications for survival because it can increase the likelihood that food items will be stolen & also increase the time & energy expended in acquiring food
• improvement in juvenile handling time & ability can largely be attributed to LEARNING & to MATURATION.

Literature cited:

Belovsky, G.E. 1978. Diet optimization in a generalist herbivore: the moose. Theor. Pop. Biol. 14:105-134.

Bryant, D.M. and A.K. Turner. 1982. Central place foraging by swallows: the question of load size. Anim. Behav. 30:845-856.

Caraco, T., S. Martindale, and T.S. Whitham. 1980. An empirical demonstration of risk-sensitive foraging preferences. Anim. Behav. 28:820-830.

Cody, M.L. 1971. Finch flocks in the Mohave Desert. Theor. Pop. Biol. 2:142-158.

Cowie, R.J. 1977. Optimal foraging in Great Tits, Parus major. Nature 268:137-139.

Davies, N. B. 1977. Prey selection and social behaviour in wagtails (Aves: Motacillidae). Journal of Animal Ecology 46:37-57.

Glander, K.E. 1981. Feeding patterns in mantled howling monkeys. Pp. 231-257 in A.C. Kamil and T.D. Sargent, ed., Foraging behavior: ecological, ethological and psychological approaches. Garland STPM Press, New York.

Krebs, J.R. and N.B. Davies. 1993. An introduction to behavioural ecology, third ed. Blackwell Scientific Publications, London.

Krebs, J. R., J. T. Erichsen, M. I. Webber & E. L. Charnov. 1977. Optimal prey selection in the great tit (Parus major). Anim. Behav. 25: 30-38.

Martindale, S. 1982. Nest defense and central place foraging: a model and experiment. Behav. Ecol. Sociobiol. 10:85-89.

Milinski, M. & R. Heller. 1978. Influence of a predator on the optimal foraging behaviour of sticklebacks. Nature 275:642-644.

Pyke, G.H. 1978. Are animals efficient harvesters? Anim. Behav. 26:241-250.

Wunderlee, J. M., Jr. 1991. Age-specific foraging proficiency in birds. Curr. Ornithol. 8: 273-324.

Zach, R. & J. B. Falls. 1978. Prey selection by captive ovenbirds (Aves: Parulidae). J. Anim. Ecol. 47: 929-943.

More lecture notes:

Living in Groups

Useful links:

Cyberbranchaea - Optimal Foraging Simulation

Food: Optimal Foraging Models

Game Theory

Introduction: Background to Optimal Foraging

Mating Walnut Flies

Optimal Foraging

Optimally Foraging Hummers

Optimal foraging experiments on captive Steller sea lions: a feasibility study

Optimality theory; Foraging Strategies

Patch use in cranes: a field test of optimal foraging predictions

Back to Behavioral Ecology syllabus