A Practical Technique for Measuring the Behavior of Foraging Animals

g k sTHow A PractIcal Technique for )D Do Measuring the Behavior of It _ . It Foraging hnlmalS

RosemaryJ. Smith Joel S. Brown

Animal behavior is well suited for havioral questions that can be readily ness (survivaland reproduction).If so, illustrating ecological and evolution- addressed gives students the opportu- an animal should leave a patch when ary principles. For ecology projects or nity to suggest their own hypotheses its benefits of continued feeding in the labs, animal behavior has a number of and experiments.The projectsempha- patch no longer exceed its cost of feed-

advantages:It is inherently interesting size the methodology of a scientist ing in the patch. The formal frame- Downloaded from http://online.ucpress.edu/abt/article-pdf/53/4/236/45243/4449276.pdf by guest on 01 October 2021 to most students, it can be observed, it and, we hope, the excitement that work behind the assertion in the pre- is flexible and it can change quickly. accompanies creative thinking and vious sentence is called Optimal Unfortunately, meaningful observa- novel results. Foraging Theory (see Stephens & tions of behavior tend to be time- Krebs 1986). consuming and difficultto analyze. To We begin by elaborating a rule for overcome this handicap, we introduce Rationale when an animal should leave a patch an indirect procedure that uses the and then discuss how this rule can be foraging behavior of animals at exper- "Talking" to animals requires a common language, and feeding be- used to reveal aspects of that animal's imental food patches to address ques- ecology. An example from our own tions in animal behavior. The data are havior can provide just such a language. Mixing food into a substrate work illustratesthis rule. We provided the food left behind by the animals. kangaroo rats living in the Sonoran Such creates a food patch and provides a data are quantitative and easily Desert of Arizona with shallow alumi- analyzed using a variety of technique for "asking" foragers how descriptive num pans (45 x 45 x 2.5 cm) filled with or inferential statistics. The experi- they perceive their environment. The a known amount of millet seed (3 g) mental procedure encourages stu- food patches are like a survey distrib- dents to ask questions relevant to how uted to the animalsbeing investigated. that has been mixed into 3 1 of sifted environmentalfactors such as climate, The animals fill out the survey by dirt. Kangaroorats foraged enthusias- vegetation structure and predation digging for and harvesting food from tically in these food patches. As more risk influence animals'foraging behav- the tray's substrate and then sign and more seeds are eaten, the large ior. When several species are included these trays with footprints, body amount of dirt in the patch makes it within the study, interspecific differ- marks and other telltale disturbances increasingly difficult for the kangaroo ences in behavior provide an easy and of the substrate. The amount of food rats to find the seeds that remain. relevant introduction to questions of left in the patch contains the answer to Therefore, the benefit of remaining in niche separation and species coexis- the survey. the patch declines. At some density of tence. The following approach to feeding seeds the cost of looking for the next Because it uses food left by animals behavior represents evolutionaryecol- seed exceeds the benefit derived from in feeding patches, the technique does ogy. From an ecological perspective, harvesting and consuming that seed. not require hours of observation, han- two universal properties of life in- At this criticalseed density the kanga- dling of animals or expensive equip- clude: roo rat should leave the patch. If it ment. Because feeding is central to all 1. Births and deaths continues to forage past this density, it animals regardless of environment, 2. The need for energy and nutri- forages at a loss (costs exceed bene- studies can be conducted on school ents to maintainhomeostasis and fits). If it quits early, it forfeits the food campuses using urban birds (spar- life functions that it could have profitablygained. rows, doves, pigeons, starlings) or An animal should leave a food patch small mammals (squirrels, mice and From an evolutionary perspective, when its benefits equal its costs (see rats). The cost/benefit theory behind these two properties of life encourage Brown 1988 for a formal treatment of the technique is intuitive and accessi- animals to have feeding behaviorsthat the theory). To apply this foraging ble to students. The breadth of be- allow them to acquire food in an effi- theory, the animal must experience a cient manner. declining rate of return from spending Feeding animals make decisions time in the food patch, and the animal about where to feed (habitatselection, must experience both benefits and Rosemary J. Smith teaches in the de- MacArthur & Pianka 1966), what to costs from exploiting the patch. The partment of ecology and evolutionary feed on (diet choice, Pulliam1974) and benefit to biology at the Universityof Arizona,Tuc- the forager is its rate of son, AZ85721. Joel S. Brownteaches in when to quit an area and move to harvest of food times (H) considered the department of biological sciences another location (patch use, Charnov in terms of energy or nutrient intake. at the Universityof Illinois,Box 4348, 1976). We assume that natural selec- The costs of spending time in a food Chicago, IL60680. tion has favored those animals whose patch include energetic costs (E) of feeding decisions maximize their fit- searchingfor and handling food items,

236 THEAMERICAN BIOLOGY TEACHER, VOLUME 53, NO. 4, APRIL1991 walk. And finally, if you knew there VARYINGFORAGING COSTS was another full jar on the shelf, or [ENERGETIC,MISSED OPPORTUNITY OR PREDATIONI that you were missing out on a great TV show (high missed opportunity costs), again you would leave more peanut butter in the jar. m The amount of peanut butter left in the jar, the GUD, is a clearreflection of D z 4- your perceptionof these three types of costs. Refer back to the equation and note that if any two costs are held constant, any differencesin GUDs be- o 3 tween experimentaltreatments will indicate the effect of the variationin the third cost (see Figure 1 for summary). 2

z Methods

Using GUDs to Study Feeding Downloaded from http://online.ucpress.edu/abt/article-pdf/53/4/236/45243/4449276.pdf by guest on 01 October 2021 o 1 Costs & Opportunities The model predicts that two identi- > Low HIGH cal feeding patches placed side by side within the same habitat should have Figure 1. An illustration of how giving up density of peanut butter might vary the same GUD. This is because both with experimental conditions. The LOW giving up density relative to HIGH trays have the same substrate and indicates a lower energetic, missed opportunity or predation cost of extracting food items (controls for H) are subject peanut butter from a jar. to the same microclimaticconditions (controlsfor E), are equally exposed to potential dangers (controls for P), are equally situated for alternative activities (controls for M) and are available A Useful Analogy of the Rule for to the same animals (differentanimals risk of predation (P) and the missed in their of the Leaving Patches may vary perceptions opportunity cost (M) of not engaging food, energetic costs of foraging, pre- in alternativefitness-enhancing activi- We have found that the following dation risk and opportunities pro- ties such as mating, defending a terri- human example of the patch-leaving vided by alternative activities). The tory or-exploiting a richer food patch. rule is useful because it provides stu- above prediction allows for controlled The patch-leaving rule can then be dents with a mental image of the way manipulations of the model's compo- written as: GUDs change when the cost components (H, E, P and M). The effect of nents are manipulated. Imagine an any one of the components on the H = E + P + M almost empty peanut butterjar (this is GUD can be tested by holding the the resource patch). As you remove other components constant. In what This rule provides the model for peanut butter from the jar it becomes follows it is important to remember investigating foraging behavior. An more and more difficultto get the next that higher GUDs mean more food is spoonful out (this demonstrates a de- left in the patch, hence the animals animal should leave a food patch clining rate of return). According to either perceived higher costs or lower when the harvest rate from the patch the rule, you will quit removing pea- benefits from harvesting the patch. no longer exceeds the sum of the en- nut butter when the benefit (the har- Consider an investigation of factors ergetic, predation and missed oppor- vest rate) just equals the sum of the that may influence harvest rates. Plac- tunity costs of foraging. In reality, it is costs (energetic,predation and missed ing food patches side by side within difficult to measure H and even more opportunity). The amount of peanut the same habitat can control for ener- difficult to measure H, E, P and M in butter left in the jar will be your GUD. getic costs, predation risk and missed terms of their fitness consequences, Now, what happens when one of opportunity costs. By varying food which is their true common currency. the costs is varied while the others are types, food size or substrate, it is pos- Fortunately, the density of food left held constant? When it is cold and sible to test for their effects on H. behind in a patch when an animal more energy is required to scrape out Larger amounts of substrate or more quits foraging is a good surrogate for the last bit of peanut butter (higher difficult substrates should increase H. We refer to this quitting density of energetic cost), then you will likely GUDs. GUDs should be lower on food as the Giving Up Density or leave more peanut butter in the jar foods that are either preferredor eas- GUD. All else equal, a higher GUD (have a higher GUD) than when it is ier to find and handle. For instance, corresponds to a higher H. For our warm. Likewise, if you were removing GUDs should be lower on conspicu- kangaroo rat work, the weight of mil- the peanut butter from a jar while in ous food items than on cryptic ones. let seeds left behind in patches follow- the middle of a busy street (high pre- Such effects can be used to great ad- ing a night of foraging (kangaroorats dation cost), again you would proba- vantage. The importance of size or are nocturnal)measured the kangaroo bly leave more peanut butter in the jar nutrients can be tested by seeing how rat's GUD. than if you were safely on the side- GUDs vary across food items with

FORAGINGANIMALS 237 different sizes or nutrient contents. substrate, food or place, manipula- may "starve" other species out of the The importance of specific sensory tions of M must be made across ani- community. Coexistence is facilitated modalities to the animal can be tested mals or across time. Manipulationsof if each species has a food (or habitat) by comparingGUDs across food items the backgroundabundance of alterna- that it can profitably harvest to the that vary in visual or olfactory cues tive foods is perhaps the most direct lowest abundance. The GUD of a spe- (foods can be dyed to influence vision way to manipulate missed opportu- cies on a particularfood or within a or dipped in vegetable oils to influence nity costs. As foods become naturally particular habitat provides this mea- olfaction). or artificially more abundant in the sure of competitive ability. The com- Consider an investigation of factors animal's environment its GUD should petitor that is superior at exploiting a that may influence energetic costs. increase. By scattering sunflower patch is the forager with the lowest Placing trays that contain the same seeds onto the home ranges of se- GUD. It can reduce the resources to a substrate and foods near each other lected fox squirrels we were able to level that cannot be profitably ex- can controlfor harvest rates, predation increase their GUDs relativeto unsup- ploited by any other species. risk and missed opportunity costs. By plemented home ranges. GUDs, by measuringrelative compet- varying the microclimateamong trays, In summary, the model allows the itive abilities, can determine whether it is often possible to test for the effects forager to reveal its preferences and patterns of food and habitat use pro- of factorssuch as wind, solar radiation assessments of the environment. mote coexistence.Within a habitat,co- and temperatureon GUDs. The exper- Thus, if a squirrelleaves more nuts in existenceis facilitatedif each species has imenter can either take advantage of a seed tray from the protection of a a food on which it has the lowest GUD. naturalclimatic variation that occurs in large tree, it may indicate an increased Similarly,when there are two habitats, differenthabitats or on differentdays, predation risk. Or, if house sparrows species coexistenceis facilitatedif each Downloaded from http://online.ucpress.edu/abt/article-pdf/53/4/236/45243/4449276.pdf by guest on 01 October 2021 or the experimenter can use equip- have lower GUDs on warm days than species has a habitatin which it has the ment such as fans, artificial lighting on cold, this indicates lower energetic lowest GUD (Figure2). and shading, or heating pads and cold costs. If pigeons have higher GUDs The senior author has done research packs to perform manipulations of close to a snack bar, this may indicate with two ground squirrel species that wind, radiation and temperature. that they have a higher missed oppor- illustratescoexistence via habitatselec- An investigation into factors influ- tunity cost when other food sources tion. Both species of squirrel feed in encing predation risk can be particu- are readily available. Students can in- open meadows, but the golden-man- larly rewarding. Even animals that vestigate any number of species-spe- tled ground squirrel (Spermophiluslat- experience few predatorswill respond cific and habitat-specificdifferences in eralis)has the lower GUD far from the strongly to manipulationsof perceived foraging costs and benefits by holding meadow's edge, while the least chip- or actual predation risk. Because of three of the model's components con- munk (Tamiasminimus) has the lower predation's costliness and irreversibil- stant among food patches. GUD closer to the meadow's edge (Fig- ity to the victim, a little predation risk ure 3). Experimentalmanipulations of can become magnified into large be- coverand predatoractivity revealed that havioral changes. (Witness the large Comparisons Across Species: differencesin perceived predationrisk decline in tourists to countries that Using GUDs to Understand generated this pattern of habitat use. experience even minor civil distur- The coexistence Species Coexistence of these two species is bances.) Many animals such as small promoted by a tradeoffbetween anti- mammals and birds seek refuge from The competitive exclusion princi- predatortactics and the ability to effi- predators by concealment in vegeta- ple-two species cannot occupy the ciently exploit resources. The ground tion. Hence, predation risk is often same niche at the same time and in the squirrelis superior at avoiding preda- greater away from cover than near same place (Hardin 1960)-has chal- tors in the more open habitatfar from cover. This can easily be exploited by lenged ecologists to provide explana- cover, but inferiorto the chipmunk at placing one feeding patch near a tree, tions for the coexistenceof species that exploiting resources in the absence of shrub, hedgerow or den and placing have similardiets and habits:How do predation risk. Similar tradeoffs have the other in the open just a few meters ecologically similar species coexist in been shown to promote coexistencein away. It is often simple to alter an one area? (Diamond & Case 1986; desert rodents (Brownet al. 1988). animal's perception of predatory risk Ricklefs1990). A widely accepted view The above study with squirrels (e.g. scarecrows) by varying visual considers how evolutionary tradeoffs shows how a species' perception of (facsimiles of the actual predator), au- in competitive abilities among differ- foraging costs and benefits influences ditory (tape recordings of the preda- ent species promote coexistence (Kot- the use of food patches, which, in tor's vocalizations) or olfactory (fur or ler & Brown 1988). According to this turn, promotes coexistence. In partic- excrement from the predator) cues. view, a species cannot evolutionarily ular, predator-mediatedhabitat selec- (Ungulates at zoos are known to improve its ability to exploit a food or tion illustrates a profound effect of spend less time feeding and more time habitatwithout sacrificingits ability to predators on community organization vigilant when their cages are near to exploit some other food or habitat. In that goes beyond the actual captureof those of their felid or canid predators). this way, species that are close com- competing prey species by predators In all cases, increased perceptions of petitors are able to coexist by special- (usually taught as the "keystone pred- predation risk should result in in- izing on differentfoods or habitats. ator effect"). As a result, students can creased GUDs. A comparison of GUDs across spe- use GUDs in feeding patches to study Factorsthat influence missed oppor- cies can provide insights into the co- importanteffects of predatorson their tunity costs are often harderto manip- existence of competitor species. One prey without having to observe and ulate in a controlled fashion, but are measure of competitivesuperiority is a measure predation events. In fact, ob- no less accessible to experimentation. species' ability to profitablyharvest a servational studies that focus only on Because an animal's missed opportu- resource to a low abundance (Tilman the actualcapture of prey by predators nity cost is a property of its environ- 1982). Such a species, by maintaining probably underestimate the impact of ment at large and not of a specific resource abundances at low levels, predators on their prey.

238 THEAMERICAN BIOLOGY TEACHER, VOLUME 53, NO. 4, APRIL1991 COMPETITIVEEXCLUSION COEXISTENCE Design & Implementation of Experiments Placement,number and replicatesof food trays depend on the hypotheses to be tested. This is an excellent op- portunityto involve students in experimental design. Paired treatments (such as one tray in the open and another near cover) are the simplest to analyze. Begin each trial by evenly GUDIN HABITAT 2 GUDIN HABITAT 2| mixing a measured amount of the food item into each tray. Allow the foragers Figure2. Examplesof how two species' GUDs (A and B) in two habitats(1 and 2) to move freely between the trays. The may either inhibit or promote their coexistence. In the first figure, species B has investigator does not have to observe the competitive advantage in both habitatsand will tend to competitivelyexclude the trays; in fact, it is usually best to the other species. In the second figure each species has a habitat in which it has leave the area entirely, since the pres- the competitive advantage: Species B is superior in habitat 1 and species A is ence of an observer acts to heighten superiorin habitat2. This arrangementof GUDs will promote species coexistence perceived predation risk. The bout is in an environment that contains both habitats. over when foraging ceases (end of day, night or other activity period). Downloaded from http://online.ucpress.edu/abt/article-pdf/53/4/236/45243/4449276.pdf by guest on 01 October 2021 When collecting data, note any footprints in the sand or dirt, as these indicate when species left the tray last (this allows for proper attribution of Materials & Equipment particle size that yields measurable the GUDs if comparisons between The technique of measuring ani- GUDs. We have found that millet seed species are to be made). Remove the mals' GUDs need require only mini- is good for seed-eating rodents and unharvested food items from the mal expenses and can be performedin birds. We have also used peanuts, trays, usually by sifting them out of most outdoor areas. The first steps are sunflower seeds, mealworms and var- the substrate. In many cases, further to select study organisms and assem- ious types of commercialanimal chow. sorting by hand will be necessary to ble appropriatefood trays. Depending Some preliminary work must be on the animal, experiments should be done to establish the amount of sub- conducted overnight or during the strate and food necessary to attract Table 1. Attributes of trays, day. Good study animals are those foragers and to insure a declining for- substrate and food items that that are abundant and eat stationary aging rate (they must leave some food should be considered when prey. Our suggestions for suburban, items or you will have nothing to designing experimental food diurnal animals include: sparrows, pi- measure). The design of the trays patches. geons, other seed-eating or fruit-eat- might be part of a project that tests ing birds and squirrels. Good subur- student ingenuity (see Table 1 for Trays ban and nocturnal animals include: guidelines on choosing materials). 1. Deep enough to prevent cats, opossums, mice and raccoons. We have successfully used aluminum excessive spillage of the Native animals in their natural habi- pans (45 x 45 x 2.5 cm) filled with substrateby foraging animals tats (seed-eating birds, rodents, 3-10 g of millet seed mixed thoroughly 2. Sufficientlydurable to skunks, foxes, coyotes) also may be into 2-3 1 of dirt or sand as feeding withstand weather conditions ideal for study. We have even seen patches. and animal use such experiments with Ibex and por- Retrieving and measuring the re- cupines. maining food within a patch usually Substrate Feeding patches consist of a tray requiresa sieve of an appropriatesize 1. Similarityto the animal's filled with a food mixed into a sub- to separate food particles from sub- natural foraging habits strate. Feeding trays can be baking strate material (we use a screen 2. Sufficientvolume to insure that pans, cardboard beer or soft-drink mounted on a wooden frame),a tub or the animal's harvest rate flats (free at most grocery or liquor large bag to catch sifted substrateand increases with the abundance stores) and buckets, or feeding trays small plastic bags to hold the remain- of food item in the patch can be constructed from materials ing food items from each patch. (We 3. Sufficientvolume so that the such as sheet aluminum. The sub- place a data tag with information on animal's GUD is greater than strate within the trays can be wood date, traylocation, treatmentand foot- zero fibers, straw, gravel and artificialturf. prints into each bag as it is collected). 4. Easily separated from As a substrate we favor sand or sifted Finally, a table is needed on which to unharvested food items by dirt because of the ease of recognizing do final food sorting (often the remain- sieving or sorting the In animal's footprints. sand it is ing food items need to be separated Food Items often possible to distinguish among from debris that still remainsfollowing 1. the Expense spoor of animals such as large and sifting) and a balance or volumetric 2. small mammals and birds. The appro- to Preferencesof study animal cylinder measure the GUD (the 3. Uniform size priate food depends on your choice of amount of food left behind). To mini- 4. Resistance to animal. The food should be attractive mize recording errors, we write the degradationand fragmentationunder the to the animal, easily available from GUDs on the back of each tag before experimentalconditions grocery, pet or feed stores and of a transferringdata to data sheets.

FORAGINGANIMALS 239 such dramatic results that students THEEFFECT OF DISTANCEFROM COVER ON GUD'S may discuss them confidently without establishing statistical significance. Paired data lend themselves to some '2 2.500 P<.05 LU of the simplest statistical tests. Such LU E=1 7 METERS data arise when trays are placed in twos and the trays in a pair differwith 20v - 21 METERS respect to some experimental treatment such as substrate,habitat or food type. The effect of treatment can be determined either with a paired t-test or sign test. When data are not paired or when there are a number of treatments, standard parametricstatistics such as z analysis of variance (ANOVA) may be 0 applicable. For instance, trays might o 2.500- be paired with respect to food type with several pairs of trays distributed at different stations, and the experi- 0.000 ment might be repeated over several Downloaded from http://online.ucpress.edu/abt/article-pdf/53/4/236/45243/4449276.pdf by guest on 01 October 2021 CD 1.5001 N\S CHIPMUNK GROUNDSQUIRREL days. In this case, the data could be analyzed as a paired t-test or, more COMPETITIVECOEXISTENCE appropriately,as a three-way random- ized block ANOVA where the three SeLU 1.000: . factorsare food type, station and day. t 2.500 Such a test will reveal the significant 0-0 CHIPMUNK effects of each factor on GUD as well o 0.500 \...... ; as the three interactioneffects of food- 2.000 - UP ( ...... GROUND type by station, food-type by day and SQUIRREL day by station. When using parametric LU statistics we have found that a loga- V') 1.500- rithmic transformation normally dis- LL 0 tributesthe data. Useful non-paramet- (I) ric tests for comparing treatment 1.000 means include the Wilcoxon's signed- ranks test, Friedman'smethod for ran- domized blocks or Kruskal-Wallisnon- parametricANOVA. 0.500- us,z Data from food patches may include the presence or absence of feeding or I some other type of frequencydata. For Di 0.000 such data we have used Chi-square 0.000 0.250 0.500 0.75 0 1.000 z goodness of fit tests or G-tests of heterogeneity (see Sokal & Rohlf 1981 for CD UP DENSITY(GRAMS OF SEED)AT 7 METERS the application of the aforementioned ~~GIVING statisticalprocedures). Figure 3. GUDs of chipmunk (Tamiasminimus) and ground squirrel(Spermophilus In any experiment there will always lateralis)from montane meadows in Colorado(Smith unpublished data). The two be residual variation in GUD among axes represent different distances into the meadow from the forest's edge: 7 replicatetrays. Students should be en- meters from cover and 21 meters from cover. The habitat heterogeneity of couraged to hypothesize about possi- distance from cover promotes species coexistence. The chipmunk has the com- ble sources of this variation, for exam- petitive advantage near cover (7 meters) and the ground squirrel has the ple: Was it cloudy one day but not the advantage away from cover (21 meters). next? Was there the same amount of disturbance on all days? At all trays? Can differences be attributed to the size or sex of the foragers?An under- standing of the possible sources of variation can lead to the design of remove the remaining debris. Weigh tical tests that range from the simple to additionalexperiments, as well as pro- or measure the volume of the sorted the complex and from descriptive to vide new variables for consideration. food items to obtain that tray's GUD. inferential. Descriptive statistics such This is, by definition, the scientific as the mean or mode of the data can be method and it can lead students to Statistical Analyses & presented graphically,i.e. bar graphs think of science as a process instead of mean a a collection of facts. Presentation of Results showing GUDs as function of specific experimentaltreatments. Such To broaden an experiment'scontext, Depending on the experimentalde- descriptive statisticsmay conclude the we suggest discussing experimental sign, GUD data are accessible to statis- analysis, as some experimentsprovide results in terms of their relevance for

240 THEAMERICAN BIOLOGY TEACHER, VOLUME 53, NO. 4, APRIL1991 FORAGINGBEHAVIOR OF POCKETMICE trays were placed out at night and the house mice in the area foraged in the trays. The mice in this study had a 8- higher GUD in cat trays than in non- cat trays. 7- Other possibilities include: Measure LU ~ ~ ~ ~ ~ ~ ~ ~ ~ ~~ -1BUSH GUDs before and after a scare by a predator (perhaps the experimenters) i- 6- o OPEN to examine recovery times; compare 6 responses among species or among 5 individuals of differentage or sex.

(1) 4- Studies of HarvestRates & z Metabolic Costs o 3- Does the color of the food item affect its harvest by a forager?Does the size 2- of the food item affect its harvest? z How does substratetype affectharvest rates? Do species of different sizes show the same preferences?How does Downloaded from http://online.ucpress.edu/abt/article-pdf/53/4/236/45243/4449276.pdf by guest on 01 October 2021 the temperatureof the patch (e.g. the 0- weather) affect GUDs? What is the NO OWLS WITHOWLS effect of hunger level on an animal's use of a food patch? Figure4. The effect of owls on the foragingbehavior of the Arizonapocket mouse (Perognathusamplus). Experiments were conducted in a large aviary that was tailored to simulate a desert environment with a community of pocket mice. Studies of Missed Opportunilty Experimentalnights varied in terms of whether barn owls were present or absent Costs from the aviary. In such a desert, there are two microhabitats:under the canopy Do GUDs vary between breeding of shrubs (BUSH)or in the open space between shrubs (OPEN). Shrub canopies and non-breeding individuals; be- provide protection from aerial predators such as owls. In response, the pocket tween those that are or are not territo- mice always had a lower GUD in the bush microhabitatthan in the open. In rial; between males, females or juve- response to the presence of owls, the pocket mice demonstrated their increased niles? How are GUDs affected by the perception of risk by increasing their GUDs in both microhabitats(Brown et al. addition of alternativefeeding oppor- 1988). tunities (for example, close to or far away from an area where students have lunch)?

questions of species diversity and con- MeasuringCompetition Studies of Predation Risk servation. For example, if the stu- The identity of the last species in a dents' results indicate a role for envi- Predation risk can be measured on patch can either be assumed from the ronmentalheterogeneity in promoting either a habitat or a patch scale. The time of activity (e.g. nocturnal vs. di- species coexistence, then the students easiest projectsare those that examine urnal) or discerned through the foot- are only a step away from realizing the effect of habitat structure on per- prints on the surface of the dirt or that the elimination of habitat types ceived predation risk. Trays can be sand. The GUD of the tray should be might foretell species extinction. Stu- placed in pairs, one in an open area, assigned to the last species that used dents can also discuss the significance another near some type of cover, such the tray. Comparisons between the of such measurable phenomena as as a shrub or tree, parkbench, etc. We GUDs of different foragers or species diet specialization, seasonal changes have used this design with birds, des- in any of the above experiments will in food values or competitive abilities ert rodents and montane ground indicate which species is the superior (why are owls predominantly out squirrels. Different GUDs found be- competitor under the conditions in a at night while hawks are predomi- tween habitattypes indicate greateror given patch. Recall that the forager nantly out by day?) and why a food's lesser predationrisk. Manipulativeex- with the lowest GUD has an advan- appeal to an animal might be habitat- periments can follow, e.g. adding tage because it can continue to use a specific (what looks like a lot of forage cover such as a large stick or rock pile patch after its competitors have quit. to a game manager might not to a to the open habitat or increasing pre- Coexistence may be promoted when deer). dation risk by disturbing the foraging each species has a distinct habitat or animals or using a facsimile of the condition in which it is the superior predator. Figure 4 gives results for competitor (refer to Figures 2 and 3). Some Suggested Projects how owl predation influences the foraging behavior of a desert rodent, the Special Cautions & We have divided projects by area of Arizona pocket mouse: Perognathus ecological interest, although a well de- amplus(Brown et al. 1988). Considerations signed experiment and more ad- On a patch scale, we have mixed Although we have used foraging vanced multifactorialstatistics can be seeds into sifted cat litter and sand. trays successfully in many projects, used to combine different questions The treatments were litter used by a there are some conditions in which into a single study. cat and litter fresh from the bag. Seed they do not work. The first is rain. If

FORAGINGANIMALS 241 you are using sand or dirt in your isolated by trying different substrates and benefits and the theory's implica- trays, it must stay dry. It is virtually and/or food types. For example, we tions for animal behavior encourage impossible to sift mud. Alternative have kept the food in squirrel trays maximum student participation in for- substrates include gravel or wood fi- away from birds by burying it in sand mulating testable hypotheses and exe- bers (the type used for packing in the or covering it with wood fibers. cuting field experiments. In the pro- Southwest). Unfortunately, these do A relatedproblem is that of multiple cess of conducting field experiments not allow for species attribution,since individuals from the same species for- students acquire knowledge of their no footprints are left. aging in a single tray. This results in a study animals' habitat preferences, Finding an appropriate food type bias of the data towards the most food preferences, patch use behaviors may require numerous trials. If a food efficient individual, that is, the one and relative competitive abilities. This is perceived as very valuable or very with the lowest GUD. In interspecific knowledge provides insights into the easy to find then the GUD may be comparisons this may strengthen the role of predators and habitat heteroge- zero. If the food has little value or is conclusions, because in effect you are neity in species coexistence. All of this impossible to detect then the animals comparing what the "best" of each knowledge has relevance for the con- may do no more than dabble in the species can do. To increase the inde- servation, maintenance and restora- food patches. However, the enthusi- pendence of data points, place trays tion of biodiversity. asm with which particularanimals ap- far enough apart to attract different proach food patches provides insights individuals or sets of individuals. into their foraging preferences and Acknowledgments

their abilities to negotiate particular Downloaded from http://online.ucpress.edu/abt/article-pdf/53/4/236/45243/4449276.pdf by guest on 01 October 2021 foraging substrates. Conclusions We thank J. Bronsteinand D. Davidson Another problem arises when ani- for suggesting that we undertakethis proj- mals are not given enough time to An animal should continue harvest- ect. The manuscriptand ideas herein were make an assessment of the patches. ing the food from a patch until the much improved by comments from B. Danielson, M. Kaspari,D. Papaj,J. Powle- We suggest that animals be allowed to benefits from its harvest rate no longer sland and two anonymous reviewers. experience the trays and food items at exceed its combined metabolic,preda- least a few days before the experi- tion and missed opportunitycosts. As ments begin. Prebaiting, the place- a result, the amount of food remaining ment of additional food items around in a patch following exploitationby an References the trays, may encourage animals to animal (its giving up density, GUD) forage in them sooner. can reveal its perceptionof its environ- Begon, M. & Mortimer,M. (1981). Popula- Other problems that might occur ment. The techniqueof using GUDs to tion ecology:A unifiedstudy of animalsand involve multiple species or individuals measure patch use allows students to plants.Oxford: Blackwell Scientific Publi- foraging in a tray. For example, seed test hypotheses regarding how food, cations. trays placed out in the evening will be substrate, climate, predation risk and Brown, J.S. (1988). Patch use as an indica- used by nocturnalmice, but if are habitatinfluence animalbehavior. The tor of habitatpreference, predation risk, they and competition. BehavioralEcology and not collected in the morning, birds technique is general and can be ap- Sociobiology,22, 37-47. may also feed in them. To prevent plied across a varietyof field situations Brown J.S., Kotler, B.P., Smith, R.J. & this, the data must be collected before (from backyards to mountain mead- Wirtz, W.O. II. (1988).The effects of owl the birds begin feeding. When dif- ows), food types (millet seeds to cat predation on the foraging behavior of ferent organisms attempt to forage at food) and study animals (house spar- heteromyid rodents. Oecologia,76, 408- the same time (and you are only inter- rows to coyotes). The tight link be- 415. ested in one of them), they can be tween the theory of balancing costs Charnov,E.L. (1976).Optimal foraging and the marginal value theorem. Theoretical PopulationBiology, 9, 129-136. Diamond, J. & Case, T.J. (1986).Community ecology.New York:Harper and Row. Hardin, G. (1960). The competitive exclu- Teaching is sion principle. Science,131, 1292-1297. Kotler,B.P. & Brown, J.S. (1988). Environ- easi'er with mental heterogeneityand the coexistence of desert rodents. Annual Reviewof Eco- logicalSystems, 19, 281-307. MacArthur,R.H. & Painka, E. (1966). On Videodiscs! optimal use of a patchy environment. AmericanNaturalist, 100, 603-609. Pulliam, H.R. (1974). On the theory of optimal diets. AmericanNaturalist, 108, Call today for 59-75. Ricklefs, R. (1990). Ecology(3rd ed.). New * Award-winningscience videodiscs your FREEcatalog York:W.H. Freemanand Co. Sokal, R.R. & Rohlf, F.J. (1981). Biometry, * Instant access to thousandsof exciting (800) 548-3472 the principlesand practiceof statistics in imagesand films biologicalresearch. New York:W.H. Free- or (206)285 5400 man & Co. * Art, musicand history discs available Stephens, D.W. & Krebs, J.R. (1986). For- * Lessonsfor Macintosh?, Apple Il? and aging theory.New Jersey:Princeton Uni- versity Press. IBM?/compatibles I] X] m]Iif i t :11 Tilman, D. (1982). Resourcecompetition and * Videodiscplayers, monitors, cables Publisherof IntelligentMedia communitystructure. New Jersey:Prince- ton University Press.

242 THEAMERICAN BIOLOGY TEACHER, VOLUME 53, NO. 4, APRIL1991