Nordic Society Oikos
A Nutritional View of Understanding and Complexity in the Problem of Diet Selection by
Deer (Cervidae)
Author(s): Thomas A. Hanley
Source: Oikos, Vol. 79, No. 2 (Jun., 1997), pp. 209-218
Published by: Blackwell Publishing on behalf of Nordic Society Oikos
Stable URL: http://www.jstor.org/stable/3546006
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OIKOS79: 209-218. Copenhagen1997
MINIREVIEW
Minireviewsprovidesan opportunityto summarizeexistingknowledgeof selected
ecologicalareas,with specialemphasison currenttopics whererapidand significant
advancesare occurring.Reviewsshouldbe conciseand not too wide-ranging.All key
referencesshouldbe cited. A summaryis required.
A nutritionalviewof understanding
andcomplexityin the problemof
diet selectionby deer (Cervidae)
Thomas A. Hanley
Hanley, T. A. 1997. A nutritionalview of understandingand complexityin the
problemof diet selectionby deer (Cervidae).- Oikos 79: 209-218.
I reviewrecentdevelopmentsin the theoryof diet selectionby deer with a focus on
the diet selectionproblemat the level of individualfood items. Much progresshas
been made in quantitativelypredictingforage nutritionalvalue, effects of plant
tannins,and the handling-timecosts of forageingestionand rumenpassage.Much
progressalso has been made in quantifyingallometricrelationsbetweendeer, their
nutritionaladaptations,and their food requirements.A much greaterappreciation
has beengainedfor the complexityof food resourcesand the heterogeneityof natural
environments.More work is needed, however, in all of the above and also in
deerrumen
quantitativepredictionsof the effectsof nontanninplantallelochemicals,
function and passage rate, and interrelationsbetween factors. The diet selection
problemis highlycomplexprimarilybecauseof interactionsbetweenconstraintsand
objectivesand enormousheterogeneityof food resources.The efficiencyand variation of learned behavior are additionalcomplications.I conclude that although
optimalforagingtheoryis a usefulparadigmfor studyingthe mechanisticprocesses
of the diet selectionproblem,its fundamentalassumptionsare very tenuous.Quantitativepredictionof a rangeof potentially"good"solutionsis more reasonablethan
that of an "optimal"solution.The theoryof diet selectionby deer must be broader
than optimalforagingtheoryalone.
T. A. Hanley, US Forest Service, Pacific Northwest Research Station, P.O. Box 20909,
Juneau, AK 99802-0909, USA.
The deer family (Cervidae) consists of 40 some species
of large herbivorous mammals. They are ruminants and
benefit from a mutualistic interaction with bacteria and
other microorganisms in their foregut to convert plant
cellulose to energy. Although most commonly associated with temperate woodlands of the northern hemisphere, deer occur in a wide variety of habitats nearly
throughout the world (Putman 1988).
The problem of diet selection is fundamental to
understanding ecological interactions between deer and
their habitat. The process of diet selection determines
both the quantity and the quality of food intake and,
hence, the nutritional status of individual animals, their
time and activity budgets, their physiological condition,
growth rates, and potential reproductive and survival
rates. It also determines which plants are consumed
Accepted31 October1996
Copyright? OIKOS 1997
ISSN 0030-1299
Printedin Ireland- all rightsreserved
OIKOS 79:2 (1997)
209
where,when, and to what degree.Diet selection,therefore, is a central process in herbivore-plant interactions, with consequences to the structure, species
composition,and ecologicalrelationsof plant communitiesand theirecosystems.It is believedto be a central
defensesof
processin the evolutionof "anti-herbivore"
plants and both the physical and chemicalnature of
plant communities.
Early studies of diet selectionby deer were entirely
descriptive.Even cafeteria-typefeeding trials were designedto simplydeterminerelativepalatabilities.Studies
of wild deer, usually by rumen analysis and later by
fecal analysis,led to an extensiveempiricalliteratureon
"food habits" of deer. Although generalpatternsbecameevident(e.g., some deerare mainlybrowserswhile
othersaremixed-feedersor even grazers),it also became
evident that tremendousvariationin diet composition
existedboth betweenandwithinspeciesandboth in time
and space.Empiricallists of food habitswereusefulfor
retrospectiveanalyses but were almost worthless for
predictionof dietsundernew or differentcircumstances.
The availabilityof food items is a criticalfactor, and
availabilitynever remains constant. The need for a
theoryof diet selectionby deer becameevident.
My purposehereis to outlinerecentdevelopmentsin
that theory. I focus on diet selection at the level of
individualfood items and do not contend with problems at the patch scale (i.e., habitat selection)or time
and activitybudgets.
harvestand process more materialper unit time than
can small mouths, but small mouths can be more
selectivein bitingthan can largemouths.Hofmannand
Stewart(1972)and Hofmann(1973)developeda major
schemefor separatingAfricanantelopealong a concentrate-selectorvs bulk-feedergradient on the basis of
their rumenanatomyalone. It was a logical extension
to subsequentlyincludedeer (Hofmann1985).
Concentrateselectors in Hofmann's (1985) scheme
includedmostlysmalldeerlike the muskdeer(Moschus
moschiferus), muntjac (Muntiacus spp.), pudu (Pudu
pudu), brocket (Mazama spp.), and roe deer (Capreolus
capreolus).Bulk feeders were not well representedin
the deer family but were most closely representedby
the Pere David's deer (Elaphurus davidiensis), fallow
deer (Dama dama), sambar (Cervus unicolor), and
barasingha (Cervus duvauceli).The caribou/reindeer
(Rangifer tarandus), red deer (Cervus elaphus) and most
other membersof the Cervidaewould be intermediate
feedersvaryingin relativepositionsalong the gradient.
Many interrelationsexist betweenbody morphology
and feeding styles. Although Hofmann (1989) emphasized the predominant importance of digestive
anatomy,body size certainlyis a majorfactorrelatedto
mouth size, rumensize and function,and food selection
(Gordon and Illius 1994, Robbins et al. 1995). The
intercorrelationof factors makes the question of primacy of any one factor largelyirrelevant.The grazerbrowser dichotomy and concentrate-selector vs
bulk-feedergradienthave been useful ways of viewing
the evolutionof body morphologyin deer and predictDiet selectionin relationto deer speciesand ing differencesin patternsof food selectionand habitat
use (e.g., Hobbset al. 1983,Hanley1984,Putman1986,
forage types
1988, Gordon 1989). Those concepts, however, are
A nutritional theory of diet selection by ruminants most relevant at the broad levels of forage types
emerged from studies of domestic sheep and cattle (browse,grasses,forbs) or plant parts (flowers,leaves,
(Bovidae)in the late 1950sand early 1960swith obser- stems).They are not very helpful at the level of plant
vation of relationsbetweenanimalbody size, digestive species.
system, mouth size, and degree of feeding selectivity
(Lofgreenet al. 1957,Meyeret al. 1957,Arnold 1960a,
b, 1962, Cook et al. 1962).Ten years later, those ideas
were refined and extended to antelope (Bovidae) in Diet selectionin relationto plant species
Africa as a means of explainingecologicalpartitioning More recent thrust in the theory of diet selection by
of habitat(Bell 1969, 1971,Hofmannand Stewart1972, deer has shifted to the plant species level for at least
Hofmann 1973, Jarman 1974) and to deer in North two reasons:(1) plant specieswithinforagetypes differ
America and Europe as a means of explaining diet greatly in physical properties,chemical composition,
selection(Nagy et al. 1969,Prinsand Geelen 1971).The and nutritionalvalue;and (2) ecologicaland evolutiontheory dealt only with broad types of forages(browse, ary interactionsbetweenherbivoresand their food regrasses,forbs)and consistedof a conceptualframework sourcesoccurat the specieslevel (andbelow),not at the
of ideas ratherthan a quantitativetheoryper se (Han- broad level of forage type. Diet selectionat the plant
ley 1982): (1) large animals are more time-limitedin specieslevel, however,is an enormouslycomplexprobtheirdietarychoicesthan are small animalsbut require lem, and we really are only just beginningto underless energyper unit body mass than do small animals; stand it. The approachthus far has been to view it
(2) large rumino-reticulumsare an adaptationto ex- within the context of an optimal foraging problem.
ploiting high-cellulosediets (i.e., grasses),while small That requiresthree very importantassumptionsthat
rumino-reticulums
are an adaptationto exploitinghigh- may or may not be true: (1) forage "value" can be
lignin diets (i.e., browses);and (3) large mouths can measuredin a currencyor combinationof currencies
210
OIKOS 79:2 (1997)
that are importantto the animal;(2) the animal can
recognizeforage value eitherdirectlythroughthe chosen currencyor indirectlythrough something highly
correlatedwith the currency;and (3) the animal behaves in such a way as to maximize its intake or
minimizeits loss of the currency.The last assumption,
particularly,is especiallytenuous,but it is necessaryto
convertthe behavioralprobleminto an essentiallymechanicalone that can be reducedto componentparts,
quantified,and modeledquantitatively.
Foragevalue,regardlessof the chosencurrency,must
be measuredin termsof nutritionalvalueper unit time.
In other words, it is a ratio, and both the numerator
(nutritionalvalue) and the denominator (time) are
equally important. Nutritional value is usually expressedin terms of digestibleor metabolizableenergy
and/ornutrients(positivevalue) and/or allelochemicals
(negativevalue).The time componentfor deer involves
searchtime (or its inverse:encounterrate)and handling
(or processing)time. Handlingtime is comprisedof two
dry-matterintakerate
very differenttime requirements:
(ingestion)and rumenpassagerate (digestion,assuming
that rumenpassageis the limitingtime elementin the
digestion process). One reason that the diet selection
problemis so complexis that all of the above factors
are interrelated.Another reason is that most of the
factorsare both difficultto measureand highlyvariable
among plant species, part, season, and habitat. Additionally, other constraintssuch as avoidanceof predation or social interactionscan restrict the range of
possiblesolutions.
Nutritional value and allelochemicals
Both nutritionalvalue and allelochemicalscould be
measuredin termsof a very largenumberof nutrients,
vitamins,elements,and organiccompounds.Digestible
energy and digestibleprotein, however, are the two
nutritionalfactors most commonlyin short supply to
deer (Van Soest 1982, Robbins 1993). Requirements
and metabolismof energy and protein are reasonably
well known. Mineral deficienciesare usually of only
local importancebut certainlywould be a complicating
factor if the deficiencywere unrecognized(e.g., Flueck
1994). Allelochemicalsare a very broad group of elements and compoundswith effects rangingfrom acute
toxicity and death to interferencewith digestion or
metabolism of energy or nutrients (Rosenthal and
Janzen1979).The group of allelochemicalsbest understood for deeris that of phenolics,particularlytannins.
Much attention also has been directedtoward etherextractableresins and terpenoid compounds (Bryant
and Kuropat1980,Duncan et al. 1994).Tannins,phenolic resins,and terpenesinterferewith digestion.
Coefficientsof digestibleenergy and digestibledry
matterarevirtuallyidenticalfor plant-baseddiets(RobOIKOS 79:2 (1997)
bins 1993).Grossenergyof plantleavesand stemsvaries
relativelylittle between species (Golley 1961), so drymatterdigestibilityis usuallythe variableof interestin
analysisof the energyvalue of food. The othercomponents of energypartitioning(metabolizableenergyand
net energy)are usuallyeitherignoredor assumedto be
constant across food items. Those assumptionsare
mostly for convenience.Metabolizableenergy coefficients do vary with foods, rangingfrom about 0.76 in
coniferbrowseto 0.84 in grassesand 0.87 in concentrate
feeds(Robbins1993),the valuedependingmostlyon the
urinary excretion of high-energy, digestion-resistant
compoundssuch as terpenoidsand phenols.Net energy
coefficientsalso may vary substantially(e.g., from 0.47
to 0.81, Robbins1993),dependingon the heatincrement
from energyconversionand whetherthe energyis used
for maintenanceor production.Both metabolizableand
net energycoefficientsare much more difficultto measure than is digestibleenergy. They are seldom mentioned in the ecologicalliteratureof food selection.
Dry-matterdigestibilityis the most variable, and
thereforeimportant,factorin the relativeenergyvalues
of potentialfood items for deer. It can be measuredin
in vivo digestiontrialsandcan be predictedwithsummative equationsbased on plant fibercomposition(detergent analysis) and protein-precipitatingcapacity of
tannins(Robbinset al. 1987a,Hanleyet al. 1992).The
predictiveequations have the advantageof requiring
small amounts of sample material for analysis and
isolatingthe factorsresponsiblefor dry-matterdigestion.
Dry-matterdigestibilityof a forageis the sum of the
digestiblefractionsof the forage'stwo principalcomponents: neutraldetergentsolubles (chieflythe cell cytoplasm)and neutraldetergentfiber(chieflythe cell wall)
(Goeringand Van Soest 1970).Dry-matterdigestibility
of neutraldetergentsolublesusuallyrangesfrom 98 to
100%(Mouldand Robbins 1982,Robbinset al. 1987a),
althoughtanninscan reducethat by about 2.8 units of
dry matterfor each unit of proteinreduction(Robbins
et al. 1987a,Hanleyet al. 1992).Digestibilityof neutral
detergentfiber dependson its concentrationof lignin,
cutin, and silica (Robbinset al. 1987a).Largeor grazing deer with slower rates of rumen passage tend to
digest more of the neutraldetergentfiberof low-lignin
diets than do small or browsing deer (Mould and
Robbins 1982, Bakerand Hobbs 1987). Differencesin
digestiveefficienciesbetweenspeciesof deer are less for
high-lignindiets than for low-lignindiets. Tanninscan
reduce fiber digestion in domestic sheep (Ovis aries),
which are usually grazers and lack tannin-binding
proteinsin their saliva (Robbinset al. 1991). Salivaof
the browsing mule deer (Odocoileus hemionus), on the
other hand, is rich in tannin-bindingproteins, and
tanninsappearto have little effect on fiberdigestionin
that animal(Austinet al. 1989, Robbins et al. 1991).
Digestibleproteinand digestibledry matterare usually highly correlatedin deer consuming tannin-free
211
Rather than seeking specificprey, the deer is usually
assumedto travelthroughan environmentcontaininga
superabundanceof potential foods varying greatly in
their potential nutritional value. Search time for a
particulartype of food is then consideredsimply the
inverseof its encounterrate, which is a functionof its
density (number per unit area), spatial distribution
(clumped,uniform,etc.), apparency(distanceat which
it can be seen), and the speedof traveland search-path
width of the foragingdeer (Roese et al. 1991,Spalinger
and Hobbs 1992).That is a mathematicallyreasonable
approach,but it ignores the concept of search image
and the idea that deer actively search for particular
food items. The role of learning in diet selection is
known to be important in domestic ruminants
(Provenzaand Balph 1987,Thorhallsdottiret al. 1987,
Parsons et al. 1994), however, and learned behavior,
search image, and active search for preferredfoods
have been shown to be used by deer in experimental,
controlled environments (Gillingham and Bunnell
1989a,b). Learnedbehaviorand active searchcomplicate the searchelementof the time componentfor deer.
It seems that this will be a difficultproblemto solve
with a strictly mechanical approach. So far, it has
receivedless attentionthan have the handlingelements
of the time component.
Adding to the complexityof the time componentis
the fact that all threeof its elements(search,ingestion,
digestion)may overlap to various degrees.Forage intake (ingestion)and forage digestionare usually measured on widely differenttime scales. Forage intake is
measuredon an "instantaneous"scale of grams per
minute,whileforagedigestionis measuredon a scaleof
percent per hour. Both are sometimes measured in
kilogramsper day, and then rumenpassageis considered to be the rate-limitingfactor for both. But such a
simplificationgrosslyunderestimatesthe importanceof
the ingestion process, which is the process where the
actual choice of bites of food takes place. Whichbites
are chosen determinesthe quality of the diet, and the
numberof bites and theirsize determinethe quantityof
intake(Parkeret al. 1996).Bitingand diet selectionare
linked throughmuzzlewidth and incisor arcade(Gordon and Illius 1988)and time budgets(Illius and Gordon 1987, 1990, Illius et al. 1995, Spalinger1997).
Dry-matterintakerate (gramsper minute)correlates
with foragebiomass(gramsper squaremeter)for deer
feeding in grass pastures(Wickstromet al. 1984), but
has no relationwith foragebiomassfor deerfeedingon
forbs or shrubs(Wickstromet al. 1984,Spalingeret al.
1988).The reasonis that bite size (gramsper bite) is the
controlling factor, and biomass frequentlycorrelates
with bite size for grassbut has no relationto leaf size of
forbs and shrubs(Wickstromet al. 1984, Spalingeret
Search and handling time: ingestion
al. 1988,Spalingerand Hobbs 1992,Gross et al. 1993).
The concept of search time for a generalistherbivore Bite size is the controllingfactor because biting and
has been taken to be differentfrom that of a predator. chewing are competing processes in forming a bolus
grassesand legumes (Robbins et al. 1987a, b). Crude
proteinalso is highly correlatedwith digestibleprotein
in such forages, averagingabout 93%digestible(Robbins et al. 1987b). Most leaves of forbs, shrubs, and
trees,however,containappreciableamountsof tannins,
which affectproteindigestionmarkedly(Robbinset al.
1987b).Tanninsare very importantin the problemof
diet selectionby deer, becausemost deer rely on leaves
of forbs, shrubs,and treesfor a substantialpart of their
diet during at least some time of the year. Deciduous
browsestems, on the other hand, are frequentlylow in
tannins(Robbinset al. 1987b).
The effects of tannins on protein digestion can be
predictedon the basis of measurementof theirproteinprecipitatingcapacity(Robbinset al. 1987b,Hanley et
al. 1992), thus greatlyfacilitatingthe problemof dealing with tannins in analysis of diet selection. More
researchis needed,however,on the occurrenceof tannin-bindingsalivaryproteins(Robbinset al. 1991)in a
wide rangeof deerspecies.Moreresearchalso is needed
on quantitativelypredictingthe effects of other major
groupsof digestionreducerssuch as terpenes,whichare
very common in coniferousfoliage and browse.
Nontannin phenolics are another group of compoundsthat are commonin foragesconsumedby deer.
Althoughtheireffectson digestionmay be minor,they
apparentlyare readily absorbed into the circulatory
system and may pose problems of acute toxicity if
consumedin sufficientquantities(McLeod 1974, Robbins et al. 1987b).Deer seem able to choose diets that
balancedigestibledry matteragainstnontanninphenolics (McArthuret al. 1993). The mechanismsand efficienciesof such choices, however,are not known.
Both phenolicsand terpenesare carbon-richand as
such are model compounds for the theories of carbon:nutrientbalance (Bryantet al. 1983, Coley et al.,
balance(Loomis1932,
1985)and growth-differentiation
1953,Hermsand Mattson 1992,Lerdauet al. 1994)for
patternsof resourceallocationwithinplants.Both theories explain relative allocation of carbon to growth
versusdefenseas a functionof the balanceof light and
nutrientavailabilityto the plant.They mighteventually
prove useful in predictingplant defensesin relationto
environmentand, therefore,become powerfultheories
linkingthe physicalenvironmentto theoryof diet selection by deer. Currently,however, the predictionsare
only qualitativeratherthan quantitative,and resultsare
highlyspeciesspecific(Van Horneet al. 1988,Happeet
al. 1990, Basey and Jenkins1993, Edenius1993, lason
and Hester 1993, Shure and Wilson 1993, Ford et al.
1994).
212
OIKOS 79:2 (1997)
before it can be swallowed.So increasedtime spent
biting is lost from chewing,and high biting frequency
cannot compensate for small bite size (Shipley and
Spalinger1992,Spalingerand Hobbs 1992,Gross et al.
1993,Lacaet al. 1994a,b). Deer can chew as they walk
to new bites, however.Dry-matterintakerate of foraging deer,therefore,can be predictedquite accuratelyas
a function of bite size alone, which correlatesclosely
with leaf size (Gross et al. 1993). The relationshipis
asymptoticand functionallydescribedby an equation
of Michaelis-Menton
form (Spalingerand Hobbs 1992):
as bite size increases,intake increasesto the maximum
rate that the deer can prepare food for swallowing.
That maximumrate scales with body mass to the 0.71
power,which also coincidesclosely with the scalingof
daily energyrequirements(Shipleyet al. 1994).
Search and handling time: digestion
Time requirementfor digestionand rumenpassagehas
become widely recognized as a critical factor controllingdiet selectionby deer,but it also is probablythe
most misunderstoodof the major componentsof the
diet selectionproblem.It certainlyis the most poorly
understood.Models of rumenfunctionhave been proposedfor deer(Illiusand Gordon 1991, 1992,Spalinger
and Robbins1992),but they are basedon veryfew data
and rely heavily on the domestic livestock (Bovidae)
literature.One thing that seems certainis that rumenpassage rate is not simply a function of chemicalor
physicalpropertiesof the forage.It is a processinextricablylinkedto the time-energybudgetof the animalas
well.
Digestion and rumen passage are interactingand
competingprocesses:as the rate of passage from the
rumenincreases,the food has less time to be digested,
and its digestibilitydecreases(Milneet al. 1978,Mould
and Robbins 1982, Robbins 1993). Three mechanisms
are believedto be responsiblefor controllingthe rate of
dry-matterflow from the rumen (Spalinger1997):(1)
Flow is restrictedby food particlesize, and particlesize
is dependenton time in the rumen, mean cell wall
thicknessof the forage, and rate of ruminationby the
animal(Spalingeret al. 1986),(2) particlespecificgravity increaseswith time and rumination,and the particles sink to the lowerportionof the rumen,wherethey
becomepart of the small-particlepool (Lechner-Dollet
al. 1991), and (3) small-particleflow is controlledby
liquid passage rate (Spalingeret al. 1993), which is
stronglyinfluencedby saliva flow and rumencontractions (Willeset al. 1970).
Dry-matterflow from the rumen, therefore,should
be partly under control of the animal itself through
control of ruminationtime and liquid passage rate.
That is a very differentview from one of limitationby
simply wet-weightof rumenfill (Belovsky 1978, 1984,
OIKOS 79:2 (1997)
1986, see Hobbs 1990),digestibleenergy(Fryxell1991,
Wilmshurstand Fryxell 1995), dry-matterdigestibility,
lignin content, or other such forage-basedvariable
(Spalingeret al. 1986).
If the deer has control over rate of passage,then it
should have options for varying intake and digestion
efficiencyby varying rumen fill and/or passage rate.
Although passage rate is variable,two sourcesof evidence indicatethat the options for varyingrumenfill
are ratherlimited:(1) dry-matterfill is highlycorrelated
with body mass in deer (Gordon and Illius 1994,
Spalinger1997);and (2) 50-78% of the dry-matterin
the rumenis commonlyof a size small enough to pass
the rumen-omasal orifice (Spalinger et al. 1993).
Spalinger(1997) has hypothesizedthat both of those
conditionsare necessaryto maintainconstancyof segregation and flow of material to the lower digestive
tract and preventomasalimpaction.Furtherreseachis
needed, however, for a better understandingof that
processand of the time costs associatedwith digestion
and rumen passage. "Embarrassinglylittle is known
about the kinetics of rumen function in cervids"
(Spalinger1997).
Interactionof factors
Much progress has been made in understandingthe
allometric relations between body size, mouth size,
rumen capacity and fill, metabolic requirements,and
maximum dry-matter intake rates in ruminants
(Demment and Van Soest 1985, Illius and Gordon
1987, Gordon and Illius 1994, Shipley et al. 1994,
Robbins et al. 1995, Spalinger 1997). Most analyses
have involvedbovids, but the same patternsappearto
hold for cervids as well. The basic pattern is that
ruminant species differentiateecologically primarily
along a body-sizegradient,whichdeterminesmetabolic
requirements,mouth and digestivesystemmorphology,
and behavior of diet selection. Deviations from that
pattern (e.g., the large, browsingmoose, Alces alces)
facilitatefurtherecologicaldifferentiation.Those relations have been very useful in understandingfood
requirementsof individualspecies (e.g., Holand 1992,
1994, Holand and Staaland 1992) and differentialexploitation of food resourcesby sexes (Staines et al.
1982, Illius and Gordon 1990) and age classes (Illius
and Gordon 1990, Andersenand Sather 1992). They
are far from sufficient,however, for predictingdiet
selectionat the level of the plant species.
It is the interactionof factorsthat makesthe problem
of diet selectionat the plant specieslevel so complex:
The bite size that the deer selects, for example, is
fundamentalin determiningits dry-matterintake rate
(discussionabove), but nutritionalquality of the bite
also is often stronglyaffected by its size. Nutritional
qualityof browsefor moose, for example,declineswith
213
increasingtwig diameter (Hjeljordet al. 1982, Vivias
and Sether 1987, Palo et al. 1992), thus creating a
trade-offdecisionbetweenintake rate and diet quality
for selectionat even the level of twig diameterwithin
the same twig (Vivas et al. 1991, Palo et al. 1992).
Similartrade-offsexist betweentwigs on the same tree
and trees withinthe same foragingpatch (Sether et al.
and Andersen1990,Astrom
1989, Sether 1990, Swather
et al. 1990, Danell et al. 1991, Edenius 1991, Suomela
and Ayres 1994). Extension of the problem to other
species within the patch involves not only their shoot
sizes (Bergstr6mand Danell 1986) but also their relative availabilities(Lundbergand Palo 1993), proximities to one another(Danell and Ericson1986,Danell et
al. 1991, Edenius1991), and prior browsing(Danell et
al. 1985, Bergstrom and Danell 1987, Danell and
Bergstrom1989, Hjaltenet al. 1994). Correlationsbetweentwig diameterand nutritionalvaluewithina twig
may be negative(above), but may be positive between
twigs of separatetrees (Niemelaand Danell 1988).
Choice of bite size or plant species also involves
trade-offswith ruminationtime, passage rate, and digestion. All are interrelated.Large bites, which can
yield greaterrates of dry matterintake than can small
bites, requiremore ruminationtime if they are more
fibrousthan the smallbites (Laca and Demment1992).
Rumen passagerate and dry-matterdigestionalso are
competing processes in the determinationof energy
intake (Robbins 1993), and rumen passage rate is to
some degree dependenton the volition of the animal
(discussedabove). Nutritionalvalue of any particular
forage, therefore,is a variableratherthan a constant,
and it depends on the animal's choice of bite size,
rumination,and passagerates. The "optimal"solution
to those decisionsis not a simpleproblem.It depends
on the entire time-energybudget (Owen-Smith1994).
Seeminglysmall differenceshave a "multipliereffect"
as they progress through the interrelations(White
1983).
Deer eat diets comprised of mixtures of forages.
Individualforages cannot be selectivelyruminatedfor
different amounts of time or selectively sorted and
passed from the rumen at differentrates, at least not
volitionally. Thus, the optimal solution to the bite
size-rumination-passage
problemmay be irrelevantanyway as "associative"effects of other dietary components influencethe outcome. Shrub stems added to a
grass diet, for example,can increasethe rumenretention time of the grass and therebyincreaseits dry-matter digestibility(Bakerand Hobbs 1987).
Additionalcomplexityof an entirelydifferentnature
is evidentin considerationof how little is knownabout
allelochemicalsof plants. The number of compounds
and their variation between and within species are
enormous. We have only just begun to scratch the
surfaceof understanding
them.Finally,complexityof an
entirely different scale is evident in considerationof
214
foraging patch and landscapechoices (e.g., Langvatn
and Albon 1986,Langvatnand Hanley1993,Kohlmann
and Risenhoover1994) and the hierarchicalnature of
foragingdecisions(Senftet al. 1987,Edwardset al. 1994,
Ward and Saltz 1994, Clarket al. 1995a,b): interrelations betweenchoice of foragingpatch, plant species,
plantpart,and size of part.Onethingthat is clearis that
despite having come a long way in understandingthe
foragingprocessin deer,we still have a lot furtherto go
for predictingdiet selection at the level of the plant
species.
Conclusions
The past decade has brought major progressin our
understandingof both the nutritionalvalue and the
handlingtime componentsof the foragingprocess.We
now have quantitativebases for predictingnutritional
value of forages in terms of digestible energy and
digestible protein and for accounting for effects of
tannins in digestion.We have a quantitativebasis for
predictingdry-matterintake rate as a function of animal body size and plant characteristics.And we have
learnedenoughabout rumenfunctionto know that it is
inextricablylinked to the time-energybudget of the
animal ratherthan measuresof forage characteristics
alone. We also have gainedmany new insightsinto the
heterogeneityof the forage resource as perceivedby
deer, which is far more complex than simply a list of
plant species with their chemicaland biomass values.
Equally important,we have seen how those factors
interactin complex,yet now understandable,
ways. Our
ability to explain patternin deer-vegetationrelations
has improvedsignificantly,and in the processwe have
gainednew insightsimportantfor managementof deer
habitat,competitiveinteractionswith otherspecies,and
effects of deer on plant communities.
A predictivetheory,however,will requiremuchmore
work in all of the above. We currentlyare especially
weak in quantitativepredictionsof the effects of nontannin allelochemicals,deer rumenfunction,and interrelations between factors. Quantitative linkages
betweendifferentlevels in the hierarchyof choice (e.g.,
leaves, plants, patches, landscape) also are greatly
needed.Our view of the forage resourcemust broaden
beyond the conceptsof genus, species,and plant part.
It must include variation in chemical composition
within species and even within plant part, physical
characteristicssuch as plant architecture,and variation
in spatialand temporaloccurrence(i.e., "availability").
Those are major challengesahead. The easy work alreadyhas been done.
In my opinion, however,it is unlikelythat a sound,
quantitativeunderstandingof the mechanisticprocesses
alone will ever be sufficientfor accurateand precise
predictionsof dietarychoiceby deerin complexhabitats.
OIKOS 79:2 (1997)
The optimal foraging paradigm is useful for the mechanistic approach, but whether its fundamental assumptions are realistic is another question. The ability of
the animal to accurately assess forage value in the
optimal currency and to behave in such a way as to
maximize its intake or minimize its loss of that currency
is highly suspect. The role of learned behavior and,
especially, its efficiency and variation remain very complicated factors and mostly unknown. Individual animals vary widely in their behavioral responses to
environment. Although an "optimal" solution to the
diet selection problem may remain an optimal theoretical goal for science, accurate prediction of behavior
corresponding to a range of potentially "good" solutions (or solution space) seems much more likely to be
achieved as a pragmatic goal.
Such a conclusion, however, is not scientifically satisfying: it begs the question of where to go next. Optimal
foraging theory already has been very useful.
Belovsky's (1978) optimal foraging analysis of the diet
selection problem in moose was a turning point in the
theory of diet selection by deer because it forced ecologists to carefully consider the handling time component
of the foraging process. It helped put into context the
trade-offs involved in ingestion and digestion and to
shift the theoretical problem from largely a behavioral
question to a mechanistic question.
A fundamental problem facing ecologists, however, is
to ensure that the mechanisms involved in their foraging models are faithfully represented. Overly simplistic
and inaccurate views of processes or constraints (involving rumen passage, for example) are not likely to
lead to real understanding (Hobbs 1990, Owen-Smith
1993), despite initial appearances to the contrary (Huggard 1994). My review of the nutritional literature
illustrates the complexity of this problem.
I believe that optimal foraging theory will continue
to play an important role in focusing attention on the
mechanisms of ingestion, digestion, nutritional value,
and dietary choice. That role is very important. However, the theory of diet selection by deer must be
broader than optimal foraging theory alone; it must
include the role of learning and possibly even phylogenetic history as well. It also must allow for the broad
plasticity so frequently seen in diet selection by deer.
The challenge is formidable, but the rate of progress
has been substantial. We have come a long way from
searching for pattern in lists of diet compositions. We
now must broaden our view of the problem and approach again.
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