The Orgins and Evolution of Predator-Prey Theory

Author(s): Alan A. Berryman

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Source: Ecology, Vol. 73, No. 5 (Oct., 1992), pp. 1530-1535
Published by: Ecological Society of America
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Ecology, 73(5). 1992. pp. 1530-1535
? 1992 by the Ecological Society of America

THE ORIGINS AND EVOLUTION OF

PREDATOR-PREY THEORY'

ALAN A. BERRYMAN
Departmentsof Entomologyand Natural Resource Sciences,
WashingtonState University,
Pullman, Washington99164 USA

Abstract. Predator-preytheoryis traced fromits originsin the Malthus-Verhulstlo-

gisticequation, throughthe Lotka-Volterraequations, logisticmodificationsto both prey
and predatorequations,incorporationoftheMichaelis-Menten-Hollingfunctionalresponse
into the predator and prey equations, and the recent development of ratio-dependent
functionalresponses and per-capita rate of change functions.Some of the problems of
classical predator-preytheory,includingthe paradoxes of enrichmentand biological con-
trol,seem to have been caused by theapplicationoftheprincipleofmass action to predator-
prey interactions.Predator-preymodels that evolved fromlogistictheoryor that incor-
porate ratio-dependentfunctionalresponsesdo not have these problemsand also seem to
be more biologicallyplausible.
Key words: logistic;Lotka- Volterra,predator-preyinteractions;ratio dependence.

INTRODUCTION burg 1989, Arditi and Berryman1991). In this paper

The dynamical relationshipbetween predatorsand I brieflysketchthe originand evolution of population
theirprey is one of the dominant themes in ecology. theoryand, in particular,predator-preymodels. My
Yet the theoryof predator-preyinteractionshas some objectivesare twofold:First,to show how conventional
notableproblems:One is the"paradox ofenrichment," predator-preymodels deviated significantly fromear-
where classical models predictthat enrichingthe sys- lier theory,and how this may have led to some of their
tem will cause an increase in the equilibrium density problems.Second, to show how ratio-dependentpred-
of the predatorbut not in that of the prey (Hairston, ator-preytheoryfollowslogicallyfrombasic concepts
Smith, and Slobodkin 1960), and will destabilize the of single-speciespopulation dynamics, and how this
community equilibrium (Rosenzweig 1969). These viewpointsolves many of the problemsand paradoxes
predictions,however,are not always in line with field of traditionalpredator-preytheory.
observations(Arditi and Ginzburg 1989, Arditi et al.
1991, Ginzburg and Akqakaya 1992). Another is the MALTHUS-VERHULST LOGISTICTHEORY
"biological control paradox" (Luck 1990, Arditi and The firstdefinitivetheoreticaltreatmentof popula-
Berryman1991), where classical models predict that tion dynamicswas Thomas Malthus' (1798) Essay on
you cannot have both a very low and a stable pest thePrincipleofPopulation. Malthus arguedthat,while
(prey)equilibriumdensity,yetthereare numerousex- populations grow logarithmically,the resources on
amples ofpredatorand parasiteintroductions(classical which they depend remain constant or only increase
biological control) that have resulted in exotic pests arithmetically.Thus, the demand for resources must
being maintainedat sparse and apparentlystable den- eventuallyexceed the supply and population growth,
sities(Turnbulland Chant 1961, DeBach 1974, Hagen being dependent on the resource supply, must then
and Franz 1973). cease. Fortyyears later,Verhulst(1838) formedMal-
Recentlytherehas been renewedinterestin what is thus' "principle of population" into a mathematical
beingcalled ratio-dependentpredator-preytheory(Ar- model-the logisticequation
diti and Ginzburg 1989, Berryman 1990). Although
ratio-dependent predator-prey models are notnew,they dN/dt = aN(1 - N/K), (1)
have not previouslyoccupied a central place in eco- where N is the biomass densityof the population in
logical theory.Yet theysolve many of the problemsof question, a is its maximum per-capitarate of change,
more conventionalmodels, includingthe paradoxes of or the instrinsicrate of increase,and K is the equilib-
enrichmentand biological control (Arditi and Ginz- rium density,oftencalled the carryingcapacityof the
I For reprintsof this Special Feature, see footnote 1, p. environment.Althoughthisequation is oftencriticized
1529. forits oversimplicity,it remainsthe centraltheoretical

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October 1992 RATIO-DEPENDENT
constructforsingle-speciespopulation dynamics and,
when generalizedto account fordiscretegrowthpro-
cesses, time-delayed and nonlinear density depen-
dence, and multipledomains of attraction,it describes
the dynamics of many single-speciespopulations in
both laboratory and field (Gause 1934, Allee et al.
1949, Thomas et al. 1980, Berrymanand Millstein
1990).
LOTKA-VOLTERRA PREDATOR-PREY THEORY
Lotka's Elements of Physical Biology (Lotka 1925)
was the next major advance in population dynamics
theory.Not onlydid Lotka derivethe logisticequation,
which he called the "law of population growth,"from
firstprinciples,but he also proposed the firstmodel of
trophic(predator-prey)interactions.However, instead
of developing the predator-preymodel by extending
the logistic"law" to two species he, and soon after-
wardsVolterra(1928, as translatedin Chapman 1931),
adopted thechemical principleof mass action. In other
words,he assumed thattheresponseofthepopulations
would be proportionalto the productof theirbiomass
densitiesso that
dN/dt = aN - bNP,
dP/dt = cNP - dP,
where N and P are the biomass densities of prey and
predator,respectively,a and d are theirper-capitarates
of changein the absence of each other,and b and c are
theirrespectiveratesof changedue to interaction.This
application of the principle of mass action seems to
have been the point where predator-preytheoryde-
viated fromclassical (logistic)thinking,and wheresub-
sequent theorizingmay have been misled.
ShortlyafterpublicationoftheLotka-Volterraequa-
tions, Nicholson and Bailey (1935) proposed a dis-
crete-timemodel of the interactionbetween insect
parasitoids and theirhosts. Althoughthis model was
developed fromthe more mechanisticperspectiveof
parasitoid searchbehavior,it is identicalin concept to
the Lotka-Volterramodel (Royama 1971).
The zero-growthisoclines of the Lotka-Volterra
equations, obtained by settingtheirleft-handsides to
zero, are perpendicularto the axis of the otherspecies
(Fig. la). Solutions of the differential
equations (Eqs.
2) forma seriesof closed ellipses thatdepend critically
on the initialconditions(neutrallystable limitcycles).
In the more reasonable discrete-time(Nicholson-Bai-
ley)form,however,themodel has an unstablesolution;
i.e., the communityequilibrium is an unstable focus
(similar to the trajectoryshown in Fig. la). A great
deal of theoreticalefforthas gone into stabilizingthe
Nicholson-Bailey equations; i.e., by incorporatingin-
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PREDATOR-PREY THEORY 1531
terferencebetweensearchingpredators,spatial hetero-
geneities,polyphagy,etc. (Hassell 1978).
INCURSIONS OF LOGISTIC THEORY
In the original Lotka-Volterraequations, the prey
populationgrowsinfinitelyin theabsence of predators.
To correctthisunreasonableassumption,a logisticself-
limitationtermis oftenadded to the preyequation,
dN/dt = aN(I - N/K) - bNP. (3a)
This modificationproduces an isocline structuresim-
ilar to that shown in Fig. lb and stabilizes the system
(the equilibrium is now a stable focus).
It is interestingthatVolterra(1928, as translatedin
Chapman 1931) and Gause (1934) both used the lo-
gisticequation as theunderlyingstructurefortheirtwo-
species competitionmodels, but failed to consider it
as a suitable frameworkfor modeling predator-prey
interactions.Leslie (1948) seems to have been the first
to consider a logisticpredatorequation
dP/dt = cP(1 - eP/N), (3b)
where e is the densityof prey required to maintain a
single predator and to replace it with one offspring
(2a) when it dies. In otherwords, e is the marginalsubsis-
tencedemand forprey,I /eis themarginalreproductive
(2b)
value of the resource,and N/e is the carryingcapacity
of predatorswhen provided witha constantsupply of
prey.Leslie's equation seems to be the firsttime that
predator/preyratios (P/N) ratherthan products (NP)
are seen in models oftrophicrelationships.The system
of predator-preyequations (Eqs. 3) has an isocline
structuresimilar to that shown in Fig. 1c, with the
communityequilibriuma stable focus.Notice thatthe
predatorisocline is slantingratherthan vertical.This
new isocline structureseems to be intuitivelyreason-
able because predator equilibrium densities are ex-
pected to be dependent on prey abundance (see e.g.,
Berryman1981, Arditiand Ginzburg 1989). In addi-
tion,theslantingpredatorisocline solves theparadoxes
of enrichmentand biological control(Arditiand Ginz-
burg 1989, Arditiand Berryman1991).
PREDATOR FUNCTIONAL RESPONSES
The next major contributionto the theoryof pred-
ator/preyinteractionswas the addition of a predator
functionalresponse.Solomon (1949) and Holling(1959,
1966) argued that,because predatorscan only handle
a finitenumberof preyin a unitof time,thepreydeath
rate should be a nonlinear functionof prey density;
i.e.,
dN/dt = aN(1 - N/K) - b(N)P, (4a)
where b(N) is the functionalresponse of the predator
to preydensity.Based on a seriesof elegantbehavioral
1532 SPECIAL FEATURE Ecology, Vol. 73, No. 5

100 a oo .
a b

8320 80

< <
u.J wU
mr 40 Cm 40

20 20

0 0
200 400 600 800 1000 200 400 600 800 1000

PREY PREY
100 100
C d

80 80

60 60

w W
ci: 40 Cr: 40

20 20

0'
~~~~~~~~~~~~~~~~0
200 400 600 800 100 200 400 600 800 1000

PREY PREY
100 100
e f
830 80

0 60 0 6

cl 40 ,' = 0: 40
al-

20 '20

0 0
200 400 600 800 1000 200 400 600 800 1i00

PREY PREY
FIG. 1. Zero-growthisoclines for models of interactingprey
(i)hand=. =
predator -) populations. The thin line is-
trajectorypredictedby the discrete-timeper-capitatrophicmodel, Eqs. 8 and 9 (see Berryman1990); i.e., N, = N,,_exp~ai
+bMNa t I + c , where i = 1 for prey and i = 2 for predator,Z, is the predator/prey ratio,
N2modl/(ws +N(,,-), in ratio
models and Z, = N,2-1 , = Nl, Iin Lotka-Volterramodels. (a) Lotka-Volterra-Nicholson-Bailey model: a, = 0.2, b, = 0,
cl= -0.004, a, = 0.1, b,= 0, c, = 0.0002. (b) L-V-N-B model with logisticself-limitationon the prey: prey model with
parametersthe same as (a) except a, = 0.3 and b, = -0.0004; predatormodel the same as (a) except C2= 0.0005. (c) Logistic-
Leslie predatorequation: preymodel as in (b); ratio predatorwitha, = 0.2, b, = 0, c, = - 1, w,= 0. (d) Holling-Rosenzweig-
MacArthurmodel: ratio preymodel with a, = 0.3,-b = - 0.0004, c, = -1, w, = 0; predatormodel as in (a), a, = - 0. 5,-b2
= 0, c2 = 0.001, wl= 0. (e) Logistic predator-preymodel with no predator self-limitation: prey model as in (d); predator
model as in (c). (f) Logistic predator-preymodel with predatorself-limitation:preymodel as in (d); predatormodel as in (c)
except b2 = -0.001.

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October 1992 RATIO-DEPENDENT PREDATOR-PREY THEORY 1533

i~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~
ii ff SE S j i .fiiii FfEf .f i ii .iFE j f Eiii g EEE i Ei L i.EiSi .

experiments,in which predators (sometimes blind- by DeAngelis et al. (1975). When insertedintoclassical
foldedstudents)searchedfordifferentdensitiesofprey predator-preymodels, this ratio-dependentfunctional
(sometimes sandpaper disks), Holling derived his fa- response produces a parabolic preyisocline and right-
mous "disk" equation whichturnedout to be identical slantingpredatorisocline (Fig. 1e), therebysolvingthe
to the well-knownMichaelis-Menten equation of en- paradoxes ofenrichmentand biological control(Arditi
zyme kinetics(Real 1977); i.e., and Ginzburg 1989, Arditiand Berryman1991).
b(N) = mN/(w + N), (5)
THE PER-CAPITA VIEWPOINT
where m is the maximum predatorattack rate and w
is the prey densitywhere the attack rate is half-satu- Berryman(1981) and Getz (1984) have argued that,
rated. The Michaelis-Menten-Hollingequation can be because population dynamics arise frominteractions
extended to account forgeneral predatorsthat switch betweenindividual organisms,theequations should be
fromone prey species to another sigmoiddfunctional derived as per-capitaratesof change. For example, we
responses) (Real 1977). When the functionalresponse could writethe followinggeneralratio-dependentper-
is included in the prey equation, we obtain the para- capita trophicequation,
bolic (humped) preyisoclines (Rosenzweig 1971) that
are characteristicof ratio-dependentprey equations dNI/Njdt = Ri = a, - f(NI/N,) - g,(N?+I/N,), (7)
(Fig. Id); note thatthe functionalresponse introduces
ratio-dependenceintothepreyequation because, when whereN, is the biomass densityof the ith species in a
w is set to zero as in Fig. 1, the per-capitadeath rate trophicchain,R, is theper-capitarateof changeof that
of the preybecomes mP/N. species, a, is its maximum per-capitarate of change in
On theargumentthatthe preydeaths can be directly a givenphysicalenvironments definesthe interaction
translatedinto predator births,functionalresponses between the species and the lower trophic level (its
are oftenemployed in predatorequations; i.e., prey) as a functionof the predator/preyratio, and g,
definesits interactionwiththe highertrophiclevel (its
dP/dt= cP[mN/(w + N)] - dP. (4b) predator),also as a functionof the predator/prey ratio.
However, this formulationgives rise to the primitive Using the typeII functionalresponse (Eq. 5) forfand
rectilinearLotka-Volterrapredatorisocline fromwhich g, we can obtain an explictper-capitatrophicequation
arise the paradoxes of enrichmentand biological con- (see Appendix),
trol(cf. Fig. 1a and d). Nevertheless,the isocline struc-
R, = a - bNj/(wjI + N_,) - cNj+1/(w,+ N,), (8)
ture shown in Fig. Id has been employed extensively
in the development of modem predator-preytheory wherebi definesthe effectof intra-specific competition
(Rosenzweig and MacArthur 1963, MacArthur and forfood on the per-capitarate of change (freduces to
Connell 1966). the classical logisticwhen w,_1+ N,-, = a constant;
see Appendix), ci is a coefficient
of vulnerabilitydefin-
ing the effectof predation on the per-capita rate of
RATIO-DEPENDENT FUNCTIONAL RESPONSES change,and w,is the biomass densityof all otherfood
Althoughthe inclusion of a functionalresponse in species in theith trophiclevel. Notice thattheper-capita
the predator-preymodel is intuitivelyappealing, be- viewpointclarifiesthe ecological meaningof the func-
cause it conservativelycouples the preyand predator tional response parameter wi, previously called the
equations, thereare some notable problems with this "half-saturation"point; i.e., it definesthe quantityof
approach. For instance, the functionalresponse de- alternativefood available to the predator.Because the
scribes the behavior of searchingpredatorson a fast denominators of the predator/preyratios in (Eq. 8)
(behavioral) timescale (minutesor hours),whereasthe contain all the preyspecies available to each predator,
population equation, into which it is inserted,often while the predatorsutilizingthat food are contained
operateson a slower(population dynamical)timescale in the numerators,it is fairlystraightforward to extend
(days or years). To overcome thisproblem,Arditiand this equation to food webs with many species in each
Ginzburg(1989) suggestthat,in cases where the time trophiclevel.
scales are incongruent,the functionalresponse should It is worthnoting that, although simple per-capita
be expressedin termsof the ratio of preyto predators; equations are nonlinear in respect to their variables,
e.g., the Holling Type II functionalresponseshould be theyare linear in theirratios and, therefore,can be fit
written to data withstandardregressiontechniques(Berryman
1990). In thisway, model parameterscan be estimated
b(N/P) = m(N/P)/(w+ N/P) = mN/(wP + N). (6)
a posteriorifrom time-seriesdata, such as mightbe
A similar feedingequation was proposed previously obtained fromannual surveysor harvestrecords.For

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1534 SPECIAL FEATURE Ecology, Vol. 73, No. 5

example, the per-capitarate of change of each species LITERATURE CITED

can be estimatedfromthe relationship

Allee, W. C., A. E. Emerson, 0. Park, T. Park, and K. P.
R, = 1/N dN/dt= d In N/dt= ln(N,/N,-,), (9)Schmidt. 1949. Principles of animal ecology. Saunders,
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and this can be regressedagainst the predator/prey Arditi,R., and A. A. Berryman. 1991. The biologicalcontrol
ratios(Eq. 8). These models can thenbe used to predict paradox. Trends in Ecology and Evolution 6:32.
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CONCLUSIONS dependent models. American Naturalist138:1287-1296.
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York, New York, USA.
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Per-capita predator/preymodels evolve naturally ecosystems.Ecology 73:1536-1543.
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October 1992 RATIO-DEPENDENT PREDATOR-PREY THEORY 1535

:: : : :: ::::::::::::::::::::::::::L:::::::::::::::::::::::E:~::
::::::::: :::::::::: ::::: ::::::::::::::: :::::::::::::: ::::i:E : ~
~~~:N0:

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APPENDIX
The type II functionalresponse (Eq. 5) definesthe attack dP/Pdt= c(l - eP/N),
rateper predatorsupplied withN prey,so forP predatorsthe
preydeath rateis mNP/(w+ N). Dividing by N gives the per- Rp= c- bP/N, with b = ce.
capita death rate mP/(w + N) which,afterrelabelling,can be For a single predatorforagingforprey in an arena, this be-
substitutedforf and g, in Eq. 7 to give Eq. 8. It is important comes
to note that the firstper-capitafunctionalresponse (f,in Eq.
7) reducesto the classical logisticwhen the lowertrophiclevel RP = c - b/N,
is constant;e.g.,a constantinputof sunlightforplants.Under whichhas an identicalformto thetypeII functionalresponse;
this condition, w, l + N, I = a constant = E, l, and E Ilb- i.e., R, - -o as N -O and Rp- c as N -oo. Equivalency
= K, -, the equilibrium densityor carryingcapacity of the betweenthe logisticequation and the functionalresponseoc-
environment.Leslie (1948) demonstratedthis implicitfunc- cursifthe per-capitarateofchangeofthe predatoris assumed
tional response withinthe logisticequation; e.g., if we write to be directlyproportionalto the numberof preyeaten, a not
the per-capitalogisticpredatorequation (Eq. 3b) unreasonable proposition.

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