Population Growth Rate

Population Growth Rate and Its Determinants: An Overview Author(s): Richard M.
Sibly and Jim Hone Source: Philosophical Transactions: Biological Sciences, Vol. 357, No. 1425, Population Growth Rate: Determining Factors and Role in Population Regulation (Sep. 29, 2002), pp. 1153-1170 Published by: The Royal Society Stable URL: http://www.jstor.org/stable/3067125 . Accessed: 18/11/2013 01:40
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E THE ROYAL SOCIETY
29 August 2002 Publishedonline
Population growthrate and its determinants: an overview

Richard M. Siblyl* and Jim Hone2
'SchoolofAnimaland Microbial RG6 6AJ,UK Sciences, University ofReading, PO Box 228, Reading 2Applied Ecology Research Group, Canberra University ofCanberra, ACT 2601,Australia We arguethatpopulation rateis thekeyunifying growth variable thevariousfacets ofpopulation linking rate lies partly in its central ecology.The importance of populationgrowth role in forecasting future indeedifthe form of density population trends; wereconstant and known, dependence thenthe future could to some degreebe predicted. population dynamics We arguethatpopulation rateis also growth central to ourunderstanding ofenvironmental stress: environmental stressors shouldbe defined as factors which whenfirst reducepopulation appliedto a population rate.The jointactionofsuchstressors growth an organism's determines which shouldbe defined ecological niche, as thesetofenvironmental conditions where rateis greater thanzero(where population growth rate= r= loge(Nt+ population While growth 1/Ne)). environmental stressors have negative on population effects growth rate,the same is trueof population the case of negative lineareffects to thewell-known density, corresponding logistic equation.Following we recognize as occurring whenpopulation Sinclair, population regulation rateis negatively growth density dependent. in population Surprisingly, givenits fundamental importance ecology, only25 studieswere in theliterature discovered in whichpopulation ratehas been plotted growth against population density. In 12 of thesethe effects of density were linear;in all but two of the remainder the relationship was concaveviewedfrom above. Alternative to establishing approaches thedeterminants ofpopulation growth rateare reviewed, paying to the demographic and mechanistic specialattention The effects of population approaches. on density ratemayact through population growth their effects on foodavailability and associated effects on somatic and survival, growth, fecundity to a 'numerical according response',the evidenceforwhichis briefly reviewed. there on population Alternatively, maybe effects growth rateofpopulation in addition density to thosethatarisethrough thepartitioning offoodbetween thisis 'interference competitors; competition'. The distinction is illustrated using a replicatedlaboratory experiment on a marinecopepod, Tisbe oftheseapproaches battagliae. Application in conservation biology, ecotoxicology and humandemography is briefly We concludethatpopulation considered. resourceand interregulation, density dependence, ference theeffects of environmental competition, stress and theform oftheecologicalniche,are all best defined and analysed in terms ofpopulation rate. growth Keywords:demography; niche;population growth rate;population regulation 1. INTRODUCTION Withthe persistent increaseof the humanpopulationnowexceeding sixbillion-all speciesfaceincreased pressure on resources. the factors Understanding responsible for limiting populationsor causing species' extinctions therefore has increased urgency. Recentdevelopments in populationanalysis,describedbelow, have refined our understanding of the determinants of population growth rate and linkedthe theoryto field data, and thereis in applying increasing interest methods ofthiskindin conwildlife and ecotoxicology. servation, management This paper emphasizesthe centralrole of populationgrowth rateand reviews theuse ofdata to testrelevant theory and forwildlife modelsprimarily In thissection populations. we consider the definition and importance of population growth rateand briefly examine itshistorical background.
(a) Definitions and estimation of population growth rate
*Author forcorrespondence (r.m.sibly@reading.ac.uk).
One contribution of 15 to a Discussion Meeting Issue 'Population growth rate:determining factors and rolein population regulation'. Phil. Trans.R. Soc. Lond. B(2002) 357, 1153-1170 DOI 10.1098/rstb.2002. 1117 1153
Populationgrowth rate is the summary parameter of trendsin populationdensityor abundance. It tells us whether and abundanceare increasing, density stableor and how fasttheyare changing. decreasing, Population growth rate describes the per capita rate of growth of a either as the factor population, by whichpopulation size increasesper year, conventionally given the symbolA or as r= logeA.Generally (= N,+,/Ne), here, population growth rate will refer to r. A is referred to variously as 'finite growth rate of increase','net reprorate', 'finite ductive rate'or 'population rate'.ris known multiplication as 'rate of natural increase','instantaneous growth rate', rateof increase'or 'fitness'. 'exponential In the simplest in the populationare populationmodel all individuals assumedequivalent, withthe same deathratesand birth
? 2002 The Royal Society
rateand itsdeterminants growth 1154 R. M. Sibly and J. Hone Population
in oroutofthepopulation, is no migration and there rates, growth occurs;in thismodel,population so exponential
and growth rateis positive population carrying capacity, capacity; concarrying increasestowards the population is above carrying capacity, popuversely when density growthrate= r= instantaneousbirthrate - instantaneous declines. and thepopulation rateis negative lationgrowth deathrate. by themechis controlled density estimatedusing In thiswaypopulation Population growthrate is typically dependenceof population density either census data over time or from demographic anismof the negative changes by growth rate,and in theabsenceofenvironmental data. Censusdata are analysed and survival) (fecundity of remains in thevicinity population density the linear regressionof the natural logarithmsof or time-lags, data using the carryingcapacity. abundanceover time,and demographic Euler-Lotkaequation (Caughley 1977) and population of (c) Historical background (Caswell 2001). The twomethods matrices projection ratehas of population growth The pivotalimportance values,as shownin studiesof can givesimilar estimation backcaurina been recognizedfor a long time. The historical the northernspotted owl, Strix occidentalis by Cole (1958) and Hutchinhas been described flamingo, ground (Lande 1988; Bumham et al. 1996), greater outlineis son (1978), on whichsome of the following ruberroseus(Johnson et al. 1991), and pea Phoenicopterus restrained population growth based.The idea ofgeometric & Stark1997). The (Walthall pisum Acyrthosiphon aphids, oftheenvironcapacity bythecarrying at higher densities power to detecta statistical census methodhas greater in a book by Botero (1588), and methodwhen mentwas put forward populationdeclinethan the demographic attention to general elaborated and brought occurs was famously and thereverse populations appliedto high-density in tablesofmortality byMalthus(1798). Detailedinterest 1993). (Taylor& Gerrodette with low-density populations century, withmathematical rate (A) beganin thelate seventeenth populationgrowth The estimation of the finite ofanalysing analysesby Huygens and later Buffonamong others. themanner factors: maybe biasedby several 'failed to that Newtonnotably Cole suggests ofspatial variance Interestingly, censusdatawith zeros,bytheexistence is a function and by the scale of the graspthebasic conceptthatlifeexpectancy covariance, and spatial-temporal theequationthatbears of age'. Euler (1760), in deriving area studied(Steen & Haydon2000). dependenceof his name, established the mathematical value of -xo to a value of 0.0 r variesfrom a minimum birthrates and rate on age-specific value (rm) when populationgrowth to a maximum fora stablepopulation, comesbackto and commented that'it always possiblerate, deathrates, the populationincreasesat the maximum thatofmortality and thatoffertility, areno predators, patho- thesetwoprinciples, and there whenfoodis abundant fora certain place, oncethey havebeenestablished valuesof A are which, The corresponding gensand competitors. whichone could all thequestions makeit easyto resolve 0.0, 1.0 and Amax.The frequencydistributionof A of a timeand space is positively propose...'. The proposal that populationgrowthrate through persisting population withpopulationdensity, knownas the of declineslinearly value further to the right maximum with the skewed, by Verhulst(1838). distri- logisticequation,was put forward value.The frequency themode thantheminimum to theworkofthemodgrowth rateis central closer to a normaldistribution Population bution of r is generally ernfounding fathers ofecology (Lotka 1925; Fisher1930; (Hone 1999). & Birch 1954), but the Nicholson 1933; Andrewartha birthand of its dependenceon age-specific complexities (b) Importance in projection offuturepopulation examthorough prevented deathrateshave untilrecently sizes rate. With the inationof the role of populationgrowth rate is that it The importance of populationgrowth of and the development advent of moderncomputing of future allows qualified populationsizes. If projection life the methods for the of tables, impormatrix analysis then were no growth there population dependence density ratein thestudy ofpopulation tanceofpopulation from theEulergrowth at a ratecalculable wouldbe exponential, theexisting ecologyis becomingmore widelyappreciated(Caswell data from Lotka equationusingdemographic population.However, in a finiteworld the resources 2001). must eventually growth needed to supportexponential (d) Scope and layout ofpaper become inadequate, and populationgrowthrate then roleofpopulation thecentral In attempting to establish ofpopulation growth dependence density declines, giving how we first consider ratein population ecology, ofdensity in ? 3. Iftheform rateas discussed dependence growth such of basic it used in the definition concepts should be future then the and were constant population known, stressand ecologicalniche, and then To what as environmental could to some degreebe predicted. dynamics in considerits role in populationdynamics, examining is discussedbelow; extent thiscan be realizedin practice between theform oftherelationship role of popu- particular population the central herewe wishonlyto emphasize rateand population density. Usingtheseas founof future ratein the projection lationgrowth population growth recent studiesin to characterize dationswe thenattempt sizes. of the termsof three approachesto the identification rateand between feedback growth population Negative rate. of population growth forpopulation determinants condition density is a necessary population thecauses ofvariation In practice, thismeansstudying (Turchin1999), and Sinclair(1996) has sugregulation variation growth rate,attributing observed as occur- in population regulation population gestedthatwe recognize whilebearing in mindthat sourcesofvariation, density to known rate is negatively ringwhen populationgrowth sources ofvariation maychangeovertimeand thespecific is dependence to thisview,density dependent. According to reviewthe extensive mechanism in space. We make no attempt negative feedback an explicit seenas providing population dynamics and on theoretical is below relatedliterature the population.When density whichregulates
Phil. Trans. R. Soc. Lond. B (2002)
Population growth rateand itsdeterminants R. M. SiblyandJ. Hone 1155 (a) 2.2 2.0 1.8~
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Figure1. Examples of the effects of environmental stressors. of temperature on populationgrowth rate= A of the (a) Effects grainbeetle Calandraoryzae(Birch 1953). The different lines represent different moisture contents.(b) Effects of the of siliconon populationgrowth availability rate= r of the diatomAsterionella (Tilman et al. 1981). (c) Effects formosa of dieldrin on populationgrowth rate= r of the cladoceranDaphniapulex.(After Daniels & Allan (1981).)
pH. When the niche is characterized at low population density and in the absence of predators, parasitesand interspecific competitors, it is referred to as the 'fundamental niche'.In thepresence ofpredators, parasites and interspecific competitors the set of pointsforwhichthe population growth rateis greater thanzerois reduced, and this set of points definesthe 'realizedniche' (Maguire 2. ENVIRONMENTAL STRESS AND THE 1973). ECOLOGICAL NICHE Birch's (1953) summary of his experimental results Environmental stressors can be defined as factors that, depicting the effects of environmental stressors on popuwhen firstapplied to a population,reduce population lationgrowth rate (figure 2a) looksverysimilar to figure growth rate (Sibly& Calow 1989; Hoffmann & Parsons 2b, and it is curiousthatwhileBirch'sworkis generally 1991). Examplesof stressors maybe climatic conditions, referred to in discussionsof the ecological niche, the foodquality, toxicants, and so on. The advan- explicit pathogens linkis rarely made. Birch(1953) concluded:'the tagesofexplicit operational definitions oftheterms 'stress' significance of thisinformation [i.e. figure 2a] is thatit and 'stressor' areobvious, and itis encouraging that ident- provides background experimental data forstudies on disical definitions are now used fromthe populationlevel tribution and abundance.The limits ofdistribution ofthe down to thatof molecular responses(e.g. animalwelfare beetles aredetermined, so faras temperature and moisture (Broom & Johnson1993) and stressproteins(Hengge- are concerned, by the combination of temperature and Aronis1999)). Some examplesof the effects of stressors moisture beyondwhichthe finite rate of increase(A) is on population growth rateare shownin figure 1. less than1'. He also showedthattheknown geographical At the individualand populationlevel the effects of distribution of the two beetle species conformed to the environmental stressors are commonly measured usinglife predictionsof the laboratorywork. A very similar table responseexperiments (Levin et al. 1987; Caswell interpretation of species distribution in termsof popu1989, 2001). The first trueexampleofthisapproach was lationgrowth rateis described by Caughley etal. (1988), Birch's(1953) classicstudyof the effects of temperature in whichtheedge ofdistribution is identified as occurring and wheatmoisture content on twospeciesofgrain beetles wherethe maximum value of populationgrowth rate is (figures1a and 2a). The approach has been much zero. Populations can however persist witha population developed bytheelaboration ofmatrix population models growth rate greater than zero if theyare maintained by (Caswell 2001), and in recentyears,increasing concern immigration ('sink'populations; Pulliam1988). abouttheenvironment has led to numerous studies ofthe An exampleof how the niche conceptcan be used in populationgrowth rate effects of pollutants(Forbes & practice is givenin figure 2c. The fundamental nichesof Calow 1999). thetreesshownoverlapin the central regionof figure 2c The combined actionofenvironmental stressors can be (Ellenberg 1988) but in nature, competition between tree thoughtof as defining an organism'secologicalniche. species restricts the occurrence of individual species as Although textbooks often treatthe conceptof an organ- illustrated. ism's ecologicalniche historically, in termsof Hutchinson's (1957) rectilinear definition of the niche, a more 3. THE FORM OF THE RELATIONSHIP BETWEEN straightforward approachis to define an organism's niche POPULATION GROWTH RATE AND as theset ofpointsin 'nichespace' wherethepopulation POPULATION DENSITY growth rateis greater thanzero (Maguire1973; Hutchinson 1978; figure 2b). The axes ofnichespace arephysical As we have seen,environmental stressors havenegative or chemicalvariablessuch as temperature, food size or effects on populationgrowth rate,and the same is true
food webs; foran introduction to thesesee Berryman et al. (1995) and Rees et al. (1996). We concludewithan exampleillustrating our ideas in practice, and some considerationof applicationsto conservation biologyand other fields of wildlife and ecotoxicology. management,
rateand itsdeterminants growth 1156 R. M. Sibly and J. Hone Population (a)

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Indeed the natureof the negative density. of population and population betweenpopulationdensity relationship rateis at the heartof populationecology.If the growth equationis thelogisthedescribing is linear, relationship analyses are built on this tic, and many theoretical Fowler(1981, 1987) has arguedon theoretiassumption. between thatrelationships grounds cal and someempirical are expectedto be rate and density populationgrowth above,forspecieswithlifehistories viewedfrom concave, and similar for largemammals convex likethoseofinsects, 3 species (see figure species,and linearforintermediate forexamplesof concaveand convex).Concave and conthanone respectto valuesless or greater vex correspond logistic 0 in the generalized forthe shape parameter ively 1987). equation(Eberhardt ecolin population importance Given its fundamental of the depenthatdata on the form ogy,it is surprising have only rate on density dence of populationgrowth thoughBerryman been plottedout and analysed, rarely No doubtthis (1999) and Turchin(1999) giveexamples. cannotbe seen without because the relationship is partly environin a fairly constant in density adequatevariation population ment;thusthebest evidencemaycome from recoveries after experimentalperturbations(Sinclair
3), 1996). Of the 25 cases we found(examplesin figure are linear,and in all but two of the 12 relationships was concave viewed from remainderthe relationship is considerable thatthere above (table 1). Note,however, 3), indicating (e.g. figure about each relationship scatter growth affect population besidesdensity factors thatother for does seemto be somesupport there rate.Interestingly, and not are the data conclusive, but Fowler'shypothesis, are (e.g. elkand sparrowhawk there are counter-examples beenprohas recently support notconvex).Further linear et al. 2002). There are videdby studiesof birds(Saether in betweenA and density, also studiesof therelationship et al. 2000), Cincluscinclus(Saether thedipper for example equation,A has to be but to relatetheseto the logistic logetransformed. dependencecan be expected density a priori Although longterm(Sinclair1996), thatpersist in realpopulations dependencein real of density the operation recognizing A datasetshas been the subject of much controversy. applying have been performed numberof meta-analyses birds different taxa,including to data from thesemethods and insects(Hassell et al. 1989; Greenwood& Baillie is suchstudy 1991; Woiwod& Hanski1992). The largest thatof Woiwod & Hanski (1992), whichanalysed5715
Population growth rateand itsdeterminants R. M. Sibly and J. Hone (a) 0.5(b)
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population density Figure3. Examplesof the formof the relationship betweenpopulationgrowth rate (r) and populationdensity. Linear in (a) magpiegoose and (b) elk; concaveviewedfrom relationships above in (c) meadow vole and (d) arcticgroundsquirrel; convexviewedfromabove in (e) wildebeest and (f) sandhillcrane. Sources in table 1.
time-series of447 speciesofmoths and aphidsin theUK, and found good agreementbetween three analytical methods whichdiffer in their assumptions abouttheform of density dependence, namelythose of Bulmer(1975); against N,. The generalconclusionof thesemeta-analyses is that the existenceof density dependencecan be established fromcensus data providedsufficient data are available. The objectivein analysing densitydependenceshould therefore be the discovery of the form of density dependence, and the effect, if any,of time-lags. The existence of time-lags can be investigated by addingterms such as into the of regression against N,_1 N, loge(N,,I/N,) (Turchin1990; Woiwod& Hanski1992; Berryman 1999;
Erb et al. 2001). Pollard et al. (1987) and simple regressionof loge(N, I/Ne)
and could producethe illusionof density dependencein invariant populations(Woiwod & Hanski 1992). Some authorsrecommend Bulmer'stestbut all methodshave and weaknesses(Lebreton & Clobert 1991; strengths Fox & Ridsdill-Smith 1996). An additional seriousconcern is thatfluctuations in environmental variables may obscuredensity effects and makeit difficult to locatethe positionsof equilibrium densities('densityvagueness'; Strong1986; Murdoch1994; Krebs 2002). 4. CONTRASTINGAPPROACHES TO IDENTIFYING THE DETERMINANTSOF POPULATION GROWTH RATE
Because so manyfactors affect population growth rate, it is nevergoingto be easyto separate their effects when Despite the successes of the meta-analyses, worries theyoperatesimultaneously. have used a varEcologists remainabout the effects of measurement errors and of ietyofmethods to study thecombined and relative effects fluctuations in environmental variables. None oftheexist- on population growth rate of determining factors. Here, ingmethods allowsfortheeffects ofmeasurement errors, we compareand contrast thethreemainapproaches that whichmayexaggerate the effects of density dependence, havebeen used to identify thedeterminants ofpopulation
rateand itsdeterminants growth 1158 R. M. Sibly and J. Hone Population rate and popubetweenpopulationgrowth Table 1. Examples of linearand nonlineardensity dependencein the relationship lationdensity. cases involving and original Some morecomplicated references shouldbe consulted. is in some cases provisional (Our classification can be foundin Berryman (1999) and Turchin(1999).) time-lags species linear cladoderanDaphniapulex treehole mosquitoAedestriseriatus annual plantSalicornia brachystachys guppyPoeciliareticulata semipalmata magpiegoose Anseranas Yellowstoneelk Cervus elaphus cuniculus European rabbitOryctolagus clupeaformis lake whitefish Coregonus red pine cone beetle Conophthorus resinosae ponderosae mountain pine beetleDendroctonus nisus sparrowhawk Accipter fieldvole Microtus agrestis concaveviewedfromabove cladoceranDaphnia magna wood mouse Apodemus sylvaticus melanogaster fruitfly Drosophila winter moth Operophtera brumata vole Chlethrionomys rufocanus grey-sided pennsylvanicus meadow vole Microtus darwini mouse Phyllotis leaf-eared maculatus cowpea weevilCallosobruchus marinecopepod Tisbebattagliai brushtail vulpecula possum Trichosurus Arcticgroundsquirrel Spermophilus pariyii plesius convexviewedfromabove wildebeest Connochaetes taurinus sandhillcrane Gruscanadensis reference Franket al. (1957) & Livdahl (1992) Livdahl (1982) and Edgerley Crawley(1990) Barlow (1992) Bayliss(1989) Coughenour& Singer(1996) Barlow& Kean (1998) Berryman (1999) Berryman (1999) Berryman (1999) Siblyet al. (2000c) Klemola et al. (2002) Smith(1963) Montgomery (1989) Turchin(1991) Roland (1994) Saitoh et al. (1997) Turchin& Ostfeld(1997) Lima & Jaksic(1999) Berryman (1999) 7a Siblyet al. (2000b); cf. figure Efford (2000) Karels & Boonstra(2000) Sinclair(1996) Berryman (1999)
generwith overlapping populations rateinwildlife growth For no explicit spatialelements. usually, ationsand with, the 'density we label thesethreeapproaches convenience and the'mechanthe'demographic paradigm' paradigm', as different istic paradigm'.These are best understood Intuitively reality. of a rather complicated simplifications determined rateis fully growth it is clearthatpopulation birthand death by the completerecordof age-specific the linkis made by theEulerrates,and mathematically of the linkbetweenpopuLotka equation.Exploration lifetablegivesthe rateand the age-specific lationgrowth and deathrates birth Age-specific paradigm. demographic as food supply per indidepend causallyon such factors stresenvironmental predation, burdens, vidual,parasite and some of these competition, sors and interference on population or indirectly Lookdensity. dependdirectly and at the linkbetweenthesecausal factors ing directly paradigm, rate givesthe mechanistic populationgrowth on thelinkbetween rate growth population and focusing these paradigm; density givesthe density and population and contrasted were identified by Krebs two paradigms can be undertaken (1995). Anyor all oftheseapproaches and modelling studies. experimental usingobservational, consider use of theseapproaches In thissectionwe first havebeenused in combion their own,and thenhowthey nation. discussedin ? 3 and illustrated The density paradigm,
effects on to describedensity in figure 3, aims primarily population growth rate,and is used to makepredictions taking account of population density,where detailed may be unnecessaryor mechanisticunderstanding data.It assumes, impossible becauseoflackofappropriate of important features of the environhowever, constancy suchassumpfoodsupply; where mentsuchas population ofwild as occursin mostpopulations tionsare untenable, (see ? 4b). approach is preferable animals, themechanistic (a) The demographic paradigm paradigm focuseson therelationship The demographic fecundity between growth rateand age-specific population and survival. rate is increasedby an Populationgrowth earlier. or survival, or by breeding increasein fecundity of the link between population Detailed examination is oftenmade parameters growth rate and demographic using populationprojectionmatricesas describedby other methods are also available Caswell(2001), although theclassicalEuler-Lotka equation(e.g. Lande employing is necessary of this to the derivation stableage structure rate growth supposedthatpopulation equationit is often Howwithout stableage structure. cannotbe estimated ever,Sibly& Smith(1998) have arguedthateven when theage structure is not stableand thevariousage classes are growing at different rates,populationgrowthrate
1988; Bumham et al. 1996; Calow et al. 1997). Because
Population growth rateand itsdeterminants R. M. Sibly and J. Hone
1159
Table 2. Examplesofwildlife populationdynamics, analysedto studydeterminants ofpopulationgrowth rate,usingone or more of the density, and mechanistic demographic analyses,and theircombinations. classification refers to whether an analysiswas or was not used.) (The yes/no density analysis demographic analysis no no mechanistic analysis no yes no exponential; largemammals (Eberhardt1987) yes
yes yes
no yes
logistic;magpiegoose (Bayliss 1989), sparrowhawk (Sibly et al. 2000c) numerical response;red ratio;wolf(Eberhardt & kangaroo(Bayliss 1987), Peterson1999), modified barn owl (Taylor 1994) numerical response;house mouse (Pech et al. 1999) modified Lotka; northern modified logistic; white-tailed spottedowl (Lande 1988) deer (Hobbs et al. 2000) modified Lotka; red fox (Pech modified logistic;kitfox et al. 1997) (White& Garrott1999)
defined as the solutionof the Euler-Lotkaequationstill provides a usefulindexof population growth, because it represents an appropriate weighted averageofthegrowth ratesof the different age classes. Many examplesof workwithin the demographic paradigmare described by Caswell (2001), and thisapproach has also been important in studies ofthenorthern spotted estimatesof fecundity and survivalobtained in markrecapturestudies (Lande 1988; Lahaye et al. 1994; Burnhamet al. 1996; Franklin et al. 2000; Seamans et al. 2001). The relative effects on populationgrowth rate (A) of proportional changesin fecundity and survival rateshave been examinedin elasticity whichwas reviewed analysis, in a seriesofrecent studies(e.g. Caswell2000; De Kroon et al. 2000; Easterling etal. 2000; Grant& Benton2000; Heppelletal. 2000; Saether & Bakke2000; Van Tienderen 2000; Wisdomet al. 2000). These studiescompared the contributions of fecundity and survivalto population in specieswith growth life differing in short-lived histories; speciesfecundity can makea greater contriproportional bution than survival,and the reversein longer-lived species.Elasticity is used alongside analysis observation of actual levels of variationin demographicparameters (Gaillardet al. 1998) to determine whichdemographic factors have mosteffect on population growth rate.In a similar vein Sibly& Smith(1998) have arguedthattraditional 'keyfactor' shouldbe redesigned analysis to identify thelife-history trait whosevariation has mosteffect on population growth rate. Spatial elementshave also been incorporated into efforts to explain in population variation rate.The growth contributions to population growth rateof in siturecruitment,survival and immigration can be estimated from mark-recapture studies,as describedformeadow voles lations for which emigration exceeds immigration are referred to as source populations;where the reverse we have sinks(Pulliam1988). Thomas & Kunin obtains, (1999) have demonstrated a graphicalmethodof repthe concepts. resenting
owl (Strix occidentalis caurina), in which A is related to
(Microtuspennsylvanicus) by Nichols et al. (2000). Popu-
(b) The mechanistic paradigm The mechanistic paradigm focuseson the relationship between population growth rateand variables such as climate, food availability, predatorabundance,pathogens and parasites, and competitors ('extrinsic factors'). Turchin (1999) provides an excellent discussion of whatwe can treat as variables: ideallyone might keep trackofthe fates of all relevantindividuals,but apart from the impossibility ofthis, there is often moreheuristic value in using summary variablessuch as 'numbersin each age class' and so on. Historically, the mechanistic paradigm was followed in early modelsoftheeffects of competition by Lotka and Volterra in the 1920s, of predation (Lotka 1925; Volterra1926), and of pathogens(Kermack & McKendrick 1927). Monod (1950) considered the between relationship population growth rateand resource in populations availability ofbacteria, and in an influential experiment Tilmanetal. (198 1) related population growth rateofthediatom Asterionella formosa to theavailability of silicon, whichdiatoms needto secrete their silicate 'shells' (figure1b). Later, in a theoretical synthesis, Tilman (1982) considered more generally the relationship betweenpopulationgrowth rate and the availability of resources. These ideas arevery similar to theformulations of ecologicalnichetheory and stressors discussedearlier. In thesimplest case, theeffect ofpopulation on density populationgrowth rate is replaced,in the mechanistic paradigm,by resourceavailability. A collation of the resultsof many studiesof mammals(table 2; Sinclair 1996) showedthatfood is veryoftena cause of density dependence.In these cases density may have no effects other thanthoseon foodavailability. We shallrefer to the betweenpopulationgrowthrate and food relationship as the'numerical availability response'(table2), although it is important to note thatnot all authors use the term thisway,as therehas been an evolution in its meaning sinceSolomon(1949) first used itto describe theincrease in numbers ofanimalsas their resources increased. Applicationto therelationship between population rate growth and foodavailability came later, via an intermediate step of May (1974, p. 83) who used the termto describe the effect of food availability on fecundity, and Caughley
1160 R. M. Sibly and J. Hone Population growth rateand itsdeterminants
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rate (r) plotting annual populationgrowth Figure4. Examples of the numerical responseof populationsto food availability, againstpasturebiomass (kgha-), exceptin (e) the x-axisis vole abundance and in (h) the x-axisis per capita food (b) red kangaroonextto KinchegaNational Park (a) Red kangarooin KinchegaNational Park (Bayliss 1987); availability. (d) western greykangaroonextto (Bayliss 1987); (c)western greykangarooin KinchegaNational Park (Bayliss 1987); = 0.72, p < 0.01);(f) feral (e) barn owl (Tyto alba)(modified from Taylor (1994);r2 Kinchega National Park (Bayliss 1987); (Krebs etal. 1999). taurinus) goat (Maas 1997); (g) feral pig (Susscrofa) (Choquenot 1998); (h) wildebeest (Connochaetes (a-d) Open circlesrepresent data not used in the estimation. of food avail(1976, p. 207) who described it as the effect abilityon the rate of amelioration of population decline. Later, the term was commonly used to describe the
relationship between population growth rate and food availability(May 1981). The divergenceis well illustrated by Caughley & Sinclair (1994): in ch. 10, p. 172 theyuse
Population growth rateand itsdeterminants R. M. Sibly and J. Hone
1161
the Solomon definition and in ch. 6, p. 75 theyuse the population growth rate definition.The relationship between theseconcepts is considered & Krebs by Sinclair (2002). Methods of analysisof the numerical response weredevelopedin particular by Caughley(e.g. Caughley 1976, 1987; Caughley & Lawton1981; Caughley & Krebs 1983), and priorto and subsequent to his deathin 1994 his workhas muchinfluenced the development of mammalianecology, in Australia and New Zealand. especially Examples of the numerical response,plotting populationgrowth rateagainstfood availability, are shownin 4. Note that as food availability figure increases, population growthrate generally increasesto a maximum. Availability is availability to individuals, and is not always best measured foodsupply(Abrams by thepopulation & Ginzburg2000). If the populationis food limited, for it maybe moreappropriate instance, to dividethepopulationfood supplyby populationdensity (see ? 4d and ? 5). In addition to theexamples in figure 4, positive generally nonlinear relationships between population growth rateand foodavailability havebeenreported for European
rabbit (Oryctolagus cuniculus;Pech & Hood 1998), red fox
decadesduring themiddle1900s,as described by Sinclair (1989, 1996), Krebs (1995) and Kingsland(1996). The debatewas partly about approaches and partly about differencesin terminology and understanding, especially limitation versusregulation (Sinclair 1989, 1996). The morerecent on biological emphasis mechanisms has shed new lighton population dynamics (Bjornstad & Grenfell 2001). (c) Analyses of demography and density Density and demography arelinked in studies ofdensity dependence on mortality, operating survival or fecundity; k-value fallintothiscategory analyses as k-values aremeasures of mortality rates (see Sinclair (1989, 1996) for reviews of k-valueanalyses).Densitydependenceof fecundityis studiedwithink-valueanalysisby positinga maximum possiblefecundity, and treating observedfecundities as falling short in consequence of'mortality'. This while awkward, manoeuvre, is of course realistic in the case of abortions. Therewouldseemno reasonnowadays notto examine therelationships between life-history traits, andpopulation density ratedirectly growth (Sibly& Smith 1998). For instanceif we writer forpopulationgrowth rate,x fordensity and b and m fortwo independent lifehistory traits, then
dr ar db dx ab dx ar dm am dx
(Vulpesvulpes;Pech & Hood 1998) and house mouse

(Mus domesticus;Pech et al. 1999). A positive linear
betweenthe annual percentage relationship population of a barn owl (Tytoalba) populationand abungrowth dance of voles (Microtus theirmain food,was agrestis), reported by Taylor(1994) and thisis converted in figure 4e to a relationship betweenpopulation rateand growth vole abundance. In these examplesof the mechanistic paradigm,density,previously seen as a surrogateof resource availability, has been replacedby a direct measure of theavailability of food. In other studies of the numericalresponse, food availability is replacedby a surrogate, such as rainfall. Exampleshavebeen reported forredkangaroo (Caughley etal. 1984; Bayliss1985; Cairns& Grigg1993; McCarthy 1996), Pacificblack duck (Anas superciliosa) and maned duck (Chenonetta & Holmes 1988), magpie jubata; Briggs goose (Bayliss 1989), feral buffalo (Bubalus bubalis) (Freeland& Boulton 1990; Skeat 1990) and feralcattle (Bos taurus)(Skeat 1990), feralpig (Caley 1993) and house mouse (Brown & Singleton1999). Lebreton& Clobert(1991) urgecautionin simpleregression analysis oftheeffects ofenvironmental variables, becausealthough estimates of slope are notbiased,their variances are,and thisleads to problems in significance testing. The above examplesof themechanistic paradigm have been observational or correlative studies.Stronger inferences of cause and effect can be obtainedusingexperiments.The effects on populationdynamics of extrinsic factors havebeen studied in field-based such experiments, as addingfoodor removing predators (thesnowshoe hare trolling pathogens (the red grouse(Lagopuslagopus) and (1998)). Thereis considerable scope forfurther testing of the cause and effect basis ofrelationships in themechanisticparadigm withsuch experimental studies,especially therelationship between population growth rateand food availability (Eberhardt 1988). Controversy between the supporters ofthe density and mechanistic paradigms dominated population ecology for
(4.1)
This showshow changesin density (dx) whichchange life-history traits (e.g. dm) result in changes in population rate (dr). In practice, growth dm/dx would be measured as the regression coefficient in, for example,a k-value analysis. The contribution thismakesto changing populationgrowth rateis givenby thesensitivity ofpopulation growth rateto the life-history trait(ar/am). Formulaefor sensitivities are available for many life histories(e.g. Caswell 2001; Siblyet al. 2000a), calculatedby implicit differentiation of appropriate formsof the Euler-Lotka equation. theeffect Alternatively, ofdensity on population growth rate actingthrough demographic parameters can be described in density-dependent Leslie matrix models & Clobert1991; Caswell 2001). (Lebreton The life-history stages at which density-dependent effects occur in mammals were reviewedby Sinclair (1996) (table 1). Density was foundto affect in fecundity overhalfthe largeterrestrial herbivores and largemarine mammals,and in some species had effects in the early juvenile in smallmammals phase. By contrast, and carnivorestheeffects ofdensity werefelt mostin thelatejuvenile phase. and density Demography have been linkedforwhiteequations(table 2) of Hobbs et al. (2000) whichassume of survival positiveeffects and fecundity on finite populationgrowth rate(A) and a linearnegative effect of density on recruitment (the net result of fecundity and survival to first reproduction). Detailed fieldstudieshave demonstrated thatdensity affects fecundity and mortality in reddeer(Cervuselaphus; Clutton-Brock & Albon 1989; Clutton-Brock et al. 1997) and Soay sheep (Ovis aries; Clutton-Brock etal. 1997; Milneretal. 1999). Lebreton & Clobert(1991) haveargued that it is moreefficient to anatailed deer (Odocoileusvirginianus) in the modifiedlogistic
(Lepus americanus)studies of Krebs et al. (1995)) or con-
nematode (Trichostrongylus tenuis)studies of Hudson et al.
1162 R. M. Sibly and J. Hone
rateand itsdeterminants Population growth (a)
ratevia its on population growth of density lysetheeffect parameters. on demographic effects Demography and density are used in population ofsmall dynamics to modeltheprobable analyses viability proin thesoftware In one implementation, populations. to makethe is theoption VORTEX (Lacy 1993), there gram and outputs dependent, density parameters demographic mean time rateand estimated growth includepopulation VORTEX has been used to assess the feasito extinction. to Scotland of reintroducing wild boar (Sus scrofa) bility 1997). (Howells& Edwards-Jones (d) Analyses of mechanisms and density abovein ? 4b calcudiscussed response' The 'numerical rateof food availgrowth on population latesthe effects be maysometimes availability and as notedthere, ability, by foodsupply thepopulation by dividing bestmeasured for (1996) reported Thus, McCarthy density. population betweenpopulation relationship red kangarooa positive ratio(a per capita rateand the resources/density growth (2001) found and Barlow& Norbury response), numerical between relationship in ferrets furo)a negative (Mustela ratio.These rateand theferrets/rabbit growth population model from Leslie's (1948) ratio derive ultimately analyses subsequently developed relationship, ofthepredator-prey & Lawton (1981) and Caughby May (1974), Caughley vein,Pech et al. (1999) ley & Krebs (1983). In similar a positive showedforthe house mouse (M. domesticus) effect of density and a negative of food availability effect on populationgrowthrate (table 2). The population relatedto elk was positively rate of Yellowstone growth relatedto density and negatively autumnprecipitation population (Coughenour& Singer 1996), and similarly rate of the San Joaquinkit fox (Vulpesmacrotis growth season relatedto annual growing was positively mutica) related to density (Dennis & Otten and negatively rainfall ofMcCarthy (1996) and ofBarlow& 2000). The analyses effect of food Norbury (2001) assumeda multiplicative of Coughand theanalyses of density, and thereciprocal enour& Singer(1996) and ofPech etal. (1999) assumed The finite rateof effect of food and density. an additive (A) of wolf(Canis lupus)populations populationgrowth related to theratioofwolvesper deer has been negatively & Peterson1999). All these 1998; Eberhardt (Eberhardt offood to producea measure for studies corrected density relative to abundance.If more animalswere availability to each,so there for thefood,lesswas available competing fortheresource. Density may,however, was competition rateadditional effects on population havenegative growth as a result ofinterference competition, to thoseofresource in ? 5. This is discussedfurther competition.
1 0 10 20 30 40 50
vole abundance (b) 60 50
40
30 20 i 10 0 10
20
30
40
50
vole abundance Figure5. An exampleof use of the combineddemographic and mechanistic paradigm.(a) First-brood youngbarn owls fledged per yearper breeding pair plottedagainstabundance of breeding adult barn owls of voles. (b) Annualmortality and vole abundance. (After Taylor (1994).)
rateoftheowlswas growth on population foodabundance owl spotted ofthenorthern 4e). In a study (figure positive from rate (A) was estimated growth the finite population rates with these demographic and recruitment survival rates influencedby climate and/or habitat features was notestimated. etal. 2000). Food availability (Franklin
(f) Combined analyses of demography, mechanisms and density and factors of trophic showsthe effects A fullanalysis growth and hence on population on demography density natalensis, rate (table 2). For instancethe rat,Mastomys on fecofrainfall bytheeffects has dynamics determined on survival and density of rainfall and the effects undity of the kit (Leirs et al. 1997). The populationdynamics rateswhichare ageby demographic foxare determined White& Garrott (1999) showedthatreprostructured. related to food (leporid) ductiverates were positively on rainfall. in turn depended (figure 6a), which availability dependensity Juvenile 6b) was positively mortality (figure Canislatrans). Soay bycoyotes, dent(becauseofpredation by influenced dynamics sheep (0. aries)have population (e) Analyses of demography and mechanisms conditions in turn dependson weather which demography The demographicand mechanisticapproaches are kill are affec- and density(Coulson et al. 2001). Harsh winters thatdemographic parameters linked byshowing years ted by variablesfromdifferent trophiclevels,e.g. food young and old sheep but only in high-density 2001). & Grenfell rate of red fox has (Bjornstad The populationgrowth availability. The manymathematical modelsthathavebeen used to and on fecundity ofrainfall effects to separate been related rateand between growth population relationships on survival (table2; Pech etal. 1997). In a barnowlpopu- describe effects and density mechanistic Scotland,Taylor (1994) showedthat demographic lationin southern parameters, evaluation comparative (figure suggest a need fora moredetailed fecundity in vole abundanceincreased an increase rate (figure5b) and of the fitof the models. Steps have been made in this 5a), decreased adult mortality of increasing direction, such as the comparative The net effect mortality. by assessing analysis decreasedjuvenile
Population growth rateand itsdeterminants R. M. Sibly and J. Hone (a)

500
1163
4 S 4
0 (b) 80
60
10
leporid abundance _ -~
~~~
0 0 0 0
640 s 0~~~~~~~ 40 ,> 20 0

0 S 0
0.5
1.0 kitfoxdensity
1.5
2.0
(b) Results and discussion ratedecreasedas density Population growth increased, the expected density-dependent response (figure7a). Population densityalone did not account for all the observed because populationgrowth variation, however, ratewas higher at thehigher foodconcentration (crosses above circlesin figure7a). This is readilyunderstood because individuals livingat higher food availability are goodness of fitusing coefficients of determination (r2) to and expected grow in reproduce faster, resulting higher (waterbuffalo and feralcattle(Skeat 1990), feralgoats rate. growth (Capra hircus;Maas 1997), red kangaroopopulations population The numerical responses of population growth rateto (McCarthy1996), Mastomys rat (Leirs et al. 1997) and food availability(figure 7b) show that populations thehouse mouse (Pech et al. 1999)). An alternative is to use an information theoretic model-selection procedure declined (populationgrowthrate< 0) when food per copepod was low, but increased (population growth (kitfox;Dennis & Otten2000). rate> 0) whenfoodavailability was higher. The increase in population ratewith growth foodsupply was notlinear, 5. CASE STUDY because as food increased, the copepods showeddiminto transform ishing ability extra food into further popuThe following exampleillustrates someoftheideas dislation When the growth. is relationship linearized a using cussedin thepaperso far, including density dependence, (figure 7c), it appearsthatwhilefood the numerical responseand the actionof environmental log transformation (foodper copepod) accountsfora greatdeal factors. The case study is based on theresults ofan experi- availability in populationgrowth rate,thereis still mentintothedynamics ofa marine copepod,Tisbe battag- of the variation some unexplained variation: note the crossesbelow the liai. Whenthedata werepresented by Siblyetal. (2000b) 7c. The combinedeffects on population theywereanalysed solelyin terms of density dependence circlesin figure rateof foodavailability, preyspeciesrichness and and environmental factors. Here, we analysethenumeri- growth the data population of density, were figure 7c, analysed by cal response, and showthatsomeofthenegative effects of the multiple regression, regression equation being population are due to density partitioning offoodbetween It turns competitors. out,however, thatinterference com- population rate growth petition further restricts access to resources and produces = -2.89 + 1.461oglo(food per copepod) (5.1) additional on population negative effects growth rate.The + 0.43 preyspecies richness -0.24 density. an exampleof analysis in termsof mechstudy provides anismand density.
Figure6. An exampleof the combineddensity, demographic and mechanistic rate of kit paradigm.(a) Adultreproductive foxand the abundance of leporids,theirmain food. (b) Juvenile The mortality (%) of kitfoxand kitfoxdensity. solid line and solid pointsdemonstrate density-dependent caused by predation mortality by coyotes.The open circles show density independenceassociatedwithothercauses of White& Garrott(1999).) juvenilemortality. (After
each appliedfor11 weeksto 10 replicate centration), labof the marinecopepod T. battagliai. oratory populations Food was either the alga Isochrysis galbana,whichalone will sustaincultures or a mix of two algal indefinitely, species, I. galbana and Rhodomonas reticulata. Each food was given at two concentrations (1300 and 3250 pug C 1-1), replaceddaily.Each Tisbe population was at low density founded twopairs),and surviving (usually copepods were transferred daily to a duplicateculture plate containing 10 ml of freshly preparedtestsolution. Population biomasswas calculatedas the sum of the dry of all age classesof copepods.Population weights growth rate(r) was estimated as thenatural logarithm of (biomass in week t + 1)/(biomass in week t). Further detailsare givenin Williams(1997) and Siblyet al. (2000b). In analysing thenumerical response a realistic measure of food availability is needed (? 4b and ? 4d). Here, we use foodper copepodbecause carrying increased capacity withpopulationfood supplyin this experiment linearly (Siblyet al. 2000b), suggesting thatthe copepods ate all thefoodsupplied to them, at leastat higher densities. The amount of food available to each copepod ('food per calculated as thepopulation copepod') was therefore food supplydividedby the copepod population biomass.This approachto measuring food availability when predators eat all thefoodsupplied was introduced byLeslie (1948).
The multiple regression was highly significant (F3,303 = 128.1; p < 0.0001; rdj1 = 56%). In theregression, prey species richnesswas 1 or 2, densitywas log10 (a) Methods A factorial experimental designwas used, comprising (copepod biomass) and otherpredictors weredefined as two factors (prey species richness and food coninfigure 7. Statistical significance ofregression coefficients
(a) 2
C
oneprey species
+ +2
++O + ++
twoprey species
+
o
-1 0.5 1.0 1.5 2.0
0
0.5 density (b) 1.0 1.5 2.0
-~~~
2
++ 0+
2 1 -2
tb 0
-22 ?~~~~~~
0++ 0
-1~
0
~ ~ ~ ~ ~ ~~~~~~200 400 600 800 0 foodpercopepod 200 400 600 800
(c) 1 0
0+
I
2 ~~~~~~++0 + +0
+++
1~~~
-2
1.5
2.0
2.5
3.0
-2
1.5
2.0
2.5
3.0
foodpercopepod logio of populationgrowth rate (r) in Tisbebattagliai. Figure7. The determinants rateper week is plottedin Populationgrowth relation to (a) density, measuredas log1ocopepod populationbiomass,,ug;(b) food availability, measuredas food supplyper unitbiomass of copepod, ,ugC 1-1 jig-'; (c) as (b) withfood per copepod transformed to loglo on the x-axis.Food was either the alga Isochrysis galbana (left-hand panels) or a mix of two algal species (I. galbana and Rhodomonas reticulata, right-hand were: crosses,3250 ,ugC l-1; circles,1300 pLg C 1-1. panels). Food concentrations were food per copepod: t300 = 11.05, p < 0.0001; prey species richness: t300= 8.46, p < 0.0001; density: t300= -2.02, p < 0.05. Plots of residuals against predictor variables show no indication of departure from model assumptions and there was no evidence of serial correlation (Durbin-Watson statistic1.81). The population's food supply is shared between its members througha process of resource competition.This is why we assess food availabilityby 'food per copepod'. The additional negative effectsof density on population growthrate of T. battagliaicould occur because of interference competition influencing reproductive performance, survival or somatic growth or foragingefficiency. Crowding is known to increase swimming activityin T. battagliai, with an associated increase in energy costs (Gaudy & Guerin 1982) possiblyas a resultof antagonism between larvae (Brand et al. 1985); crowding is also known to reduce reproductiveoutput and depress larval viability(Fava & Crotti 1979; Zhang & Uhlig 1993) and to influencethe sex ratio froma female bias at low density
to a male bias at high density in T. holothuriae (Hoppenheit 1976; Heath 1994). Negative effects of population densityon population growthrate could occur in nature because of density-dependenteffectsof predators, parasites, pathogens, interspecific competitorsand mutualists,but theywere excluded in this experiment. We thereforeconclude that the negative effectsof density, additional to effects throughfood availability, were caused in this experimentby interference competition. A graphicalmodel of how food availability, densityand prey species richnessjointlyaffectpopulation growthrate in this example is given in figure8. Note that population growthrate is related to percapita food availability in contrast to the numerical responses of figure4, which were not per capita relationships 4h. The results except in figure suggest that the ratio model of Leslie (1948) should be modifiedto incorporateothertrophiceffects, such as prey species richnessand interference competition.For a given level of per capita food availabilityin the present study, increasing interferencecompetition reduces population
Population growth rateand itsdeterminants R. M. Sibly and J. Hone (a)
1165
2.0 1.5
1.0 A
1
-
0.5 0 200 -0j5 -1.0 l c) i = (b) -1.5 -2.0-i 400
100
600 800 1000 foodpercopepod
2.0 1.5- /
1.0-
rateto wildlife management and other topicsinpopulation ecology.The threeclassicalapplications of conservation, harvesting and pestcontrol aim to increase, maintain and decreasepopulationgrowth rate,respectively (Caughley 1976, 1977). Each of these applications also affects the frequency of populationgrowth distribution rate (Hone 1999). Of generalconcernin conservation biologyis populationperformance at low density, whichis the danger zone forendangered species.Population growth ratemay be submaximal when density is low because of the difoffinding ficulty mates(theAlleeeffect; etal. Courchamp 1999; Stephens& Sutherland1999) or because of an ofpredation effect on a prey wherein thepredpopulation, ator has a type III functional response (Sinclairet al. 1998). An exampleofa declinein population growth rate at low densitywas describedfor pronghorn antelope thought thatan Allee effect might have keptthe North Atlantic whaleat low density, right butthispossibility has recently been eliminated by demographic analysis (Fujiwara & Caswell2001). Another potentially important issue in conservation biologyis the effect of inbreeding on population growth. is debateaboutthe Although there practical of inbreeding significance in wild animalpopulations(Caughley1994; Gundersen etal. 2001), it is easy to see thatit could be important in smallisolatedpopulations, because we knowfrom theEuler-Lotkaequation thatany reductions in fecundity and survival caused by inbreeding would necessarily depresspopulationgrowth rate. Inbreeding is includedas a determinant of populationgrowth ratein population viability analyses such as VORTEX (Howells & Edwards-Jones 1997). These topics in conservation focuson thesmallpopulation biology size beinga cause of conservation problems (Caughley1994). Also ofinterest are thequestions as to whythepopulation is small,whyit declined,and whatmanagement can do to reverse the decline. Another commonthemein conservation is the biology declineof populations because of highmortality caused by people. The rateof population growth of populations subjectto intensive illegalharvest, such as the African (Diceros has been relatedto the effort bicornis) expended in reducing or preventing poaching(Leader-Williams & Albon 1988). The dynamics ofseabirds, such as thewanderingalbatross(Diomedeaexulans),are influenced by fishing activities. For instance, Weimerskirch etal. (1997) showedthatthe rateof population declinedependedon the cumulative numberof longlinefishing hooks set in albatross areas.These studies foraging use themechanistic approachto identify the causes of population declines. Also of generalinterest are the effects of habitatloss, and research here aims to identify the main features of wildlife and to establish habitats, thewaythey affect distributionand abundance,i.e. to characterize each species' ecological niche.Traditionally suchresearch has involved measuring a largenumber ofhabitat features though typicallynot including food,predators, pathogens and competitors.In an encouraging effort to advance wildlife habitat studies and hencewildlife management in general, Morrison(2001) recommended a changeto a focuson resources such as food,and theireffects on survival and
elephant (Loxodonta africana) and black rhinoceros (Antilocapra americana; Sinclair 1996). It had been
1.5~~~~~0
0.50 200 400 600 800 1000 foodpercopepod
-1.0 -
-1.5 -2.0 Figure8. Graphicalmodel showing how food availability (food per copepod), density and preyrichness together determine populationgrowth rate.The curvesare derived fromequation (5.1). Densityhas an indirect directly effect via food availability, and a directnegative effect through interference illustrated here by the contrasting competition, solid and dashed lines (solid line, copepod biomass= 1; dashed line,biomass= 100). (a) refers to one and (b) to two preyspecies.
growth rate (compare solid and dashed lines) and increases theleveloffoodavailability neededto support a stable(population growth rate= 0) population. Increasing prey speciesrichness increases population growth rateand lowersthe level of per capita food availability needed to supporta stablepopulation(figure 8a,b). This graphical model illustrates our results, and showsthatthe densitydependentand the mechanistic approachesof figures 3 and 4 are not incompatible. Instead,figure 8 showsthat the two approaches are complementary and can be combined by joint analysisof the effects of mechanism and thusclarifying themechanistic density, linksthatconnect density, food availability and population growth rate. 6. APPLICATIONS IN CONSERVATION BIOLOGY, WILDLIFE MANAGEMENT, ECOTOXICOLOGY AND HUMANDEMOGRAPHY A better of how to estimate understanding population growth rate,and whatdetermines population growth rate, is fundamental to the application of populationgrowth
In thisrespect ideally from independent sites/populations. oftheclassicearly itis interesting to revisit thepredictions they rediscovered paperofPearl& Reed (1920), in which thelogistic equationand appliedit to data on the size of the humanpopulationof the continental United States. They implied that the logisticequation resultsfrom namely humancompetition forthemeansof subsistence, thecarfood,clothing material and fuel.Theycalculated United States as 197 rying capacityof the continental then million, but noted thatat the levelsof production it would be necessary abouthalfthe obtaining to import low now,but food supply.Theirprojections look a little this can be attributed to technological advances.There would seem to be a need formore studiesof the type thematch initiated by Pearl& Reed (1920) thatconsider is verylow, as in if theirrmax values are higher.When rmax resources and individa sustained between globallevelsofsustainable long-lived specieslikewhalesand elephants, ual levelsofhumanconsumption (cf.Lutz & Qiang2002). harvest may not be economic(Clark 1973; Caughley& based projection for theglobalhumanpopulation in the effects of environmental A recent Sinclair1994). Variation on existing harvest (Bayliss1989) indicatesthat factors lowers thelevelofsustained downwardtrendsin fertility willslowoverthecoming decades,and growth and of course increasesthe variationof the harvest population effects ofharvesting peak in ca. 2070 at a population size aroundninebillion & May 1977). Negative (Beddington in white- (Lutz et al. 2001). ratehave been described on population growth can be foundin Further examplesof modelvalidation etal. 1991), mallard(Anas taileddeerin Ontario(Fryxell themodelling ofa Mastomys rat(Leirsetal. 1997) and of in North America (Reynolds & Sauer platyrhynchos) (Pech et al. 1999). In house mousepopulation dynamics 1991), and moose (Alcesalces)in Norway(Solberget al. each study, observed rodentabundanceswerecompared 1999). froma model of dynamics constructed is another fieldwherepopulationgrowth withpredictions Pest control thesamesitebutat an earlier timeperiod. rate is central (Hone 1994); indeed, several early usingdatafrom wherever essential and validation are clearly populationecologists(e.g. Howard, Fiske, Nicholson, Model testing of modelprojections. thereliability pro- possibleto increase Andrewartha and Birch)studied pests.A pestcontrol if pest abungrammemay become a sustainedharvest dance is reducedand keptat low levels.Pest populations 7. CONCLUSION may, however, adapt to control, for example, by to rate of The resistance developpesticides. developing thesisis thatpopulation rateis the Our central growth rateand mentofresistance growth dependson population variablelinking the variousfacetsof population unifying interval (Dobson & May 1986). generation density ecology;thus analysesof populationregulation, ratecan also be seen as thekeyuni- dependence, growth Population and resourceand interference competition in ecotoxicology etal. 2001). Thus, (Walker fying concept of environmental are all bestundertaken theeffects stress chemicals that with populationgrowthrate as the responsevariable. can be defined as environmental pollutants levelsand have the potential Throughout, exceed normalbackground roleofstatistical we haveemphasized thekey or mortality to adversely affect rates,with analysesof observational birth, growth or experimental data, and we in population rate.Defined hopein thefuture reduction growth consequent to see morestudies analysed bymultiple case of regression in this way, pollutantsappear as a particular to estimate and and alliednonlinear techniques theimpactof distinguish environmental stressors (see ? 2). Although on population rateof food the effects growth at on organisms is studied within ecotoxicology pollutants environmental and so on. stressors, density availability, from different biochemistry through Effects levels, organizational within be treated oftime-lags can also,inprinciple, each withits own measureof pollutant this framework. to communities, Such analysesare needed not only to it can be arguedthatpopulation ratepro- improve growth effect, oftheunderlying thequality science,but also to the increasethe realismand accuracyof prediction Afterreviewing vides the best summarystatistic. in key Forbes& Calow (1999) conclude appliedareas such as conservation, literature, experimental wildlife management that population growthrate is a better measure of and ecotoxicology. in controlling, Much practical concern than are individual-level effects, managing responsesto toxicants or conserving has to do withlimitpopulations because it integrates complex interactions ing,managing potentially one key or encouraging growth; population traitsand providesa more relevant indicator among life-history is population ofeffect in suchenterprises growth & Sutherland measureof ecologicalimpact.By contrast, stillmanyunresolved issuesin rate.There are, however, in build- identifying Norris(2002) suggest thatthereare advantages in populationgrowth the causes of variation to a popu- rate,stemming the levelof individual behaviour ing up from largely the fromthe need to distinguish rate. growth lationlevelperspective on population effects ofmanycausal factors withdistinctly limited dataof popu- sets.Much challenging Wherecomplexmodels of the determinants research remains. purposes, rate are used for management lation growth how do is clearly of crucialimportance: modelvalidation forgenerously We thank T. D. Williams and M. B. Jones For we know we can believe the model's predictions? allowing us tO use the Tisbe data,M. Rees forpointing us useful data sources, M. Begon,P. Doncaster, P. field datasetsare needed, towards long-term model validation,
to demoSuch a focus would be a shift reproduction. analysisas describedabove, and if graphic-mechanistic of would lead to greaterunderstanding implemented rate. mechanisms growth determining population has twoother ofstudy, harWildlife fields management similar and pest control. These are conceptually vesting (Caughley1976, 1977), beingbased on ideas ofreducing in one responses compensatory abundanceand expecting harvest The sustainable and survival. or bothoffecundity populationgrowingaccordingto logistic of a wildlife is a function of abundance, capacity and carrying growth rateof population the maximum growth (rmax; Caughley 1977). Species at the same abundancehavingthe same sustainable annualharvests have higher carrying capacity
Population growth rateand itsdeterminants R. M. Sibly and J. Hone Caley, C. J. Krebs,A. R. E. Sinclairand M. Walterforcommentson an earlier draft manuscript, and J. C. Whittaker and H. Grubb of the Department of AppliedStatistics, University of Reading, for statistical advice. We also thankThe Royal Societyand theUniversity ofCanberraforfinancial assistance.
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J. Wildl. Mngmt 65, 425-431.

Population Growth Rate

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Population Growth Rate

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Population Growth Rate and Its Determinants: An Overview Author(s): Richard M.

E THE ROYAL SOCIETY

29 August 2002 Publishedonline

Population growthrate and its determinants: an overview

*Author forcorrespondence (r.m.sibly@reading.ac.uk).

rateand itsdeterminants growth 1154 R. M. Sibly and J. Hone Population

in oroutofthepopulation, is no migration and there rates, growth occurs;in thismodel,population so exponential

dieldrin concentration (jig 11)

rateand itsdeterminants growth 1156 R. M. Sibly and J. Hone Population (a)

for forest toodry

8 112 24 20 16 (a) temperature 28 32

fresh; shsiver (b) damp / 0.00. 0.

hombeam common oak

alder ~~~~~~~~~~hairy birch acidic acidic very

elm neutral alkaline

Population growth rateand itsdeterminants R. M. Sibly and J. Hone (a) 0.5(b)

-0.5 , 1000000 * 1500000 , 80000

Population growth rateand itsdeterminants R. M. Sibly and J. Hone

owl (Strix occidentalis caurina), in which A is related to

(Microtuspennsylvanicus) by Nichols et al. (2000). Popu-

1160 R. M. Sibly and J. Hone Population growth rateand itsdeterminants

(a) 0.4 -0.60.2 -0 2 -0.2? -1.0 -0.4 00 40 0 600 800 1000

800 1000 1200

0.6 0.4 0.2 0 -0.2

0.8 0.6 0.4 400 600 80 1000 0.2 -0.2 -

-1.0 (e) 0.8

0.8 00.6-1.0 0.2 A -0.6-06-0.2 -0 6t -0.8 --0.4 0 1.2

0 250 300 350

150 200 250 300

Population growth rateand itsdeterminants R. M. Sibly and J. Hone

(Vulpesvulpes;Pech & Hood 1998) and house mouse

(Lepus americanus)studies of Krebs et al. (1995)) or con-

nematode (Trichostrongylus tenuis)studies of Hudson et al.

1162 R. M. Sibly and J. Hone

rateand itsdeterminants Population growth (a)

vole abundance (b) 60 50

Phil. Trans. R. Soc. Lond. B (2002)

Population growth rateand itsdeterminants R. M. Sibly and J. Hone (a)

640 s 0~~~~~~~ 40 ,> 20 0

Phil. Trans. R. Soc. Lond. B (2002)

1164 R. M. Sibly and J. Hone Population growth rateand itsdeterminants

~ ~ ~ ~ ~ ~~~~~~200 400 600 800 0 foodpercopepod 200 400 600 800

Population growth rateand itsdeterminants R. M. Sibly and J. Hone (a)

0.5 0 200 -0j5 -1.0 l c) i = (b) -1.5 -2.0-i 400

600 800 1000 foodpercopepod

0.50 200 400 600 800 1000 foodpercopepod

1166 R. M. Sibly and J. Hone Population growth rateand itsdeterminants

1168 R. M. Siblyand J. Hone

Population growth rateand itsdeterminants

J. Wildl. Mngmt 65, 425-431.

Phil. Trans. R. Soc. Lond. B (2002)

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