Contributed
TheUseofSpeciesAccumulation
forthePrediction
Functions
ofSpeciesRichness
JORGESOBERON M.
Centrode Ecologia
UniversidadNacional Autonomade Mexico
Apdo. Postal 70-275
Mexico D. F.
JORGELLORENTEB.
Facultadde Ciencias
UniversidadNacional Autonomade Mexico
Apdo. Postal 70-399
Mexico D. F.
Introduction
Faunisticand floristicstudies oftenreveal that as the
timespentcollectingincreases,the numberofnew spePaper submittedSeptember26, 1991; revisedmanuscriptaccepted
March 9, 1992.
480
ConservationBiology
Volume 7, No. 3, September1993
El uso de funciones
de acumulacion
de especiesparala
prediccion
de la riguezade especies
Resumen: Se presenta una teoria estoca'sticade la acumulacion de especiesnuevas en inventariosfloristicos
ofaunisticos.Se obtieneny resuelvencasos particulares de las ecuaciones diferencialesque relacionan el tamafio esperado de
las listasy su variancia con el tiempodedicado a la colecta
Los casos particulares correspondena diferentesmodelos de
como laprobabilidad de aniadiruna especie nueva a la lista
cambia con el tiempo,el tamafiode la lista; la complejidad
del area y otrosparacmetros.
Se discutenejemplos con datos
de campo de mariposasy mamiferosy se argumenta que el
contar con ecuaciones que relacionen el esfuerzode colecta
con el tamafiodel inventariopuedeser uztilparapropositos
conservacionistasporque se podran formalizar las comparaciones entre inventarios y porque tales ecuaciones
pueden tenerun valorpredictivoal extrapolarpara obtener
los valores asint6ticos de las listas. Tambie'nse discute la
conveniencia de los diferentesmodelos a distintas situaciones de campo.
& Ilorente
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Prediction
ofSpeciesRichness 481
TheModel
A simple model of the process of accumulatingnew
species is the pure birthprocess (Bailey 1964; Pielou
1969). This model assumes that the systemis represented by states,in our case the numberof different
species,and thata suitabletimeincrementmaybe chosen such thatthe systemeithermoves to the next state
or remainswhere it was at time t. In symbols:
prob(ij
prob(i j)
+ l)At = X(,t) At
&t = 1 -X(j ,t)At.
(1)
P(i)t X(jt).
(2)
(3)
ptj) X(,t), (4)
LinearDependenceon j
The simplestcase is when the collectingfunctiondepends linearlyon the size of the listand the parameters
are constantin time:
X(j,t)= a - b j,'
(5)
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Volume 7, No. 3, September1993
482
ofSpeciesRichness
Prediction
Soberon& LUorente
(6)
(7)
(9)
Equation6, we obtainS(tk)
Exponential
Dependenceon j.
A slightlymore complex model forthe collectingfunction ariseswhen we assume thatincreasingthe size of
thecollectiondecreases theprobabilityofaddinga new
species in a nonlinearway. The simplestsuppositionis
an exponentialdecrease:
(11)
(10)
(12)
The ClenchEquation
The Michaelis-Menten
equation used by Clench (1979)
can be derivedfromthemodelpresentedhere,bygoing
ofthecollecting
functions
discussed.
Table 1. Somestatistics
Exponential
,(Jt)
S(t)
Var(t)
tq
tk
Asymptote
a-bj
ab(1 - ebt)
S(t) ebt
l/bln[1/(1 - q)]
1/bln(1 + b/k)
a/b
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Volume 7, No. 3, September1993
Logaritbmic
ae bi
lz ln(1 + zat)
k - za/[(1 + zat) ln(1 + zat)]
Clencb
a + b/a[S(t)2 - 2j
at/(1 + bt)
q/[b(l - q)]
[(1 +
a/b
4bk)1/2
1J/2b
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Prediction
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2 bj/ a
(13)
2bj/a
(14)
or, equivalently,
X(j,t) = a + b2/a[at/(l
+ bt)]2
Substituting
eitherofthe above equationsin Equation3
and solvingyields
S(t)
a t/(l + b t),
Examples
Lamas et al. (1991) presentdata obtainedfroma 200person-hourscollection (during September 1989) in
the Pakitza biological station,Parque Nacional Manu,
Madrede Dios, Peru.Theyfittheirdata to the equation
of Clench and obtaineda verygood fit.They also estimated the asymptote(905 species) and calculated the
time required to reach different
percentagesof it. We
digitizedthe information
fromtheir Graph 1, and in
Figure1 and Table 2 we presenttheresultsoffitting
the
Clench,the exponential,and the logarithmicfunctions
to datafromLamaset al. ( 1991). The modelswere fitted
by the quasi-Newtonmethodprovidedby the package
STATISTICA(StatSoft1991).
It is clear thatalthoughthe data fitwell to each ofthe
functions,
theyextrapolateto verydifferent
numbersof
species. In fact,it is impossibleto choose the best ofthe
threemodelsbased solelyon the data set. To choose an
equation,one has to decide whichunderlying
collecting
model describes most accuratelythe particularsituation.For the threeequationsdiscussed above the models are (1) the probabilityof adding new species decreaseslinearlywiththesize ofthelist(Equation 5); (2)
addinga new species becomes more and more difficult,
butneverreacheszero (Equation I 1); and (3) theprobabilityof addinga new species eventuallyvanishes,but
fieldexperience increasesit (Equation 13).
900
800
700
600
a 500
C', 400
300
........
....;.-
20 0
O~~~~~~~~~~~~~
0
100
200
..................
300
........ .......
400
.............
..
...............
500
600
700
Person-Hours
Figure 1. Accumulation curvefor butterfliesin Pakitza Peru Data fromLamas et al. (1991). a correspondsto
the logarithmicequation, b to Clench's equation, and c to theexponential equation.
Conservation Biology
Volume 7, No. 3, September 1993
484
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ofSpeciesRichness
Prediction
ofthefourexamples.
statistics
Table 2. Regression
Atoyac2
Pakitza'
r.2
0.99
7.57
0.0085
890
0.96
6.64
0.0134
495
r.2
0.99
6.72
0.011
611
0.95
5.63
0.0155
363
a
b
asymptote
Clench
a
b
asymptote
Exponential
0.97
8.413
0.00675
0.99
8.869
0.00347
r.2
a
z
Logarithmic
Powdermilt'
Chajut3
0.967
2.88
0.035
82
0.986
1.073
0.0135
79
0.972
2.65
0.047
56
0.988
0.761
0.011
69
0.917
2.447
0.065
0.96
3.207
0.0356
Time units:
' person-hours '.
2person-days'.
3 nights '.
4person-hours '.
value is 979. Althoughthisextrapolationcovers an increase of more than 180% over the time intervalused
the models,and thisintervalincludes a nonforfitting
partofthe curve,thelog model predictsthe
asymptotic
correctvalue whithin15%.
In anothercase, Vargaset al. (1991) reportedtheir
sampling,over threeyears,of a large transect
butterfly
(300-2500 metersabove sea level) fromsemideciduous rainforestto pine forest.In Table 2 and Figure2,we
themodels.As in thePakitza
presenttheresultsoffitting
data, the three models provide excellent fittingsin
termsofexplainedvariance,displaysimilarresidualdisbut predictcontrastinglong-termbehavior.
tributions,
600
500
a) 400
2~00
o~~~~~~~~~~~~~~~~
00
100
200
300
400
500
600
Person-Days
Figure2. Accumulation curvefor butterfliesin Sierra de Atoyac,Mexico. From Vargas et al (1991). a corresponds to the logarithmicequation, b to Clench's equation, and c to theexponential equation
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As in thepreviousexample,and forsimilarreasons,it
is reasonableto assume thateitherthe log or Clench's
model maybe betterpredictorsof the futurebehavior
Theypredicta species increaseof
ofthesamplingeffort.
around 15% (Clench) or 20% (log) ifsample effortis
doubled to 300 person-days.The exponentialmodel,on
the otherhand,predictsan increase of only about 1%
which in thiscase seems unafterdoublingthe effort,
likelysmall.
Anotherexample is the listofbat species reportedby
Medellin(1986 and unpublished)fromthe Chajul Biological Stationin the Lacandon rainforestof southern
Mexico. The collectionsof bats have been ongoingfor
about seven years,usingmistnets at severalspots near
the station.Table 2 and Figure3 show the results.As in
the previous cases, variance explained by each model
and residuals are very similar.Accordingto Medellin
(personal communication),his methodsare well establishedand thearea,althoughveryrich,is relativelysmall
(a few hundred hectares), so the exponentialmodel
should apply.This predicts an increase of about 10%
afterdoublingthe samplingtime.
In our last example we reanalizedthe example provided by Clench (1979) to illustratehis species-time
formula.This studywas carried out for 13 years and
totaled820 hoursofcollectingand observingbutterflies
at the 2000-acre PowdermillNature Reserve in WestmorelandCounty,Pennsylvania.The list appears to be
withonlyone species added in
almostin theasymptote,
the lastfouryearsofdata. The resultsappear in Table 2
and Figure4. The nonlinearfitto Clench's model gives
Discussion
The use ofextrapolationsofspatialdata to estimatespecies richnessis not new (Kernshaw 1973; Palmer1990,
among others) and can be traced back to the classical
works of Preston(1948, 1962a, 1962b), Fisher et al.
(1948), and others.To our knowledge,however,extra-
80
70
60
50
CI)~~~~~~~D
G)~
40
3
~ ~ ~
0 k
1
u 04
....'......
~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~.
..........-...
............................
20
40
'.
'.
60
80
100
120
Nights
Figure3. Accumulation curvefor bats in Cbajul, Mexico. From Medellin (1986 and unpublished). a corresponds to the logarithmicequation, b to Clench'sequation, and c to theexponential equationr
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ofSpeciesRichness
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100
90
80
70
(
60
a,
50
tX
50
40
I,X
40
20
250
750
500
1000
1250
1500
Person-Hours
Figure 4. Accumulation curvefor butterfliesin PowdermillReserve,Pennsylvania Data from Clench (1979). a
correspondsto the logarithmicequation, b to Clench's equation, and c to the exponential equationo
apolationsover the timedomainhave not been systematically pursued by conservation biologists (Clench
1979; Miller& White 1986; Lamas et al. 1991).
One of thepotentialuses of such methodologycould
be to lend rigorto faunalinventoriesof areas.In poorly
collected sites,which oftenare importantforconservation purposes,reportinga numberof species may be
misleadingwithout some informationabout how far
fromcomplete such lists are. Eitherthe rates of accumulationof new species or an estimateof the percentage ofthe totalnumberis necessaryto makemeaningful
comparisons.Obviously,a place in which 80 species of
have been reportedwith 0.1 additionalspebutterflies
froma place withthe
is verydifferent
cies/person-hour
same 80 species and a rate of 0.01 additionalspecies/
person-hour.In orderto make such comparisonspossi(time/personand numberof persons) alble, the effort
located to the addition of new species should be
reported.It is clear,however,thatas with the size and
ofpersonsofdifferent
compositionof the list,the effort
expertisemay not be equivalent,thus hinderingcomparisonsbetween lists.It is also clear thattimein itself
is notwhatcounts,but how thistimeis distributedover
the seasons. For example 50 person-hoursduringthe
fromthe same 50 perdryseason maybe verydifferent
son-hourswell distributedover one year. We shall returnto thispoint later.
Predictingtherichnessofthefaunaofa site,giventhe
We
known accumulationcurve,would be interesting.
believe thatthe models presentedhere can be used to
thispurpose with some precautions.First,a sample biased eithertemporallyor spatiallyis useless forextrap-
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Soberon
Acknowledgments
We thankGabrielaJimenezforher help withthe graphs
and tables.Dessie Underwoodgave us some helpfuladvice. Town Peters made severalveryusefulcomments
and improvedour Englishsignificantly.
RodrigoMedel-
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Prdicton
ofSpecies
Richness
Sober6n
& Liorente
Appendix
To deriveEquations3 and 4, we beginwiththe definitions
of thefirst
two moments:
(7) =
(2)
Ejp(p)t
= Xj2p(j)
ConservationBiology
Volume 7, No. 3, September1993
dQf/dt=
d(2)/dt =
j dp()/dt
(Al)
j2 dp()/dt
(A2)
Substitution
ofthevalues ofdp()Idt givenby Equation2 yieldsequationsthatcan be simplified,
in the case ofAl, by addingand subtracting Xp(j -1 )X(f - 1) and thensimplifying
and,in the case ofA2, by
addingand subtracting
termsto completetheexpressionsTp(j-1 Xi
1)2 and :p(j - 1)( - 1)3. Furthersimplification
yieldsEquation
4.