G. Bronner* & J.

Meester
Department of Biology, University of Natal, King George V Avenue, Durban, 4001 Republic of South Africa

Monthly population estimates generated by five standard methods (numbers caught; direct enumeration;
Bailey's Lincoln index; Hayne's removal method; Jolly-Seber stochastic model) were compared using vari-
ation coefficients and cluster analysis. Assessments from the first three methods were the most similar.
Hayne's method apparently underestimated numbers when sample sizes were low, and overestimated when
numbers caught on different trapping occasions were dissimilar. The Jolly-Seber model apparently over-
estimated population size consistently. The inaccuracies of the three statistical models resulted from inherent
statistical and biological pitfalls, which render them less heuristic than the simpler enumeration methods. The
direct enumeration method is the best available when trapping data indicate unequal catchability and high
population gains and losses.

Vyf standaardmetodes (aantal gevang; direkte telling; Bailey se Lincoln-indeks; Hayne se uitvangmetode;
Jolly-Seber se stochastiese model) is gebruik om maandelikse bevolkingskattings te verkry wat met behulp
van variasie-koeffisiente en groepanalise vergelyk is. Ramings gebaseer op die eerste drie metodes het die
meeste ooreenkomste getoon. Hayne se metode het getalle onderskat wanneer steekproewe klein was, en
dikwels oorskat wanneer die getalle wat met verskillende vangpogings versamel is, verskillend was. Die Jolly-
Seber metode het bevolkingsgrootte konsekwent oorskat. Die onakkuraatheid van die drie statistiese mode lie
spruit voort uit inherente statistiese en biologiese tekortkominge wat hulle minder heuristies as die meer
eenvoudige telmetodes maak. Die direkte telmetode is die beste metode beskikbaar wanneer vangdata dui op
ongelyke vangbaarheid en hoe vlakke van bevolkingsaanwins en verlies.

'To whom correspondence should be addressed at: Department of Mammals, Transvaal Museum, P.O. Box 413, Pretoria,
0001

Introduction Table 1 Dates and trapping configurations

The accurate estimation of small mammal population used to sample Mastomys natalensis at
size is notoriously difficult. Most of the assessment Bluff Nature Reserve
methods available (reviewed by Caughley 1977; Flower-
dew 1976; Seber 1973) rely on certain assumptions which
are seldom satisfied. Since even small deviations from
these may render derived estimates misleading, mark-
recapture models are not particularly robust, and must
be used with caution (Smith, Gardner, Gentry, Kaufman No. of stations 20 100
Station interval 15 m 15 m
& O'Farrell 1975). Only when the truth of assumption is
Traps per station 3 2
unequivocally demonstrated is the use of a particular
Sampling period 4 nights 4 nights
method justified. interval 4 weekly 4 weekly
As part of a demographic study of the multimammate duration March 1985 - January -
mice Mastomys natalensis sensu stricto (see Green, March 1986 March 1986
Keogh, Gordon, Pinto & Hartwig 1980) on an urban 2808 2400
nature reserve, it was necessary to monitor seasonal
changes in numbers. Five standard methods were used to
assess population size. This paper compares population
mediately behind the trapdoor. Traps were baited with a
estimates yielded by the various techniques, and com-
mixture of peanut butter, oats, currants and sunflower
ments on the heuristic value of each method. oil, set at dusk and cleared every morning.
Multimammate mice captured (on the last trapping
Methods occasion) were karyotyped as 2N = 32, and thus are re-
Sampling ferred to M. natalensis (Green et al. 1980). Individuals
The study comprised 12 line-trapping and three grid- were marked using the 1-2-4-7 toe-clipping system (P.
trapping trials undertaken between March 1985 and Cilliers 1972, unpublished) and released at the site of
March 1986 at Bluff Nature Reserve, Durban capture.
(29°55'S /30 59'E).
0
Trapping configurations and
sampling periods are given in Table 1. The traps used Estimation methods
were 320 x 70 x 60 mm PVC live traps modified from Assumptions commonly made by estimation methods
Willan (1979) to include a locking-pin situated im- are:
 mals (y-axis) to the cumulative total of animals marked
(1) animals do not lose their individual marks;
previously (x-axis). A line fitted by eye to a plot of these
(2) captures are correctly recorded as marked/
points (Figure 1) is continued to the x-axis, the abscissa
unmarked;
representing total population size. A regression analysis
(3) marking does not affect the animal's probability of
of the data produces a line that roughly coincides with
survival or subsequent recapture;
that drawn by eye.
(4a) the population is closed, such that there is no gain
Only when the points lie fairly close to a straight line is
(birth and/or immigration) or loss (death and/or
fitting by eye acceptable. While fitting by regression ana-
emigration) during sampling, or;
lysis is not reaIly acceptable owing to the non-
(b) there is birth and immigration, but death and emi-
independence of x and y values (Southwood 1978), it
gration affect marked and unmarked animals
allows the computation of confidence limits, and there-
equaIly, and survival rates are not age-correlated;
fore is to be preferred. If the fit of the line is not signifi-
(5) marked and unmarked animals intermingle freely
cant at the 5% level, then the resulting population es-
(so that subsequent samples are 'random'), and
each animal has the same probability of capture. timates are questionable, and should not be used (Smith
(Caughley 1977; Flowerdew 1976; Seber 1973; et al. 1975) (A 1;2;3;4a;5).
Smith et al. 1975)
Monthly population estimates were derived using the (iv) Bailey's (1951; 1952) Modified Lincoln Index
foIlowing enumeration and statistical models. Relevant This model (A 1;2;3;4a;5) makes use of progressive
assumptions (A) (see above) are indicated in par- change in the proportion of marked animals in the
entheses. trap able population, and gives less biased estimates than
the classical Lincoln index with small samples. Popula-
Enumeration methods tion size at time i is given by the equation
(i) Total numbers of individuals captured
(A 1;2;3).

(ii) Direct enumeration (Krebs 1966) M 2 (nj + l)(nj - mj)

This estimates the minimum number alive (MNA). This
includes all individuals trapped in a particular session, (mj + 1) (mj + 2)
plus those marked previously which were recaptured at a where Nj = population size at time i
later date. One disadvantage of this method is the sub- M = cumulative total of individuals marked pre-
jective decision which must be taken on the time all owed viously
to elapse while stiIl counting an animal present, rather nj = total number of individuals in the i th sam-
than assuming that it has emigrated temporarily (Flower- ple
dew 1976). Based on high recapture rates between mj = number of individuals in the i th sample that
trapping occasions, this period was arbitrarily taken as were marked previously.
three months (A 1;2;3).
(v) Jolly-Seber stochastic model (Jolly 1965; Seber 1973)
Mark-recapture models
This model aIlows for birth and immigration, and pro-
(iii) Hayne's removal (trap-out) method (Hayne 1949; vides estimates of numbers and associated variances for
Southern 1973) each trapping occasion except the first and last. Popula-
This method relates the daily captures of unmarked ani- tion size at time i is found by

njZjRj ZR· mj
Nj = nj+ _ OJ = mj + __ 1 _1_ aj = __
12
rj nj
10
OJ-mj + Rj 1 1 1-aj
SE j = V N;(N j - nJ----{---}+--
1Ii 8
OJ rj Rj mj

I
6
where Nj, nj and mj are as above
§ OJ = number of animals in the population imme-
4
'0 diately preceding the i th occasion
.;
z aj = proportion of marked animals in the i th sam-
ple
0
Rj = number of individuals released at time i
0
Zj = number of individuals marked before the i th
occasion which were not in the i th sample,
Figure 1 Regression line calculated by Hayne's method for but which are subsequently recaptured.
data on trapping of M. natalensis. The intersection of this line rj = number of animals released on the i th occa-
with the x-axis (18,5) represents total population size. sion that are subsequently recaptured.

Jolly-Seber estimates are usually accurate when 9% or
more of a population is sampled, and if the survival rate
is not less than 0,5 between trapping occasions (Bishop
& Sheppard 1973). However, its reliability strictly de-
pends on the condition that survival rates are not age re-
lated (A 1;2;3;4b;5).
More information, including formulae for the calcu-
lation of recruitment rates, is given by Caughley (1977),
Seber (1973) and Southwood (1978).
With methods (i), (iii) and (iv), data for days one to
three of each trapping session were combined to es-
timate numbers on day four. Owing to low daily sample
sizes, Jolly-Seber estimates were calculated by com-
bining data for each four-day session, and treating these
data as if they applied to a single trapping occasion, so
that the effective sampling period was 12 months (d.
four days per month).
The mean absolute differences (ie. 'Manhattan dis-
tances') between monthly estimates provided by each
particular combination of techniques (Table 2) were
used with Sneath & Sokal's (1973) unweighted
pair-group arithmetic averaging clustering (UPGMA) to
Table 2 Grid population estimates yielded by the var-
ious methods used to assess numbers of M. nata-
lensis. Estimates are as follows: NC - numbers
caught; MNA - minimum number alive; BLI -
Bailey's Lincoln index; HTO - Hayne's removal (trap-
out) estimator; J-S - Jolly-Seber estimate
January 1986 19 19 21,O±3,6 17,8*
February 16 16 18,6±2,7 16,4
March 18 18 20,6±3,4 18,5
*Based on a statistically non-significant linear regression.
/ Estimation of population size not possible.
construct phenograms (Figure 2) showing the degree of
overall similarity I dissimilarity between population
assessments yielded by the various estimation methods.
Results
Evidence used to test which of the implicit assumptions
of the different methods were satisfied is shown in Table
3. Only assumptions 1 and 2 were not violated during the
study.
The overall trapability rate, expressed as the number
of captures / number of individuals, was high for both
the grids (3,42) and the traplines (3,99). The overall re-
capture rates were 70,7% and 75% for the grids and lines
respectively. Recaptures outnumbered intial captures by
a factor of three, indicating a high degree of trap-
proneness.
Grid population estimates for January-March 1986
(Table 2) were not significantly different (X2 =
9,18 x 10-2; p = 0,99). Numbers caught and MNA were
identical in each of the three months, and agreed most
closely with Hayne's removal estimates (Figure 2). How-
ever, the latter method underestimated population size
in January 1986. Bailey's modified Lincoln indices were,
on average, 14% higher than estimates given by the first
three methods. The Jolly-Seber estimate for February
1986 was markedly higher (23%) than MNA and num-
bers caught.
Although monthly line estimates provided by the five
methods for March 1985-March 1986 (Table 4) varied
concordantly, differences between them were statistic-
ally significant (X2 = 231,74; P < 0,001). In general,
greater disparity between monthly estimates occurred
between April and December 1985 when population
gains and losses were high. Numbers caught, MNA and
/ Bailey's Lincoln indices were comparatively the most
19,8±1,2 similar (Figure 2), and did not differ significantly
/ (X2 = 8,18; p = 0,997). However, the last method
yielded considerably higher (over)estimates in May and
December 1985.

Table 3 Evidence for and against the

meeting of assumptions made by methods
for estimating numbers of Mastomys nata-
____ cNC & MNA
lensis (see text for explanation)
HTO
_____ BLI
, , , ,
2.0 1.0 0

1 Yes Property of 1-2-4-7

toe-clipping.
2 Yes Human error, if any,
was standardized.
3 No High recapture rates.
Trap-proneness.
4a No Presence of parturient
females. High birth &
immigration rates.
4b No Age-related mortality.
Figure 2 Dissimilarity phenogram of population estimates 5 No Caughley's (1977) test
provided by five assessment methods. Estimate symbols are as for unequal catchability
in Table 2.
Table 4 Monthly trapline population estimates (±1SE) of trapability, represented population size most ac-
for M. natalensis with associated variation coefficients curately. While Hilborn, Redfield & Krebs (1976) noted
(CV) (estimate symbols are the same as in Table 2) in simulation studies that MNA is generally 10-20%
lower than absolute population size, Flowerdew (1976)
Estimates commented that MNA estimates are usually accurate
when trapping is intensive and recapture rates are high.
Month NC MNA BLI HTO J-S CY Both of these conditions were fulfilled during the present
study.
1985 Relative to the enumeration estimates, the three
March 8 8 8,0±0 9,9* / 11,2 statistical models all apparently under- or overestimated
April 6 10 6,4± 1,3 5,6 18,2±0,6 57,4 population size on several occasions. Bailey's index
May 26 28 42,0± 12 44,6* 34,6±3,9 23,5 method overestimated trapline numbers in May and De-
June 25 34 28,8±3,6 26,0 50,6±5,0 31,9
cember 1985, when recruitment of young M. natalensis
July 28 39 37,5±8,2 28,0 67,2±11 40,3
into the trapable population was high, even within a
August 23 30 29,3±6,0 28,0' 33,1±9,8 12,8
September 33,0±7,2
four-day sampling period. This suggests that derived es-
25 30 30,2 45,8±1O,7 23,9
October timates are biased upwards by birth or immigration, or
November 9 14 9,8±2,1 9,6* 42,4±24,8 84,8 both; a conclusion also reached by Caughley (1977).
December 17 18 27,5±9,5 138,8* 29,3± 10,2 112,0 Hayne's removal estimates were lower than numbers
1986 caught when monthly sample sizes were small (April
January 16 17 19,6±4,2 15,4 26,7±9,1 24,7 1985; January and February 1986). Hence, the accuracy
February 9 10 9,0±0 8,9 12,3±2,8 14,7 of this method is somewhat dependent on sample sizes.
March 10 10 1O,3±1,2 9,5 / 3,45 However, a more serious shortcoming is its reliance on a
uniform pattern of captures (i.e. constant probability of
*Based on statistically non-significant linear regressions. capture) during the sampling period. Unless numbers
/ Estimation of numbers not possible. captured on each trapping occasion are similar, the cor-
relation coefficient of the regression line is decreased,
making resulting population estimates statistically ques-
Hayne's removal and Jolly-Seber monthly estimates tionable (Smith et al. 1975). This was often the case
were, in general, markedly dissimilar, both from each during the present study (Table 3), regardless of sample
other, and from assessments from the other three sizes. While this may sometimes be remedied by de-
methods (Figure 2). Jolly-Seber estimates were, on creasing the sampling period, or by lumping data from
average, more than 45% higher than concurrent MNA, different trapping occasions (see Southern 1973), there
numbers caught and Bailey'S Lincoln indices, and thus will always be some occasions where no rearrangement
were probably overestimates. Hayne's removal es- of data will result in a smooth, statistically significant, re-
timates were often based on statistically non-significant gression line (Hayne 1949). Estimates based on statistic-
linear regressions which resulted from a non-uniform ally non-significant regressions should not be used
pattern of captures during particular sessions (ie. the (Smith et al. 1975), but were here included in analysis in
probability of capture did not remain constant). On such order to evaluate this method in its entirety.
occasions, it under- or overestimated population size. The Jolly-Seber technique apparently overestimated
(For instance, the December 1985 estimate was 470% population size consistently throughout the study. This
higher than the next highest assessment, and was based reflects the longer effective sampling period (12 months)
on a linear regression with a probability of 0,97.) Re- used in calculations, so that the potential for error as a
arrangement of values in an attempt to yield a smooth, result of assumption violation (equal catchability; con-
significant line (see Southern 1973) was not permitted by stant mortality rates) was greater than with the other
the available data. methods which were based on data collected over four
days each month. Manly (1971) and Southwood (1978)
have noted that Jolly-Seber estimates are sensitive to
Discussion age-dependent variations in mortality rate, while Bishop
The objective evaluation of estimation methods ideally & Sheppard (1973) found that this method overestimates
requires that absolute population size be known. This population size when a large proportion of the animals is
can be determined by enumeration of mice excavated sampled, and conversely, that it underestimates numbers
from burrows (Smith 1968), but was not possible during when sample sizes are small and survival rates are high.
the present study since the associated disturbances The inaccuracy of the three mark-recapture models
would undoubtedly have altered population dynamics can therefore be attributed to statistical flaws of these
subsequently. methods, as well as the violation of their implicit (and
While congruency does not necessarily imply ac- biologically unrealistic) assumptions. The major weak-
curacy, it is the only useful criterion for the evaluation of ness of these models is their reliance on equal catch-
population assessment methods in a study such as this. ability, which is the exception rather than the rule in
The high monthly and overall similarity between direct most field studies (Caughley 1977). While various modi-
enumeration (MNA estimates) and numbers caught fications to allow for unequal trapability have been pro-
suggests that these methods, by reflecting a high degree posed (Pollock 1981; Smith et al. 1975), these invariably
involve further restrictive assumptions, and are useful in
only highly individual cases.
Statistical models therefore have certain statistical and
biological pitfalls which may reduce their heuristic value
when estimating population size. The simpler enu-
meration methods, however, make no assumptions
about uncaught animals, are thus more robust, and are
to be preferred over statistical models for assessing num-
bers when trapping data indicate that certain assump-
tions are being violated. Although statistical models may
allow the quantification of other demographic para-
meters, such as recruitment and mortality rates, the enu-
meration methods can also be used for this purpose with
less risk of distortion arising out of assumption violation.
Direct enumeration (MNA) seems to be the method
with the greatest accuracy and widest applicability, since
derived estimates are not as susceptible to distortion by
minor fluctuations in sample sizes resulting from, for ex-
ample, weather. While Roff (1973) has sharply criticized
this approach, various authors have used it with success
(Carolyn Ascaray 1986, unpublished; Christian 1979,
1980; Perrin 1979), and Cheeseman & Delany (1979)
concluded that it is the best of the five estimation
methods they compared.
Acknowledgements
Thanks are extended to the Natal Parks Board for per-
mission to trap at Bluff Nature Reserve. Financial assist-
ance from the Council for Scientific and Industrial Re-
search, and the University of Natal, is gratefully acknow-
ledged.
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