POPULATION ECOLOGY OF THE ENDEMIC RODENT NESORYZOMYS

SWARTHI IN THE TROPICAL DESERT OF THE GALÁPAGOS ISLANDS

Author(s): Donna B. Harris and David W. Macdonald
Source: Journal of Mammalogy, 88(1):208-219. 2007.
Published By: American Society of Mammalogists
DOI: http://dx.doi.org/10.1644/05-MAMM-A-370R4.1
URL: http://www.bioone.org/doi/full/10.1644/05-MAMM-A-370R4.1

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Journal of Mammalogy, 88(1):208–219, 2007

POPULATION ECOLOGY OF THE ENDEMIC RODENT

NESORYZOMYS SWARTHI IN THE TROPICAL DESERT OF
THE GALÁPAGOS ISLANDS
DONNA B. HARRIS* AND DAVID W. MACDONALD
Wildlife Conservation Research Unit, University of Oxford, Department of Zoology,
Tubney House, Abingdon Road, Tubney, Abingdon OX13 5QL, United Kingdom

Ancestrally continental forest species of the tribe Oryzomyini, the endemic cricetid rodents of the Galápagos,
have had to adapt to the harsh tropical desert of the Islands. Following the recent rediscovery of the Santiago
nesoryzomys (Nesoryzomys swarthi) endemic to Isla Santiago, Galápagos, we conducted the 1st autecological
study of this species. Our 3-year study revealed mean annual survival of 23.2% and maximum survival of 812
days. Reproductive activity was restricted to the wet season with a stable annual proportion of breeding females
and a consistent peak in pregnancy in April. The likelihood of postpartum breeding increased with rainfall
when 2 litters were produced. The growth and development of juveniles was slow and they did not reproduce
in their natal year. Positive correlations between rainfall and mean adult body weight and between vegetation
density (particularly prickly pear cactus [Opuntia galapageia]) and population levels supported a hypothesis
of food limitation. Comparisons with the Galápagos oryzomys (Oryzomys bauri), endemic to Isla Santa Fe, and
a review of continental members of the tribe Oryzomyini suggest that the ephemeral, unpredictable environ-
ment of the Galápagos arid zone has selected for a strategy of relatively high survival and low reproduction in
N. swarthi and O. bauri that is more typically found among the desert Heteromyidae than other members of
the Oryzomyini. We also present data on sex ratio, home range, and philopatry that together indicate a promis-
cuous or polygynous mating system. Our findings may help to guide future conservation strategies for this
endangered rodent species.

Key words: desert rodent, food limitation, Galápagos, island, life history, Oryzomys bauri, rainfall, reproduction, small
mammal, survival

Mammals optimize life history traits to survive and to breed.
Although the ultimate evolutionary objective is to reproduce,
where this capacity is constrained by environmental factors,
there is selection for high survival (French et al. 1975). The
harsh physical and biotic conditions of the North American
desert have selected for a strategy of high survivorship and low
reproduction among rodents (French et al. 1975; Kenagy and
Bartholomew 1985). Such a strategy might be advantageous
to species other than classic desert-adapted taxa such as the
Heteromyidae, and we reason that the conditions on the
Galápagos Islands might have led the endemic rodents to
converge on this life history pattern.
More specifically, a verbal model proposed by Kenagy and
Bartholomew (1985) describes how reproductive patterns of
* Correspondent: donnabharris@googlemail.com
Ó 2007 American Society of Mammalogists
www.mammalogy.org
208
North American desert rodents represent 2 different responses
to the temporal ephemerality of desert resources. Temporally
flexible ‘‘pulse matchers’’ respond rapidly to individual, unpre-
dictable resource pulses with small, successive litters, rapid
development of young, and reproduction of juveniles in their
natal year but do not respond to extreme drought conditions. In
contrast, ‘‘pulse averagers’’ are temporally fixed, once-a-year
breeders that rely on the general predictability of environmental
seasonality. Even in severe drought, pulse averagers start
breeding on schedule but reproductive failure may result
through various adjustment techniques.
The Santiago nesoryzomys (Nesoryzomys swarthi) is en-
demic to Isla Santiago where it exists as a single population
in the arid zone of the north-central coast (Harris et al. 2006).
This area lies within the rain shadow of Isla Santa Cruz and
the Santiago highlands and thus is prone to drought periods.
However, the climate is erratic and periods of drought are
contrasted with the heavy rains associated with El Niño South-
ern Oscillation events. Annual rainfall over the past 40 years
has ranged from 63.6 mm in 1985 to 2,768.7 mm in 1983.
February 2007 HARRIS AND MACDONALD—NESORYZOMYS SWARTHI POPULATION ECOLOGY
FIG. 1.—Map of the Galápagos Archipelago showing the distribution of extant (bold, underlined text) and extinct rodent species. Undescribed
species are noted with an asterisk (*).
Nesoryzomys swarthi is 1 of an original assemblage of 12
endemic rodent species of the Sigmodontine tribe Oryzomyini.
The continental ancestors of this group are believed to have
drifted on vegetation rafts from the South American mainland,
and there were at least 3 separate colonizations (Orr 1966;
Steadman and Ray 1982; Steadman and Zousmer 1988). The
thomasomyine ancestor of the giant rat genus Megaoryzomys
was the 1st to colonize, followed, around 3–3.5 million years
ago, by the ancestor of Nesoryzomys—probably a species of
Sigmodontomys or Melanomys, originating from lower mon-
tane and lowland forested habitats in South America. Finally,
the yellowish oryzomys (Oryzomys xanthaeolus) from coastal
Peru is believed to have rafted over in recent historical times,
giving rise to the Oryzomys species of Galápagos (Hutterer and
Oromı́ 1993; Patton 1975; Patton and Hafner 1983; Steadman
1985; Steadman and Ray 1982; Weksler 2003). Unfortunately,
the introduction in the late 1600s and subsequent spread of the
black rat (Rattus rattus) probably pushed at least 6 endemic
species of Oryzomys and Nesoryzomys to extinction (Brosset
1963; Clark 1984; Dowler et al. 2000; Key and Muñoz Heredia
1994; Niethammer 1964; Fig. 1). Until its rediscovery in 1997,
N. swarthi also had been presumed extinct (Dowler et al. 2000;
Orr 1938) and with the exception of data recorded over the 2
nights when it was rediscovered (Dowler et al. 2000), nothing
is known of the population ecology of this species.
We aimed to quantify population stability, the abundance–
vegetation relationship, reproductive seasonality and fecundity,
juvenile growth and development, and survival to test whether
209
N. swarthi has adopted the high survival–low reproduction
strategy of the desert Heteromyidae. Furthermore, we predicted
that N. swarthi would be identified as a pulse averager. This
prediction stems from the only other substantial study of
Galápagos rodent ecology in which the Galápagos oryzomys
(Oryzomys bauri ¼ O. galapagoensis bauri in Wilson and
Reeder [2005]), endemic to low-lying, arid Isla Santa Fe,
exhibited a desert rodent strategy of high survival and low
reproduction with demographic traits typical of a pulse
averager (Clark 1980). The recent rediscovery of N. swarthi
on Isla Santiago has therefore provided an opportunity to test
for convergence of life history tactics by comparing the pop-
ulation ecology of 2 rodent species exposed to the harsh
tropical desert of the Galápagos arid zone. Furthermore, to
assess the exceptionality of the Galápagos rodent life histories
we compared the population ecologies of N. swarthi and
O. bauri to those of other oryzomyine rodent species studied in
a variety of habitats.
Finally, because N. swarthi is listed as vulnerable by the
IUCN (http://www.redlist.org/), an autoecological study is
a crucial 1st step for the conservation of this poorly known,
endangered species (R. C. Dowler, D. S. Carroll, and C. W.
Edwards, 2000, Nesoryzomys swarthi, in 2004 IUCN Red List
of Threatened Species, www.redlist.org). We therefore present
biometric data and exploratory data on the breeding system,
including sex ratio, operational sex ratio, philopatry, and home-
range information that should be useful for the future
management of this species.
210 JOURNAL OF MAMMALOGY
MATERIALS AND METHODS
Study Site
The volcanic Galápagos Islands are situated 960 km west of
mainland Ecuador in the Pacific Ocean (Jackson 1993). The
uninhabited island of Santiago is the 4th largest Galápagos
island at 585 km2 with a maximum elevation of 907 m (Jackson
1993). The habitat of our study area on the north-central coast
is typical of the Galápagos arid zone. Prickly pear cactus
(Opuntia galapageia), incense tree (Bursera graveolens),
yellow cordea (Cordea lutea), and Galápagos croton (Croton
scouleri) dominate among a shrub layer that mostly consists
of glorybower (Clerodendrum molle), castela (Castela gal-
apageia), and Galápagos lantana (Lantana peduncularis—
McMullen 1999). The climate is strongly influenced by oceanic
currents and there are 2 seasons; the warm, wet season
(January–May) is characterized by warm temperatures with
variable rainfall at all latitudes and the cool, dry season (June–
December), caused by the Humboldt Current, is characterized
by cool temperatures with high rainfall in the highlands
but almost no precipitation in the lowlands. Although rainfall
at our study site is probably lower, data from equivalent ele-
vation on Isla Santa Cruz (Charles Darwin Research Station,
in litt.) are suitable for demonstrating temporal fluctuation in
rainfall in the Galápagos arid zone. Mean annual rainfall in
the Santa Cruz arid zone for the period 1965–2004 was
491.44 mm, notably higher than the median of 277.55 mm,
due to occasional years with very high rainfall. The tempera-
ture is relatively stable with an annual mean of 23.958C 6 0.14
SE ranging from 22.68C to 26.28C.
Data Collection
Livetrapping of N. swarthi spanned 2002–2004 and was
conducted on 11 trap grids. Data were collected during 10
trapping sessions: April 2002, December–January 2003 (here-
after referred to as December 2002), February 2003, April
2003, June 2003, July 2003, August 2003, April–May 2004
(hereafter referred to as April 2004), July 2004, and
September–October 2004 (hereafter referred to as September
2004). We analyzed data from 5 trapping grids, including 3
control grids (coastal grid C1, with data from all sessions, and
inland grids I1 and I2, with data from December 2002 through
September 2004), and 2 nonexperimental coastal grids (C2 and
C3; April 2002 and December 2002 sessions). The other 6
grids (coastal C4 and C5 and inland I3, I4, I5, and I6) were
subject to experimental treatment during 2003 (removal of
R. rattus) and 2004 (food addition) so usable data were limited
to premanipulation periods (December 2002 and April 2004).
Coastal grids were situated 100 m from the shore. The
remaining grids were positioned approximately 1 km inland.
Trap grids consisted of 7
7 arrays. Following Otis et al.
(1978), we used our radiotracking data (presented below) to
calculate a recommended maximum trap spacing of 44.55 m
and optimal spacing of 15.75 m; we selected a midpoint of 30
m. Radiotracking also revealed that a minimum intergrid
spacing of 550 m would prevent intergrid migration and ensure
sample independence. During 2002 we placed 1 Tomahawk
Vol. 88, No. 1
live trap (model 201, 410
125
125 mm; Tomahawk Live
Trap Co., Tomahawk, Wisconsin) per grid point and sampled
for 10 nights. During the 2003 and 2004 trapping periods we
placed 2 traps per station but reduced our censuses to 5 nights.
Therefore, total sampling effort was equal across years,
although based on different sampling durations. Traps were
baited between 1600 and 1830 h with a mixture of peanut
butter and oats. Traps were sheltered with fitted tarpaulin
covers and placed under a shrub or a lava overhang to provide
shade from sunlight and rain. Traps were checked between
0500 and 0830 h.
Animal Processing
All N. swarthi were anesthetized using halothane, indi-
vidually marked using subcutaneous passive integrated tran-
sponder tags (type FDX-B; Francis Scientific Instruments,
Cambridge, United Kingdom), and released. Sex, weight (to
0.1 g), and reproductive condition (females: perforate or imper-
forate, enlarged or normal nipples, pregnant or not pregnant,
males: scrotal or inguinal testes) were recorded at the date of
1st capture within each session. The body (nose tip to base of
anus) and tail length (base of anus to tail tip) of anesthetized
animals was recorded where possible (to 1 mm). All methods
were in agreement with recommendations of the American
Society of Mammalogists (Animal Care and Use Committee
1998).
Life History Strategy
Abundance.— Data from the control grids C1, I1, and I2
(2003–2004) were used to assess population stability. The
abundance, estimated using the minimum number known alive
(Krebs 1966), was calculated for each grid, within years. We
used minimum number known alive because the total number
of captures was less than 25 for some trapping session–grid
combinations, failing criteria required by closed population
estimators based on capture probabilities (Otis et al. 1978). To
explore the relationship between population levels and vege-
tation density, abundance and habitat data were collected from
4 coastal (C1–4) and 4 inland trap grids (I1–4) during the
December 2002 trapping session. We used T-square sampling
at 20 randomly selected grid points (Greenwood 1996) to
estimate the density of the dominant plant types (cactus, trees,
and shrubs) on each grid.
Reproduction.— Inspection of all trapping data revealed that
the minimum weight at which rats became sexually active was
41 g for males and 45 g for females. These weights were there-
fore set as the threshold weights for inclusion of individuals in
the denominator of breeding proportion. Animals were pooled
across all grids for each time period and the proportion of
reproductive males (scrotal testes), proportion of reproductive
females (perforate vagina, pregnant, lactating, or any combi-
nation of these), and proportion of breeding (pregnant,
lactating, or both) females were estimated. The number of
juvenile recruits also was recorded and reported as a proportion
of the total minimum number known alive.
Growth.— The growth of individual, recaptured juvenile
males (,80 g—explained below) and juvenile females (,70 g;
February 2007 HARRIS AND MACDONALD—NESORYZOMYS SWARTHI POPULATION ECOLOGY
FIG. 2.—Monthly rainfall at Bahia Academica (008449S, 908189W, 2 m above sea level), Puerto Ayora, Isla Santa Cruz (data courtesy of the
Charles Darwin Research Station). Bars show total monthly precipitation and the line is mean monthly temperature.
explained below) was estimated on control grids C1, I1, and I2
in 2003 and 2004 by subtracting the weight at 1st capture from
the weight at last preadult capture, converting to a monthly
growth rate for each individual, and then calculating the mean
monthly growth rate for each sex.
Survival.— All data (including experimental grids) were
consulted to obtain the record for maximum longevity. Data
from the control grids (C1, I1, and I2) were used to estimate the
median survivorship. The 1st control animals were marked
during the December 2002 trapping session. The survival of
this cohort was then monitored until October 2004. Disappear-
ance rates among these 3 grids (with different habitat types)
also were compared. Disappearance was defined as in Clark
(1980) as 1  [(N known alive at both time t and t þ 1)/N
known alive at time t].
Biometrics and breeding system.— To calculate mean body
weight, thresholds of 80 g for males and 70 g for females were
used to distinguish adult and juvenile N. swarthi. These thresh-
old weights were based on inspection of frequency histograms
of body weight and the weight at the plateau in growth.
Pregnant females were excluded from the weight comparisons
but were included in the length comparisons. Sex ratio was
calculated from the pooled 1st captures on all grids, across all
sessions (n ¼ 726). The operational sex ratio (the average ratio
of fertilizable females to sexually active males at any given
time—Emlen and Oring 1977) was analyzed for significant
intersexual skew by comparing the number of scrotal males to
the number of perforate, nonpregnant females for the breeding
seasons of 2002, 2003, and 2004.
Twenty-three adult N. swarthi (11 females and 12 males)
were radiotracked between May and July 2002 on the coastal
grids C3 and C4. Radiocollars (Biotrack Ltd., Dorset, United
Kingdom) were fitted under anesthesia (halothane). The cable
tie collar plus radiotransmitter weighed between 2 and 4 g, such
that the collar did not exceed 5% of the body weight (Animal
Care and Use Committee 1998). Animal locations were ob-
tained by triangulation of 2 bearings taken by 2 trackers
working on a 30
30-m grid (trap grid). The trackers 1st
moved toward the animal and when the signal strength indi-
211
cated that they were close the trackers positioned themselves on
grid points (or took global positioning system locations off-
grid) at 30–60 m from each other and took simultaneous
bearings using TR4 receivers (Telonics Inc., Mesa, Arizona)
and flexible 3-element Yagi antennas (Biotrack Ltd, Dorset,
United Kingdom). Radiotracking shifts alternated between
1600–0200 and 2200–0800 with a fix obtained for each of 4
animals every hour. Schoener’s index was used to test for
autocorrelation between subsequent fixes. In all cases loca-
tions met a randomness criterion of 3 consecutive values of
Schoener’s V greater than 1 after 1 h, indicating that fixes were
sufficiently independent at 1-h intervals (Kenward 2001;
Kenward et al. 2003). Only 4 animals were tracked in a given
night. All analyses were carried out using program Ranges6
(Kenward et al. 2003). Individual incremental plots of range
area versus the number of fixes were inspected to check that
the range area estimate reached an asymptote, ensuring that
sufficient fixes had been collected to delineate the home range
of each animal (Harris et al. 1990). The number of fixes per
female ranged from 16 to 43 (X  ¼ 31 6 9 SD, n ¼ 11) and for
males was 18 to 58 (X  ¼ 38 6 11 SD, n ¼ 12). Bearing error
was estimated from stationary animals during periods of
inactivity: A total of 3 pairs of sequential bearings at 1-h
intervals were taken from each of 5 stationary animals (3 on
grid C3 and 2 on grid C4) following the protocol described
above. These data were then input into the program Locate III
(Nams 2006) and we used the maximum likelihood estimator
option to estimate the most likely locations of the test animals
and the deviation of each bearing from those estimated
locations. The overall error angle (bearing standard deviation)
was then calculated and we converted this to a 95% confidence
interval. The result was a 95% likelihood of the true bearing
lying within 9.888. Finally, using the placement of the tracking
stations, the number of bearings, and the bearing standard
deviation, Locate estimated the error ellipse. The mean area of
the 95% confidence ellipse was 0.0086 ha 6 0.0084 SD. When
delineating the home range, high-use core areas may be
separable from peripheral areas that are seldom visited (Burt
1943; Kenward et al. 2001). To quantify high-use core areas,
212 JOURNAL OF MAMMALOGY
FIG. 3.—Variation in the abundance (minimum number known
alive) of Nesoryzomys swarthi on the three 3.24-ha control grids
(C1 ¼ coastal and I1 and I2 ¼ inland) over 9 trapping sessions span-
ning December 2002–September 2004.
cluster analysis was used to determine a ‘‘truncated minimum
convex polygon (MCP)’’ home-range estimate. Polygon areas
were calculated at 5% (from 20% to 100%) increments as lo-
cations were added using the clustering method. Inspection of
area plots for each subject enabled selection of the core percent
at which there was an inflection in the curve of area versus
percentage of locations (Kenward et al. 2001). The 100% MCP
estimate of home-range area (i.e., the estimate before
truncation) also was included. This estimate includes move-
ments made by the animals out of the home range or high-use
core area (i.e., the truncated MCP). The 100% MCP method
was used to obtain the range span, which was defined as the
maximum dimension of the MCP (Kenward et al. 2003). All
home-range parameters were compared between sexes. Finally,
the interannual grid residencies of males and females were
estimated to compare philopatric tendencies.
RESULTS
Precipitation
The total rainfall amounts for 2003 and 2004 were 190.20
mm and 161.20 mm, respectively. These levels are notably
FIG. 4.—The relationship between cactus density and abundance of
Nesoryzomys swarthi on 8 trapping grids. Open symbols represent
inland grids (I1–4, n ¼ 4), closed symbols represent coastal grids (C1–
4, n ¼ 4). Data labels are abundance (minimum number known alive).
Data were collected during December 2002.
Vol. 88, No. 1
FIG. 5.—a) The proportions of potentially reproductive males and
females that are reproductive (males: scrotal; females: perforate,
pregnant, lactating, or a combination of these), and breeding
(pregnant, lactating, or both). Columns are labeled with the number
of reproductive or breeding individuals. Proportion of the total
minimum number known alive consisting of recruiting juveniles
(pooled across all grids for each trapping session except when
experimental grids were subject to manipulation during parallel
research). Columns are labeled with the number of juvenile captures.
lower than the annual average of 491.44 mm, and that of the
preceding year (2002) of 577.70 mm. The period 2003–2004
can therefore be considered a drought period (Fig. 2).
Life History Strategy
Abundance.— Intergrid abundance (minimum number
known alive) varied up to 5-fold (at the start of the dry season
of 2003). However, intragrid abundance was relatively stable,
with a mean coefficient of variation of 33 (Fig. 3). The abun-
dance of N. swarthi was higher on coastal relative to inland
grids (t ¼ 5.9, d.f. ¼ 6, P ¼ 0.001) and was positively
correlated with cactus density (R2 ¼ 0.913, d.f. ¼ 6, P ¼
0.0002; Fig. 4) and shrub density (R2 ¼ 0.478, d.f. ¼ 6, P ¼
0.058), but was not related to tree density (R2 ¼ 0.018, d.f. ¼ 6,
P ¼ 0.752). Cactus density and shrub density were correlated
(R2 ¼ 0.654, d.f. ¼ 6, P ¼ 0.015).
Reproduction.— Breeding spanned the wet season (Decem-
ber–May) with a peak in pregnancy and lactation in April (Fig.
5a). Although reproductive activity appeared to vary with
rainfall (Figs. 2 and 5a), the breeding rate (proportion of fe-
males that were pregnant, lactating, or both) remained rela-
tively constant across years (see April 2002, 2003, and 2004;
Fig. 5a). Simultaneous pregnancy and lactation revealed
February 2007 HARRIS AND MACDONALD—NESORYZOMYS SWARTHI POPULATION ECOLOGY 213

TABLE 1.—Biometric data collected from coastal grids C1–4 and

inland grids I1–4 between December 2002 and January 2003 for
Nesoryzomys swarthi. Male adults are  80g and female adults are
 70g.

Weight (g) Body length (cm) Tail length (cm)

 6 SD (range)
X n X 6 SD (range) X 6 SD (range) n

Male 109.4 6 26.5 154 16.0 6 1.4 13.9 6 1.1 32

(59.0182.5) (12.918.5) (11.415.8)
Female 86.7 6 18.9 153 14.3 6 1.0 12.9 6 0.9 25
(48.0137.0) (12.115.7) (10.914.8)
Male adult 114.8 6 23.6 135 16.2 6 1.1 14.1 6 1.0 29
(80.5182.5) (13.718.5) (11.715.8)
Female adult 91.1 6 17.1 129 14.7 6 0.7 13.2 6 0.8 19
(70.0137.0) (13.115.7) (11.214.8)

postpartum breeding by 17 (18.1%) of 94 potentially repro-

ductive females in April 2002 compared to 0 of 46 in April
2003 (although 2 females produced litters in both December
2002 and April 2003) and 8 (6.2%) of 130 in April 2004. We
did not quantify mean litter size, although dissection of 1
pregnant female revealed 3 embryos. The proportion of the
minimum number known alive consisting of captures of
juveniles peaked during April of each year (Fig. 5b). There
were no sexually mature juveniles (scrotal or perforate) in 2003
(of 10 males and 6 females). In 2004, just 6 (4 of 38 males and
2 of 39 females) juveniles attained sexual maturity. However,
there was no evidence that juveniles actually reproduced in
their natal year.
Growth.— The mean monthly growth rate of juvenile males
(,80 g) was 5.62 g 6 4.25 SD (n ¼ 29) and that of juvenile
females (,70 g) was 4.12 6 3.92 g (n ¼ 33) with no
intersexual difference (t ¼ 1.447, d.f. ¼ 60, P ¼ 0.153). By the
end of the dry season (December–January) the previous year’s
cohort of juveniles had reached adult weight and the popula-
tion was largely composed of adults (Table 1).
Survival.— The longevity record of 812 days pertained to
a female 1st marked in July 2002 (during the radiotracking
work). The median time known alive for 82 of 96 recaptured
individuals was 199 days for males (n ¼ 38) and 203 days for
females (n ¼ 44) and cumulative frequency distributions of
time known alive were similar (Kolmogorov–Smirnov Z ¼
0.654, n ¼ 38 males and 44 females, P ¼ 0.786). Annual
survivorship of this sample was 23.2%, although the same
individuals were still alive after 500 days. A total of 15.9% of
recaptured N. swarthi survived for the duration of the sampling
period. Disappearance rates did not differ between coastal (high
FIG. 6.—Home ranges of Nesoryzomys swarthi estimated by
radiotracking on coastal grids C3 and C4 between May and July
2002 and plotted as minimum convex polygons (MCPs). Solid lines
symbolize MCPs of males and dotted lines are MCPs of females. The
thick bars show the edges of trapping grids.
vegetation cover) and inland (low vegetation cover) grids for
any time period (v2 tests; all P . 0.250).
Biometrics and breeding system.— Adult males were signif-
icantly heavier than adult females (Welch’s t ¼ 70.082, n ¼
135 males and 129 females, P , 0.0001; Table 1) and
significantly larger (body length: t ¼ 5.159, n ¼ 29 males and
19 females, P , 0.0001; tail length: t ¼ 3.552, n ¼ 29 males
and 19 females, P ¼ 0.001; Table 1). The mean weight of male
and female (excluding pregnant females) adult N. swarthi was
positively correlated with monthly rainfall (R2 ¼ 0.520,
d.f. ¼ 8, P ¼ 0.019 and R2 ¼ 0.747, d.f. ¼ 8, P ¼ 0.001,
respectively). There was no interaction effect between rainfall
and sex on mean adult weight (F ¼ 0.148, d.f. ¼ 1, 16, P ¼
0.706).
The sex ratio was significantly skewed toward males, with
56.5% and 43.5% males and females, respectively (v2 ¼ 12.17,
d.f. ¼ 1, P ¼ 0.0005). This male bias was more evident in the
operational sex ratio during the breeding seasons of 2002
(April ratio of 117:53; v2 ¼ 24.094, d.f. ¼ 1, P , 0.0001) and
2004 (April ratio of 120:44; v2 ¼ 35.220, d.f. ¼ 1, P ,
0.0001). The operational sex ratio did not differ significantly
from 1:1 in 2003 (February and April; P .0.05) although it
was skewed earlier in the year (December 2002–January 2003
ratio of 94:63; v2 ¼ 6.121, d.f. ¼ 1, P ¼ 0.013). However, an

TABLE 2.—Home range estimates for male and female Nesoryzomys swarthi radiotracked on coastal grids C3 and C4 between May and
July 2002. MCP ¼ minimum convex polygon.

Males (n ¼ 12) Females (n ¼ 11)

 6 SD (range)
X Median CV  6 SD (range)
X Median CV
Truncated MCP (ha) 1.948 6 1.52 1.56 77.95 0.564 6 0.33 0.49 58.57
(0.124.67) (0.221.38)
MCP (ha) 2.792 6 2.61 1.76 93.51 0.993 6 0.72 0.68 72.18
(0.279.56) (0.242.44)
Range span (m) 240.42 6 130.15 220.50 54.14 159.55 6 79.26 130.00 49.68
(73528) (63296)
 TABLE 3.—Life history information summarized from studies of oryzomyine rodents in South, Central, and North America. This review compares stability (coefficient of variation [CV]),
reproductive seasonality (whether breeding is seasonal or occurs throughout the year), fecundity (number of litters per year and the litter size estimate from number born or number of 214
embryos), and survival (minimum annual survival and maximum survival) estimates for each species from studies in different geographic locations and habitats.

Litter size (*) or

No. no. embryos (**) Annual Maximum Study
Species name Mean CV Breeding litters/ X,
 6 1 SD survival survival duration
(common name) Location Habitat (minimum) (season) year (range) (%) (months) (months) References
a b
Nesoryzomys swarthi Galápagos Islands Arid scrub 33 (16) Seasonal 2 (24) 23 34 30 This study
(Santiago nesoryzomys)
Oryzomys bauri Galápagos Islands Arid scrub 28 (13) Seasonal 2c 4.2 (27)** 37 20 31 Clark 1980
(Galápagos oryzomys) 3* 3** Brosset 1963
Oligoryzomys longicaudatus North-central Chile Semiarid thorn scrub 9 52 Meserve et al. 1995
(long-tailed colilargo) North-central Chile Semiarid thorn scrub 8d 14 Meserve et al. 1996
Chile Temperate scrub grassland 88 7 Fulk 1975e
Argentina Transition zone: Andean 112 Seasonal 9 42 Guthmann et al.. 1997
Forestsemiarid
Patagonian steppe
South Chile Temperate forest 93f Seasonal 252 Murua and Briones 2005
(OctoberApril)
Chile Temperate rain forest 125 Seasonal 4 53 Murua et al. 1986
Temperature grassland 91 (OctoberMay)
Oligoryzomys nigripes Southeastern Brazil Grassland 141d 0 12 Feliciano et al. 2002
(black-footed colilargo) Argentina Temperate grassland 147 17 Dalby 1975e
Brazil Secondary scrub/ 66 All year 9 12 Veiga-Borgeaud 1982
agricultural
Oligoryzomys eliurus Brazil Tropical savanna 75 24 Mello 1980e
(Brazilian colilargo) Central Brazil Gallery forest 112 Seasonal 0 2 14 Mares and Ernest 1995
Oecomys concolor Central Brazil Gallery forest 154 Seasonal 0 6 14 Mares and Ernest 1995
(unicolored oecomys) Venezuela Tropical humid forest 80 22 O’Connell 1981e
All year Hershkovitz 1960g
JOURNAL OF MAMMALOGY

Oecomys bicolor Venezuela Tropical savannah 61 6 August 1981e

(white-bellied oecomys) Central Brazil Gallery forest 96 Seasonal 0 5 14 Mares and Ernest 1995
South America All year Hershkovitz 1960g
and Panama
Panama 3** Enders 1935g
Oryzomys capito (Azara’s broad- Panama Tropical dry forest 100 13 Fleming 1971e
headed oryzomys) Central Brazil Gallery forest 62 Seasonal 0 8 14 Mares and Ernest 1995
Southeastern Brazil Gallery forest 85d Seasonal 2h 53 12 Talamoni and Dias 1999
Brazil Mature forest 127 Seasonal 4 Olmos 1991
French Guiana Tropical rain forest All year (16)* 3.68** 30 Henry 1994
Panama Tropical moist forest 57 13 Fleming 1971e
Venezuela Tropical humid forest 65 22 O’Connell 1981e
Panama Tropical forest All year Fleming 1970
Oryzomys capito Trinidad Open evergreen 23 2.8 (maximum 5)*i 0 12 36k Everard and
velutinus seasonal marsh forest 2.9 (maximum 4)*j Tikasingh 1973

Oryzomys palustris Everglades, Florida Tropical hardwood Seasonal 4.5* 21 Smith and Vrieze 1979
(marsh oryzomys) hammocks
Breton Island, Louisiana Coastal sedge 92 Seasonal 4.8** 36 Negus et al. 1961
Vol. 88, No. 1
 February 2007

TABLE 3.—Continued.

Litter size (*) or

No. no. embryos (**) Annual Maximum Study
Species name Mean CV Breeding litters/ X,
 6 1 SD survival survival duration
(common name) Location Habitat (minimum) (season) year (range) (%) (months) (months) References
Mississipi, Tidal marsh All year 1 24 48 Wolfe 1985
Gulf of Mexico
Galveston, Texas Tidal marsh All year
Upland habitat Seasonal Kruchek 2004
Virginia, northeastern Tidal marsh All year 18 24 Bloch and Rose 2005
United States
Delaware Salt marsh Seasonal 6.7 6 0.6 (SE) Edmonds and Stetson 1993
(410)**
Oryzomys Florida Keys Freshwater wetlands and (35)* FWS 1996l
palustris natator saline wetland habitat 45 All year 9 E. A. Forys et al., in litt.
Oryzomys russatus Brazil Atlantic Forest All year 6 10 14m Bergallo 1995
(russet oryzomys)
Nectomys squamipes South America Forest Up to 5* (27)** Reviewed in Ernest 1986
(Atlantic Forest nectomys) Central Brazil Mature gallery forest 35 All year 0 9 14 Mares and Ernest 1995
Brazil Rural valley 68 All year Gentile et al. 2000
Brazil Captive (wild caught) 4.1 6 1.2 (16)* D’Andrea et al. 1996
Brazil Mixed: plantation All year 14.3 # 62 D’Andrea et al. 1999
pastureforest 16.07 $
fragments
a
A dissected female N. swarthi contained 3 embryos and several adult females were each trapped with 2 juveniles (D. B. Harris, in litt.). Data for other Galápagos species suggest that 2–4 embryos are typical in the Galápagos Oryzomyini
(Beebe 1924; Brosset 1963).
b
Updated because of recent data collection by S. D. Gregory.
c
Two breeding bouts.
d
Estimated from a figure.
e
From O’Connell 1986.
f
Interannual (n ¼ 21 years).
g
From Fleming 1970.
h
Two reproductive periods.
i
From wild-caught individuals in captivity.
j
From wild-caught individuals in forest.
k
Nine (for population estimates) and 36 (other data).
HARRIS AND MACDONALD—NESORYZOMYS SWARTHI POPULATION ECOLOGY

l
FWS (Fish and Wildlife Service), 1996, Rice rat Oryzomys palustris natator. Multi-species recovery plan for south Florida, United States, http://www.fws.gov/southeast/vbpdfs/species/mammals/srra.pdf.
m
But previous capture data available.
215
216 JOURNAL OF MAMMALOGY
analysis of a sample of the resident population confirmed that
this skewed sex ratio and operational sex ratio were weighted
by transient males. Of the 82 marked individuals recaptured on
control grids, 38 were male and 44 were female (v2 ¼ 0.878,
d.f. ¼ 1, P ¼ 0.349).
The area of the truncated MCP and 100% MCP of male
N. swarthi significantly exceeded that of female N. swarthi
(Mann–Whitney U ¼ 27, n ¼ 12 males and 11 females, P ¼
0.016 and U ¼ 33.5, n ¼ 12 males and 11 females, P ¼ 0.045,
respectively; Table 2). Mean range span was similar for males
and females (t ¼ 1.779, d.f. ¼ 21, P ¼ 0.090; Table 2). Ranges
of males overlapped those of multiple females and there was
some intrasexual overlap as well (Fig. 6). However, overlap
statistics were not analyzed and are not presented because
home-range data were only collected for a subset of animals
present in the areas. The majority of males (9 of 12) and
females (10 of 11) were in breeding condition. In 2004,
significantly fewer resident males from 2003 were recaptured
on control grids (C1, I1, and I2) than resident females from
2003 (19.2% versus 65.4%, v2 ¼ 11.345, d.f. ¼ 1, P ¼ 0.001).
DISCUSSION
When Clark (1980) found that O. bauri had high survivor-
ship and low reproduction relative to congeners of other
geographic areas he did not know if this strategy was specific
to O. bauri or a common feature of Galápagos rodent life his-
tory. Our account supports the latter in that reproduction, survi-
val, and population stability of both species appear to be
converging on the life history strategy characteristic of desert
Heteromyid rodents (French et al. 1975).
Our study of N. swarthi confirms that the abundance of all
4 extant oryzomyine rodents of the Galápagos is positively
related to vegetation density (Clark 1980; Dowler and Carroll
1996; C. W. Eshelman, in litt.), suggesting that these species
are resource-limited. Our results suggest that food, rather than
protective cover, is the finite resource, as concluded for
O. bauri (Clark 1980), because the mean adult body weight of
N. swarthi was correlated with rainfall and the rate of
disappearance did not vary with habitat type as would be
expected if predation by raptors varied with shrub cover. Food
availability correlates with rainfall and the arrival of the wet
season rains presumably triggered the start of the reproductive
period in December, followed by a peak in pregnancy in April
before ceasing in May, the end of the wet season. This strict
seasonality of reproduction was most evident in the breeding
condition of males. Clark (1980) described a similar breeding
pattern for O. bauri, with reproduction recorded in March and
May. Ultimately, embryo production by O. bauri was limited
by the quantity of rainfall, presumably through food limitation
(Clark 1980), and the fecundity of N. swarthi appears to be
similarly restricted.
According to the model of Kenagy and Bartholomew (1985),
the traits exhibited by N. swarthi suggest adoption of a pulse-
averaging response to the temporal ephemerality of resources
in the Galápagos arid zone. A high proportion of individuals
became sexually active on cue each year and females bred once
Vol. 88, No. 1
a year. The proportion of breeding females (pregnant, lactating,
or both) was comparable across years despite the substantial
difference in rainfall. However, although there was evidence
for postpartum breeding in 2002, 100% and 94% of females
appeared to be limited to single litters during the dry years of
2003 and 2004, respectively. This suggests that females adjust
their reproductive output according to resource availability,
perhaps through failed implantation or embryo reabsorption, as
implied for O. bauri and as predicted by the pulse-averaging
strategy (Kenagy and Bartholomew 1985). Further support for
this hypothesis comes from the slow maturation of young and
lack of breeding in the natal year.
After recruitment in the wet season, juveniles reached adult
size by the end of the dry season. The annual survival rate of
23.2% is lower than the 37% recorded for O. bauri but these
same individuals were alive after 500 days, whereas the
proportion of survivors dropped to 13% for O. bauri (Clark
1980). Maximum time known alive for an individual
N. swarthi was 812 days (27 months) but this record has since
been exceeded by recaptured animals aged at approximately 34
months and in their 3rd reproductive season (data collected in
February 2005 by S. D. Gregory). The maximum survival
recorded for O. bauri was 599 days and this shorter longevity
probably is explained by its relatively smaller body size of 74 g
for males and 55 g for females (Western 1979). Nevertheless,
the high survival rates of both species are striking by
comparison to the continental Oryzomyini, few of which sur-
vive for more than a year (Table 3). Furthermore, the com-
parison highlights a discrepancy in the length of the breeding
season. The continental Oryzomyini either have a relatively
extended breeding season or may breed throughout the year,
with reproductive peaks where and when climate and resource
availability allow (Bergallo and Magnusson 1999; Feliciano
et al. 2002; Negus et al. 1961). An exception is the long-tailed
colilargo (Oligoryzomys longicaudatus) of temperate Chile and
Argentina, for which we could find no accounts of continuous
breeding. However, fecundity may instead be boosted by
multiple litter production in this irruptive species (Table 3). In
contrast, the breeding season of Galápagos Oryzomyini is
truncated by the onset of the long dry season and although the
litter size seems average for an oryzomyine rodent, we have no
evidence to suggest that they produce more than 2 litters in
years with good rainfall. This compressed reproductive season,
coupled with extended longevity, appears to buffer any density
fluctuations because population levels of N. swarthi and
O. bauri are remarkably stable, in contrast to the erratic
dynamics of other tribe members (Clark 1980; Table 3).
In summary, the high annual survivorship, compressed
breeding period, and numerical stability of the Galápagos
Oryzomyini appear to be adaptations to the high probability of
reproductive failure under conditions of extremely variable
rainfall and food limitation in desert habitats, as experienced by
heteromyid rodents (Kenagy and Bartholomew 1985). This life
history strategy sets the Galápagos Oryzomyini apart from
other South, Central, and North American species, where
a comparative release from climatic and resource constraints
selects for the maximization of reproductive output at the cost
February 2007 HARRIS AND MACDONALD—NESORYZOMYS SWARTHI POPULATION ECOLOGY
of shortened longevity. The desert-adapted life histories of the
Galápagos species are impressive because their ancestors were
not well adapted to dry environments and oryzomyine rodents
of semiarid habitats lack the physiological adaptations to xeric
conditions typically seen in desert-dwelling rodents (Best 1988;
Meserve 1978; Ribeiro et al 2004).
Other commonalities of life history within the Galápagos
Oryzomyini include sexual dimorphism and a male-biased sex
ratio in the total number of individuals captured (Clark 1980).
This male bias was more pronounced for the operational sex
ratio of N. swarthi during the breeding season, suggesting
that competition for access to receptive females may be high
(Clutton-Brock and Parker 1992). Because the sex ratio of the
resident population was close to unity and male and female
survival rates were equivalent, but males had a lower in-
terannual recapture rate, we conclude that the male bias in
overall number of individuals captured was caused by transient
males. This also may be the case for O. bauri. A hypothesis of
greater mobility by males is further supported by the larger
extent of home ranges of males compared to those of females
for both N. swarthi (this study) and O. bauri (Clark 1980).
Ranges of male N. swarthi overlapped those of several females
and there was some overlap with other males. In contrast,
ranges of females appeared largely exclusive, although this
cannot be concluded with certainty because we did not track all
females in the area. Nevertheless, female territoriality seems
logical in N. swarthi, a species that relies on ephemeral, patchy,
slowly renewed foods such as seeds and fruits. In turn, female
territoriality renders territorial defense by males inefficient and
males benefit instead from extensive ranges overlapping both
sexes (Ostfeld 1990). The resultant spacing pattern is sug-
gestive of a promiscuous or polygynous mating system (e.g.,
Gaulin and Fitzgerald 1988; Shier and Randall 2004). Further
work is needed to ascertain the proximate and ultimate causes
of dispersal and philopatry, and the social organization of N.
swarthi. Understanding social behavior may be crucial to the
conservation of this species through its effects on the minimum
threshold density required for population persistence (Lidicker
2007).
RESUMEN
Especies de bosque de la tribu Oryzomyini, ancestralmente
continentales, como el cricétido endémico de las Islas
Galápagos, han tenido que adaptarse al desierto tropical agreste
de las islas. Luego del reciente redescubrimiento del Santiago
nesoryzomys (Nesoryzomys swarthi) endémico a la Isla
Santiago en los Galápagos, nosotros llevamos a cabo el primer
estudio sobre la ecologı́a de ésta especie. Nuestros resultados
de 3 años de estudio revelaron una media anual sobrevivencia
de 23.2% y un periodo máximo de sobrevivencia de 812 dı́as.
La actividad reproductiva fue restringida a la estación hùmeda
con una proporción anual estable de hembras reproductivas y
un pico constante de hembras preñadas en abril. La
probabilidad de una segunda camada en el mismo año se
incrementó con relación al aumento de la precipitación cuando
2 camadas fueron producidas. El crecimiento y el desarrollo de
217
juveniles fueron lento y no se reprodujeron en el primer año.
Las correlaciones positivas entre la precipitación y la masa
media del cuerpo de adultos y entre la densidad de la
vegetación (particularmente el cacto pera espinoso [Opuntia
galapageia]) y los niveles de la población apoyaron una
hipótesis de la limitación del alimento. Las comparaciones con
el Galápagos oryzomys (Oryzomys bauri), endémico a la Isla
Santa Fe, y una revisión de los miembros continentales del
tribu Oryzomyini sugiere que el efı́mero e imprevisible
ambiente de la zona árida de Galápagos ha provocado que
N. swarthi y O. bauri seleccionen una estrategia de sobrevi-
vencia relativamente alta y reproducción baja que se observa
más tı́picamente entre los Heteromyidae del desierto que en
otros miembros de Oryzomyini. Presentamos tambien datos
sobre proporción de sexo, ámbito de hogar y fidelidad al
territorio que juntos indican, en este estudio, un sistema de
acoplamiento promiscuo o poligamia. Nuestros resultados
pueden ayudar a dirigir unas estrategias futuras de conserva-
ción requerida para proteger esta especie de roedor en peligro.
ACKNOWLEDGMENTS
We thank the Galápagos Conservation Trust, Flora and Fauna
International, Columbus Zoo, and the Peoples Trust for Endangered
Species for financial support. We thank the staff of the Charles Darwin
Research Station and the Galápagos National Park Service, especially
B. Phillips and B. Cooke, for their collaboration and logistic support.
We also thank F. Cruz and the Project Isabela team for their logistic
support. We are incredibly grateful for the field assistance provided by
S. Gregory and A. Illfield. Finally, we thank J. Wolff and C. Dickman
for providing useful comments on an earlier draft of this manuscript.
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Submitted 31 October 2005. Accepted 5 June 2006.
Associate Editor was Douglas A. Kelt.