ORIGINAL ARTICLE

Peter R. Brown Æ Nguyen Phu Tuan

Grant R. Singleton Æ Dao Thi Hue Æ Phung Thi Hoa

Phi Thi Thu Ha Æ Tran Quang Tan Æ Nguyen Van Tuat

Population dynamics of Rattus argentiventer, Rattus losea,and Rattus rattus inhabiting a mixed-farming systemin the Red River Delta, Vietnam

Received: 20 April 2005 / Accepted: 25 July 2005 / Published online: 15 September 2005� The Society of Population Ecology and Springer-Verlag Tokyo 2005

Abstract Rodent pests cause significant damage tolowland irrigated rice crops in the Red River Delta ofnorthern Vietnam. Data from a 4-year study wereexamined to look at the population dynamics of thericefield rat, Rattus argentiventer (representing 50% ofcaptures), the lesser ricefield rat, Rattus losea (30% ofcaptures), and the black rat, Rattus rattus complex (9%of captures) that inhabit the irrigated mixed-croppingsystem. We tested the hypothesis that these rodent spe-cies were breeding in response to the availability of high-quality food provided by crops rather than in responseto rainfall. The abundance of rodents fluctuated annu-ally, with a main peak following the spring rice crop,and a secondary peak following the summer rice crop.There was a strong relationship between the monthlyabundance of rats and rainfall, but a weak relationshipbetween monthly rates of increase and rainfall. Therewere distinct peaks in breeding activity during thereproductive stages of the rice crops suggesting thatchanges in crop stages were more important than rainfallin this seasonal, but irrigated agroecosystem. The modallitter size for R. argentiventer was 8 (mean of 8.67±0.20SE, range 2–16), where the mode for R. losea, was 7(mean of 7.32±0.15 SE, range 3–14). Management ofthese species needs to be conducted prior to the onset ofthe main breeding seasons.

Keywords Black rat Æ Breeding Æ Interspecificcompetition Æ Lesser ricefield rat ÆLowland irrigated rice Æ Ricefield rat

Introduction

Rodents are a significant problem for agriculture inVietnam, particularly for lowland irrigated rice in the twomain rice-production areas in Vietnam—theMekong andRed River Deltas (Singleton and Petch 1994; Brown et al.1999; Singleton 2003). Rodents damage 20–30% of theannual pre-harvest rice crop. It has been argued that if thedamage can be reduced to 5% there would be enough riceto feed an additional 7.8 million Vietnamese people/an-num (Singleton 2003). It is therefore desirable to reducethe impact of rodents on rice crops, to increase foodsecurity, and improve the economic stability for thecountry through increased exports.

The ricefield rat, Rattus argentiventer (Robinson andKloss) is recognized as the main rodent pest in thelowland irrigated rice-growing areas of Vietnam (Brownet al. 1999; Lan et al. 2003), but other sympatric speciesinclude the lesser rice field rat (Rattus losea, Swinhoe),the black rat (Rattus rattus complex; for discussion ontaxonomy see Aplin et al. 2003b), the brown rat (Rattusnorvegicus, Berkenhout), the Pacific rat (Rattus exulans,Peale), bandicoot rats (Bandicota indica, Bechstein andBandicota savilei, Thomas), and Mus species. Thesespecies also are likely to damage crops. Populations ofR. argentiventer have been studied in Malaysia andIndonesia (Lam 1982; Tristiani et al. 1998; Leung et al.1999; Jacob et al. 2003) where they comprise >95% ofrodents inhabiting rice fields. In Vietnam, anotherpopulation of R. argentiventer has been studied (Brownet al. 1999), and little is known about the populationdynamics of R. losea and R. rattus in intensive ricecropping systems, especially in terms of the factors thatdrive changes in abundance and breeding.

P. R. Brown (&) Æ G. R. SingletonCSIRO Sustainable Ecosystems,GPO Box 284, 2601 Canberra, ACT, AustraliaE-mail: Peter.Brown@csiro.auTel.: +61-2-62421562Fax: +61-2-62421505

N. P. Tuan Æ D. T. Hue Æ P. T. Hoa Æ P. T. T. HaT. Q. Tan Æ N. Van TuatNational Institute of Plant Protection, Hanoi, Vietnam

Present address: G. R. SingletonInternational Rice Research Institute, Metro Manila, Philippines

Popul Ecol (2005) 47:247–256DOI 10.1007/s10144-005-0228-x

The distribution of R. argentiventer includes lowlandcropping areas from northern Vietnam to southernVietnam, through the lower reaches of the MekongRiver Valley into Cambodia, lowland areas of Thailand,all of Malaysia, most islands of Indonesia and someislands of the Philippines (Marshall 1977; Aplin et al.2003a). R. losea generally is found only in northern andsouthern Vietnam, Cambodia, Thailand, southern partsof China and in Taiwan. The geographic distribution ofthe various genetic forms of the R. rattus complex is stillto be resolved (Aplin et al. 2003b). The main economicimpact of these species is damage to crops, but they alsorepresent a source of disease for humans. For example,R. losea can carry ticks infected with Lyme disease (Shihet al. 1998) and harbours hanta virus (Nitatpattana et al.2002). In the central highlands of Vietnam, R. rattus is areservoir of plague (Yersinia pestis; Suntsov et al. 1997).Therefore, understanding population dynamics of thesespecies may assist in reducing damage to crops, andlessening the chance of disease transmission to humans.

Farmers use a range of control techniques to reducerodent damage (Tuan et al. 2003). There is a growingrecognition that these conventional methods are notmaintaining rodent populations below an economicthreshold (when costs of control outweigh yield gains),and so ecologically based rodent management practicesare being developed to reduce the impact of these spe-cies on rice crops (Singleton 1997; Singleton and Brown1999). This strategy requires a good understanding ofthe population dynamics of the principal pest species.The objective of the current study was to develop abetter understanding of the population dynamics of thethree main pest species of rodents in a lowland mixedrice agro-ecosystem in the Red River Delta, Vietnam, asa basis for developing ecologically based managementpractices. We tested the hypothesis that these rodentspecies were breeding in response to the availability ofhigh-quality food provided by crops rather than inresponse to rainfall. We examine population dynamicsof R. argentiventer, R. losea and to a lesser extent,R. rattus, over 4 years in Vinh Phuc Province. We re-port on temporal changes in population abundance,rate of population increase in relation to rainfall,breeding dynamics and percentage of juveniles in thepopulation.

Materials and methods

Study site

The study was located near Tien Phong village, Me LinhDistrict, Vinh Phuc Province, 40 kmnorth ofHanoi in theRed River Delta of northern Vietnam (21�08¢N,105�45¢E). Two sites were used; these were untreatedcontrol sites of a larger study assessing methods for con-trolling rodents. Each site was approximately 100 ha andthe distance between each sitewas 1 km.This locationwaschosen because an outbreak of rodents in the area in 1997/

1998 substantially damaged rice crops (N. P. Tuan,unpublished data). The principal crop grown in the area isrice. There are two main rice-growing seasons each year,spring (transplanted late February and harvested midJune) and summer (transplanted mid July and harvestedlate September). Other crops, grown throughout the year,are vegetables (broccoli, cabbage, chilli, kohlrabi, onion,pumpkin, and tomato) and flower crops (chrysanthe-mum, rose). In March 2002, 51% of the land was undervegetable crops, 20% was under rice crops, 17% wasunder flower crops, 10% was channel banks and road-sides, and 2% was fallow. In June 2002, 40% was underrice crops, 35%of the landwas under vegetables, 11%wasfallow, 10% was channel banks and roadsides, and 4%was under flower crops. At other times, particularlyduring the summer rice crop, up to 100% of the land wasplanted to rice.

Summers are hot and wet, and winters are cool anddry. Maximum temperatures in Hanoi are 15–25�C inspring, 30–36�C in summer, 25–30�C in autumn, and 10–15�C in winter. The annual average rainfall wasapproximately 1,675 mm, most falling between May andSeptember (summer). Rainfall was below average in1998, 1999, 2000, and 2002 (80, 93, 76, and 87% of thelong-term mean, respectively) and was above average in2001 (135% of the long-term mean). Farmers irrigatedtheir crops using water supplied by channels originatingfrom large storage dams in nearby hills.

Live-trapping

Two replicate lines of 20 live cage traps were set in eachof three main situations denoting: (1) big channel banks,>2 m high and >2 m wide carrying irrigation water; (2)medium banks, about 1 m high and 1 m wide, smallerchannels or paths between fields; and (3) small banks,<0.3 m high and <0.3 m wide separating rice fields.Trapping occurred for 4 consecutive nights for a total of480 trap nights per site per month. Traps were con-structed from open wire mesh (150 · 150 · 400 mm)with a hinged, sprung door. Traps were baited withroasted vegetables. Trapping occurred each month fromApril 1999 to November 2002. One site was trappedmonthly, the other less frequently depending on avail-ability of labour. Trapping results are presented as theabundance of rats captured each month. Upon capture,each animal was identified to species, marked with anear punch, weighed, and lengths of tail, hind foot, andear were measured to assist with identification to species.Breeding condition was assessed for females (lactating ifteats were raised and free of hair at their base; pregnancyby palpation).

Monthly records of rainfall (mm) were obtained forHanoi from monthly weather reports for Vietnam. TheHanoi weather station was approximately 30 km fromthe study sites. The relationship between rainfall andrats was assessed using two methods. Firstly, a simplelinear regression was performed on the abundance of

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rodents and monthly rainfall. Secondly, the exponentialrate of increase per month (r; rate of change) wascalculated as r=ln(rat abundance for month t/ratabundance for month t�1). This relationship effectivelyremoves the effect of density and looks at how much thepopulation increases or decreases in response to rainfall.To ascertain whether rainfall, as a surrogate for foodsupply, was an important factor in driving the rodentpopulations, exponential rates of increase were corre-lated against monthly rainfall that was lagged by 0–6months, accumulated rainfall of 1–6 months and 6-monthaccumulated rainfall but lagged by 0–6 months.A similar approach has been used for other rodents(Pseudomys hermannsburgensis, Notomys alexis, andMus domesticus) in arid central Australia (Southgateand Masters 1996), and M. domesticus in wheat fields inAustralia (Brown and Singleton 1999). The periods oftime when populations increased and decreased werethen defined (spring increase, summer decrease, summerincrease, and winter decrease), and the rates of increaseover these periods were analysed by a one-way ANOVA.

The abundance of the two most common species,R. argentiventer and R. losea, was analysed using athree-way ANOVA using ln-transformed abundance ofrats with month, year, and species as factors. Theoccurrence of adult females breeding (lactating and/orpregnant as determined by palpation) was comparedover time using generalized linear models (analysis ofdeviance) for binomially distributed data (breeding yesor no) using the logit link. Probabilities were determinedusing the F statistic using df/residual df. The effect ofmonth, year, and species (R. argentiventer and R. losea)and all interactions were examined. Linear regressionanalyses were conducted to determine whether the pro-portion of adults in breeding condition could be pre-dicted by rainfall or crop stage. Crop stage was scoredon a scale of 1–10 (sowing/transplanting through toharvest) and analysed separately for spring and summerrice crops. This scaling of crop stage is a rough estimateof food supply and assumes that it increases linearlyfrom sowing to harvest (Tristiani and Murakami 2003).The presence of juveniles trapped in the population wascompared over time with generalized linear models for

binomially distributed data (juveniles yes or no). Thesame analysis was conducted for juveniles as for adultfemales breeding, with the addition of sex in the model.

Kill-trapping

Kill-trapping was conducted each month to collect adultfemale R. argentiventer and R. losea to assess breedingcondition in more detail. Kill-traps and live-traps werelocated at least 200 m away from the regular trappinglines. The aim was to collect at least 15 adult femaleR. argentiventer and R. losea each month where capturerates permitted. After capture, rats were weighed andmeasured and assessed for breeding condition as for live-trapped animals, then autopsied to ascertain conditionof uterus, number of embryos, trimester of embryodevelopment, and number and sets of uterine scars.

The occurrence of adult females breeding (presence ofembryos in uterus) was compared over time using thesame analysis as used for live-captured animals above.Litter sizes were compared over time using generalizedlinear models for Gaussian distributed data (ln-trans-formed counts of embryo number per pregnant female).Probabilities were determined using the F statistic usingdf/residual df. The effect of month, year, and species(R. argentiventer and R. losea) and all interactions wereexamined.

Results

Abundance of rats

The overall abundance of rats during this study was low,with the majority of trapping sessions yielding <40animals/480 trap nights per month. A total of 411 ratswere captured from 20,340 trap nights from site 1 (44trapping sessions) and 458 rats were captured from12,420 trap nights from site 2 (27 trapping sessions).Abundance peaked in July 1999 at 52 and 82 rats forsites 1 and 2, respectively. The abundance of rats wasstrongly related to the cycle of cropping and was similar

Month

A J A O D F A J A O D F A J A O D F A J A O D

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1999 2000 2001 2002

M J S N J M M J S N J M M J S N J M M J S N

Fig. 1 Average abundance(±SE) of rats from both sitesand monthly rainfall (mm,vertical bars) from Hanoi(30 km from study site). Theshaded horizontal bars at thebottom of the graph representthe approximate timing of thespring and summer rice cropsand winter vegetable crops

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on each site, with two peaks in abundance each year, thehigher peak occurring shortly after harvest of the springrice crop. A second peak occurred shortly after theharvest of the summer rice crop (Fig. 1), but was not asobvious for site 2 possibly because it was trapped lessfrequently. Abundance declined shortly after harvest ofthe summer crop and into the winter period, thennumbers of rats were low through until the middle of thespring rice crop when rat numbers started to increase. Asignificant relationship existed between the monthlyabundance of rats and monthly rainfall with no lag(y=0.060x+3.113; F1,42=57.95; P<0.001), explainingover half of the variation in abundance (R2=0.580).

Rate of increase

Rainfall was not a significant factor in the rate of changein population abundance of these rodents during thestudy. The highest correlation between the monthlyexponential rate of increase (r) and rainfall was for zerolag and zero accumulation for rainfall (Pearson’s cor-relation=0.334; P=0.029; n=43). The correlationcoefficients for all other comparisons for lagged andaccumulated rainfall were poor (range of Pearson’scorrelation �0.342 to �0.122).

On average over the 4 years of study, the monthlyrates of increase were generally positive in January,March, May, June, July, and October, with all othermonths having a negative rate of increase (Fig. 2).There were three consecutive months when the rate ofincrease was positive (May, June, and July; spring-in-crease phase), and this coincided with the increase inabundance of rats leading to the peak in populationabundance after the harvesting of the spring rice crop inJuly each year. There was only one month, October,when the rate of increase was positive during the sum-mer rice crop. There were large variations about themean for the monthly exponential rate of increase forDecember to May (large SEs, Fig. 2) due to the lowpopulation abundance in these months (winter-decreasephase). There was a significant difference betweenthe rates of increase between seasons (F3,11=16.65;P<0.001) with rates of increase higher during thespring-increase phase (May–July; r=1.24±0.25 SE)

than the summer-increase phase (October; r=0.88±0.21 SE) and rates of increase were lower during thesummer-decrease phase (August–September; r=�1.15±0.41 SE) than the winter-decrease phase (November–April; r=�0.58±0.12 SE).

Species composition

Most rats captured were R. argentiventer (49.7%),followed by R. losea (30.0%), R. rattus complex (8.6%),Bandicota species (B. indica and B. savilei, 5.4%), Musspecies (3.6%), R. norvegicus (0.8%), and Suncus muri-nus (0.1%), with 1.8% of captures not identified.R. argentiventer were more abundant (4.6 rats/month)than R. losea (2.6 rats/month) (F1,46=15.80; P=0.003)(Fig. 3). There was a difference among months(F11,46=9.57; P<0.001), but no difference among years(F3,46=2.40; P=0.080). The year-by-species interactionwas significant (F3,46=3.72; P=0.018) showing thatR. argentiventer was more abundant in most years (meanabundance per month, 1999=5.8, 2000=5.3, 2001=3.8,2002=2.9) except for in 2001 when R. losea was moreabundant (mean abundance per month, 1999=3.1,2000=1.4, 2001=4.1, 2002=2.3). The abundance ofR. rattus generally remained low, and followed similarpatterns in abundance to the dominant species throughthe year, with peaks in abundance following the harvestof the spring and summer rice crops.

Breeding ecology from live-trapping

There was no difference in the percentage of adult femalesin breeding condition between R. argentiventer (39.2%)and R. losea (43.0%) (F1,233=0.001; P=0.977), but sig-nificant differences among months (F11,234=5.194;P<0.001) (Fig. 4). Therewas anobvious peak in breedingactivity in September (92.2%) for both species (summerrice crop), but the peak in breeding activity for the springrice crop was less clear, probably because of small samplesizes. Approximately 50% of adult females were inbreeding condition in June. Little or no breeding wasfound in January (14.3%), March (14.3%), November(3.8%) or December (0.0%). The apparent high rates of

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Fig. 2 Exponential monthlyrate of increase (r) averagedover two sites for each monthfrom April 1999 to November2002, Vinh Phuc, Vietnam(±SE). A positive r indicatesthat there is an increase inpopulation size, whereas anegative r indicates a decrease inpopulation size. The shadedhorizontal bars at the bottom ofthe graph represent theapproximate timing of thespring and summer rice cropsand winter vegetable crops

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breeding observed in February and April were related tolow sample sizes, but nevertheless, breeding was occur-ring. There was no difference between years (P=0.605)and the species by month interaction was not significant(P=0.445).

Linear regressions showed that crop stage was a poorpredictor of adult breeding females for both R. argen-tiventer (R2<0.01; P>0.05) and R. losea (R2<0.02;P>0.05) for both spring and summer rice crops. Fur-thermore, rainfall was a poor predictor of the percentageof adult females in breeding condition. For R. argenti-venter, the best fit was for 5-months lagged rainfall(R2=0.147; F1,28=4.83; P=0.036), and for R. losea, thebest fit was for 2-months lagged rainfall (R2=0.226;F1,30=10.31; P=0.003).

Recruitment

Juvenile animals were present in nearly all months, ex-cept in March and April (Fig. 5). There was a significantdifference in the presence of juveniles between months(peak in October of 42.7%; F11,670=11.61; P<0.001), adifference between species (R. argentiventer=13.3%,R. losea=16.9%; F1,669=6.00; P=0.015), a differencebetween years (1999=20.8%, 2000=13.7%,2001=8.8%, 2002=12.1%; F3,666=4.80; P=0.003), butno difference between sexes (males=14.1%;females=15.5%; P=0.679). The month by year inter-action was significant (F23,628=3.25; P<0.001), as wasthe species by sex interaction (F1,613=11.04; P<0.001).No other interactions were significant.

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M J S N J M M J S N J M M J S N J M M J S N

Fig. 3 Relative abundance ofthe three main rodent species(Rattus argentiventer, R. loseaand R. rattus) and other species(R. norvegicus, Bandicota spp.,Mus spp., and Suncus murinus),averaged across two sites (noteach site was trapped eachmonth). The shaded horizontalbars at the bottom of the graphrepresent the approximatetiming of the spring andsummer rice crops and wintervegetable crops

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4,3 3,3 5,2 0,1 6,2 19,12 16,27 23,40 6,12 22,10 18,6 2,1

R. argentiventerR. losea

Fig. 4 Breeding of adult female R. argentiventer (open bars) and R.losea (hatched bars), Vinh Phuc Vietnam, 1999–2002 from live-trapping, showing percentage of adults females pregnant (deter-mined by palpation) and/or lactating (mean±SE). Sample sizes are

shown at the top of each figure and represent R. argentiventer andR. losea, respectively. The shaded horizontal bars at the bottom ofthe graph represent the approximate timing of the spring andsummer rice crops and winter vegetable crops

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Breeding ecology from kill-trapping

The percentage of adult females in breeding conditionfor autopsied adult females showed different resultsfrom that observed by live-trapping (lactating and/orpregnancy through palpation) for both R. argentiventerand R. losea. On average, pregnant females were foundin each month for both R. argentiventer and R. loseaexcept November (Fig. 6). There was no significantdifference in the percentage of adult females pregnantfor R. argentiventer (mean=60.1%) and R. losea(mean=60.4%) (F1,601=0.162; P=0.688), suggestingthat conditions that govern breeding activity are thesame for both species. There were two distinct peaks inthe percentage of adult females pregnant, occurring

from April through to June (reproductive stage of thespring rice crop, mean of 70% pregnant) and in August(tillering stage of the summer rice crop, mean of 83%pregnant). The percentage of adult females that werepregnant was lower than expected by the crop stage inSeptember and October (ripening stage of the summerrice crop, approximately 50% pregnant). Furthermore, aconsiderable percentage of adult females were pregnantthrough winter and early spring, prior to the reproduc-tive stage of the spring rice crop (>30% pregnant).There were significant differences among months(F11,602=12.58; P<0.001), and a significant differenceamong years (1999=82.0%, 2000=55.0%,2001=58.4%, 2002=64.5%; F3,598=5.70; P<0.001).There was a significant month by year interaction

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12,7 10,31 4,6 6,2 16,95 2,33 70,56 110,71 10,19 74,36 42,16 7,3

R. losea

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Fig. 5 Percentage of juvenile R. argentiventer (open bars) and R.losea (hatched bars) in the population averaged for each month,Vinh Phuc Vietnam, 1999–2002 from live-trapping. Juvenile R.argentiventer were classified as animals <50 g and R. losea as<45 g. Sample sizes are shown at the top of each figure and

represent R. argentiventer and R. losea, respectively. The shadedhorizontal bars at the bottom of the graph represent the approx-imate timing of the spring and summer rice crops and wintervegetable crops

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9,11 9,8 16,18 19,23 29,15 41,37 48,58 77,76 20,19 30,45 12,6 4,2

R. argentiventerR. losea

R. argentiventerR. losea

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Fig. 6 Breeding of adult femaleR. argentiventer and R. losea,Vinh Phuc Vietnam, 1999–2002from kill-trapping, showinga average number of embryosper pregnant female ±SE, andb average percentage of adultfemales pregnant as determinedfrom kill samples (±SE). Datapooled from two sites. Samplesizes are shown at the top ofeach figure and represent R.argentiventer and R. losea,respectively. The shadedhorizontal bars at the bottom ofthe graph represent theapproximate timing of thespring and summer rice cropsand winter vegetable crops

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(F26,561=5.70; P<0.001), but no other interactions weresignificant (P>0.05).

Linear regressions showed that crop stage was a goodpredictor of pregnancy rates of adult R. argentiventer inspring (R2=0.445; F1,15=12.12; P=0.003), but not forsummer (R2=0.095; F1,14=1.48; P=0.244). Similarly,crop stage was a good predictor of pregnancy rates ofadult R. losea in spring (R2=0.516; F1,13=13.87;P=0.003), but not for summer (R2=0.025; F1,14=0.37;P=0.555). This indicates that the rats were respondingstrongly to the availability of resources provided by therice crops during the spring rice crop (increasing fromsowing through to harvesting), but the crop stage couldnot explain changes in the percentage of adult femalespregnant in the summer rice crop. Rainfall, however,was a poor predictor of the percentage of adult femalespregnant. For R. argentiventer, the best fit was for zero-lagged rainfall (R2=0.088; F1,41=3.93; P=0.054), andfor R. losea, the best fit was for 1-month lagged rainfall(R2=0.050; F1,38=2.02; P=0.164).

There was a significant difference in the litter sizeamong months (F10,339=2.90; P=0.002), with averagelitter sizes highest in May (mean=9.7±0.6 SE) andlowest in March (mean=6.3±0.3 SE) (Fig. 6a). Therewere no differences between years (P=0.098) or for themonth by species interaction (P=0.463). The litter sizefor R. argentiventer was higher (mean=8.67±0.20,mode=8, range 2–16, n=182) than for R. losea(mean=7.32±0.15, mode=7, range 3–14, n=168)(F1,338=16.09; P<0.001). The data for placental scarsshowed a similar pattern; the mode for R. argentiventerwas 9 (mean of 8.22±0.21, range 3–14, n=124), and themode for R. losea was 7 (mean of 7.30±0.19, range 2–13, n=123). The overall minimum weight of pregnantR. argentiventer was around 50 g, whereas the minimumweight of pregnant R. losea was around 45 g, andtherefore these weights represent a crude cut-off pointbetween juvenile and adult females for both species.These weights are used above to look at the percentageof juveniles in the population.

Discussion

The rodent populations inhabiting the lowland irrigatedmixed farming system in the Red River Delta ofnorthern Vietnam annually fluctuate in abundance.There was a strong relationship between abundance ofrodents and monthly rainfall, which reflected the highlyseasonal rainfall pattern, the cropping pattern used bythe farmers, and the cold temperatures during winterwhen rice could not be grown. The combination of thesefactors lowered the breeding rate of females over winterand early spring. The rodent populations in the areahave been known to reach high densities and signifi-cantly damage crops, such as the outbreak in 1997/1998(N. P. Tuan, unpublished data). Nevertheless, fromApril 1999 to November 2002, populations were rela-tively low. The peaks in abundance of rodents coincided

with harvesting of the spring and summer rice crops. Thepeak in abundance of rodents following the spring ricecrop was higher than the peak following the summer ricecrop. There were three consecutive months of positiverates of increase during the spring rice crop and only onemonth of positive rates of increase during the summerrice crop. The abundance of rodents was low during thewinter season when little or no breeding occurred.

We were unable to recapture any marked animal sowe have little understanding of whether our trap catch isa good measure of actual abundance. Our trap catch islikely to be influenced by a range of factors includingtrappability, environmental conditions and anthropo-genic activities such as ploughing and harvesting. Fur-thermore, we were unable to conduct more sophisticatedcapture–mark–recapture analyses or to examine changesin density rather than abundance alone. A more reliablemeasure of the dynamics of the rats is from pregnanciesof females from kill-trapping, and we found that therewere changes in the pregnancy rate and litter size of bothR. argentiventer and R. losea over time. There appearedto be strong associations between crop stage and rates ofpregnancy during the spring rice crops for bothR. argentiventer and for R. losea, but not during thesummer crops. Furthermore, rainfall was a poor pre-dictor of pregnancy rates for both species. Based onthese breeding dynamics, we believe that the responsesshown in changes in the abundance of rats over timewould make biological sense, and therefore we areconfident that our observations and findings areappropriate. A radio-tracking study of R. argentiventerin this area showed that most collared animals remainednear their capture location (Brown et al., in press), so itis likely that there is some behavioural response totrapping.

R. argentiventer and R. losea in Vietnam bred duringthe reproductive stages of the two main rice crops, asexpected, but they bred at other times of the year also. Therate of breeding increased through the spring rice crop,presumably as food quality improved, then remainedconstant throughout the summer rice crop. The reason forthis is not clear, but it could be due to the presence of otherhigh-quality food resources available through the summermonths such as grasses found along channel banks, rip-ening vegetable crops, or from grain spilled after harvestof the spring rice crop. In Malaysia and Indonesiabreeding by R. argentiventer is confined to the reproduc-tive stages of the wet- and dry-season rice crops with littlebreeding occurring outside these periods (Lam 1983;Tristiani et al. 1998; Leung et al. 1999). Presumably, bothR. argentiventer and R. losea in Vietnam were obtainingsufficient quality food in their diet from the vegetablecrops and other food sources to initiate or maintainbreeding at timeswhen the ricewas not in the reproductivestage. There is little known about the diet of R. argenti-venter or R. losea in the fields, but they are known to eatcrabs, snails, insects, rice and other plant material (N. P.Tuan and P. R. Brown, unpublished data). Furthermore,given thatR. argentiventer andR. losea have similar levels

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of breeding each month they may be responding to thesame environmental cues. The breeding dynamics of ratsin the Mekong Delta of southern Vietnam were moreclosely aligned to the growth of the main rice crops, andthere was little breeding occurring outside of these periods(Brown et al. 1999).

There appeared to be a positive, although weak,relationship between the monthly exponential rate ofincrease (rate of change) and the monthly rainfall withno lag. This is probably coincidental because no strongpositive relationships existed with lagged or accumu-lated rainfall. Such relationships exist for a range ofother rodent species, including Mastomys natalensis inTanzania (Leirs et al. 1996), P. hermannsburgensis,N. alexis and M. domesticus in central Australian deserts(Southgate and Masters 1996), Peromyscus leucopus in awoodlot in the USA (Lewellen and Vessey 1998), M.domesticus in wheat fields in Australia (Brown andSingleton 1999), Phyllotis darwini in semi-arid Chile(Lima and Jaksic 1999), and for Mus musculus in beechforests in New Zealand (Choquenot and Ruscoe 2000).In general, the above species respond to accumulatedand lagged rainfall and to subsequently improved foodsupply. The relatively poor response shown here indi-cates that rainfall, although highly seasonal, was not asignificant factor in determining the populationdynamics or breeding of R. argentiventer and R. losea inthis irrigated mixed agroecosystem. Moreover, the rela-tionship between the monthly exponential rate of in-crease (rate of change) and rainfall within the samemonth does not make biological sense. If rodents wereresponding to good conditions, a lag period must occurto allow time for plants or other food sources to growand reach a stage of growth where they are highlynutritious before the rodents can respond and com-mence breeding. A delay would then occur from com-mencement of breeding to birth of the young and thenrecruitment into the trappable population. For R. ar-gentiventer and R. losea, this timing would take 3–6months. Therefore, we believe that the rodents wereresponding more to the availability of high-quality foodprovided by irrigated crops including rice and vegetables(such as kohlrabi, tomato, onion, and pumpkin). Thishypothesis was supported by the regression analysis ofincreasing pregnancy rates for both species during thespring rice crop, and then pregnancy rates remained highduring the summer rice crop.

Overall, there was little effect of rainfall on the pop-ulation dynamics or breeding rates of R. argentiventer orR. losea. Rainfall would have little direct impact onthese rodents except during periods of high rainfall andin low-lying areas, where burrows could be flooded.Flooding did not occur during this study. In the MekongDelta of southern Vietnam, Brown et al. (1999) foundthat flooding reduced population abundance of rats, andpresumably affected survival directly.

Tristiani and Murakami (2003) examined the rate ofincrease of R. argentiventer in response to food supply inan enclosure in West Java, Indonesia. They assumed

that nutritional quality linearly increased from trans-planting to harvest of the rice crop. They concluded thatR. argentiventer was able to adapt to the growth stagesof the rice crop by reproducing when food supply wasoptimal (Tristiani and Murakami 2003), but reproduc-tive data were not provided. Furthermore, they did notlook at the response of the population to lagged foodsupply.

The litter sizes for R. argentiventer of eight to nineobserved in this study were generally lower than littersizes of nine to 12 reported for Malaysia and Indo-nesia (Lam 1980, 1983; Murakami et al. 1990) and inKien Giang Province in the Mekong Delta of southernVietnam, where the average litter size for R. argenti-venter was 10.8 (Brown et al. 1999). It is unclearwhether the lower litter size observed for R. argenti-venter in the Red River Delta of Vietnam was due tocompetition with R. losea and other rodent species orbecause of the availability of vegetable crops in themixed irrigated farming system in Vinh Phuc Provinceof Vietnam. Theory suggests that there should be areduction in fecundity, survivorship or growth throughinterspecific competition (Begon et al. 1996). There arefew published examples to support this theory in ro-dents. However, Eccard and Ylonen (2002) found thatreproduction of bank voles in enclosures was nega-tively affected by the presence of field voles, with fewerbank vole females breeding, although, there was nodifference in the litter size between their treatments.Another possibility is that there are latitudinal effectson litter size. While latitudinal effects on the cyclicdynamics of arvicoline rodents have been well studied(Henttonen et al. 1985; Saitoh et al. 1998; Tkadlec andStenseth 2001), there are few studies on the effects oflatitude and litter size. It is generally considered that inthe northern hemisphere there is a positive relationshipwith latitude and litter size, as found for P. leucopus(Long 1973), but Bilenca et al. (1994) found a negativerelationship in the southern hemisphere for Akodonazare. It seems that photoperiod, temperature andavailability of food influence litter size rather thanlatitude alone (Bilenca et al. 1994; Trillmich 2000). Ourdata on R. argentiventer in Vietnam compared to thoseobserved for R. argentiventer in Indonesia andMalaysia are consistent with reduced fecundity,through lower litter size, because of interspecific com-petition with R. losea, and there is a suggestion thatthere is a negative relationship with latitude and littersize.

The minimum weight of pregnant R. argentiventerand R. losea were determined as 50 and 45 g,respectively. The published figures for adult R. ar-gentiventer are slightly heavier. Murakami et al. (1990)found female R. argentiventer with open vagina from28 g body weight (estimated at only 28 days old), butpregnant females from 60 g body weight (estimated as40 days old). Lam (1983) showed that in double-cropped areas, females showed signs of sexual matu-rity with perforated vagina, placental scars and much

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enlarged mammae starting at the 60 g mid-pointweight class (the size of the weight classes was notstated).

Because we found pregnant female R. argentiventerand R. losea above 50 and 45 g respectively, we classifiedanimals that were lighter in weight as juveniles. This wasa crude method for determining the presence of juvenilesin the population. A general observation was thatbreeding was occurring in nearly all months, and as aconsequence, juveniles were observed in nearly allmonths except for the early part of the spring rice crop.

The recapture rate of marked animals was zero for allspecies. It is well known that the recapture rates forR. argentiventer are very low (Brown et al. 1999; Leunget al. 1999; Jacob et al. 2003). Because there were norecaptures of marked animals, it was not possible todetermine the growth rates of individuals or to calculatesurvival. An apparent survival rate could be calculatedbased on the shift of body weights from one month tothe next at a population level; however, little is knownabout the growth rates of R. argentiventer, or whetherthis would be an appropriate method for estimatingsurvival. The age of R. argentiventer can be estimatedfrom eye lens weight (Vejaratpimol and Liat 1983), butthe relationship between eye lens weight and bodyweight was not provided. This requires further investi-gation.

Conclusion

R. argentiventer and R. losea show similar dynamics inthis complex farming system in the Red River Delta,Vietnam. There was a strong relationship between themonthly abundance of rats and rainfall, but a weakrelationship between monthly rates of increase andrainfall. While breeding was occurring during thereproductive stage of the rice crop as expected, somebreeding was occurring outside of these periods, pre-sumably because of the availability of high-qualityfood provided by the vegetable crops. Given thesesimilar dynamics, it is likely that these two speciescompete for resources. There are many interestingecological questions relating to the competition be-tween R. argentiventer and R. losea which can beinvestigated, such as examining diet preferences andusing radio-telemetry to study the habitat use of boththese species. The findings from this study will help torefine the management of the rodent community byfocusing management prior to the onset of the mainbreeding periods.

Acknowledgements We thank all the village heads and farmers in-volved in the project for their support and willingness to participatein the project. Staff of the National Institute for Plant Protection,Vietnam, provided excellent support while in the field and gettingthe project underway. In particular we thank Le Than Hoa, PhamThi Lien, and Pham Van Kien. We thank Drs J. Jacobs and K.Williams for critical comments on the manuscript. This research ispart of the Australian Centre for International Agricultural

Research funded project Management of Rodents in Rice-BasedFarming Systems of Southeast Asia (AS1 98/36) and was con-ducted in accordance with the Australian Code of Practice for theCare and Use of Animals for Scientific Purposes. The approval nos.were WEAEC 98/99-09 and SEAEC 01/02-09.

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