Seasonality of reproduction in the three largest terrestrial rodents of French Guiana forest

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Original investigation

Seasonality of reproduction in the three largest terrestrial rodents of French Guiana forest By G. Dubost, O. Henry and P. Comizzoli Muse´um national d’Histoire naturelle, Paris, France; Smithsonian’s National Zoological Park, Washington, USA Receipt of Ms. 13.4.2004 Acceptance of Ms. 15.9.2004

Abstract We investigated the main life history of the three largest terrestrial rodents of French Guiana forest: the acouchy (Myoprocta exilis), the agouti (Dasyprocta leporina) and the paca (Agouti paca), using data collected during several years. There were noticeable differences among the species in sexual maturation and degree of seasonality in reproduction. Percentage of pregnant females, births and juveniles, and body weight of juveniles decreased progressively from the acouchy, through the agouti to the paca. The acouchy was by far the most seasonal: no births occur in the period August–October, 56% of births were encountered in November–January; consequently, young form an unique cohort in the population. The agouti was also seasonal, but to a lesser degree. Newborns appeared in every period of the year in paca, without any formation of cohort of young. These differences tended to be linked to the seasonal importance of fruits in diets, the most aseasonal species having the most diversified diet during the poor fruit season. r 2005 Elsevier GmbH. All rights reserved. Key words: Large rodents, reproduction, seasonality, French Guiana

Introduction The reproductive characteristics and population dynamics of tropical rainforest mammals have been rarely investigated. This is mainly due to the difficulty in gathering sufficient data on these mostly elusive and solitary species, especially terrestrial ones. A widespread belief is that rainforests are fairly stable biomes that do not undergo marked seasonal changes. Actually, this assertion denotes more a lack of knowledge than a reality, because in many countries there are noticeable seasonal differences both in rainfall and primary production. For example, in French Guiana, during the driest month the

rainfall is 16% (6.4 times less) that occurring during the wettest month, and the minimal monthly number of both plant species and individuals in fruit is 14% that found during the maximum production season (Sabatier 1983; Henry 1994). Due to the small variation of day length in such latitudes, one can hypothesize that these environmental factors can play a key-role in the regulation of reproduction of the primary consumers. Three large rodents are present in forests of French Guiana, the acouchy Myoprocta exilis, the agouti Dasyprocta leporina, and the paca Agouti paca. They are important

1616-5047/$ - see front matter r 2005 Elsevier GmbH. All rights reserved. doi:10.1016/j.mambio.2004.09.001 Mamm. biol. 70 (2005) 2
93–109

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species of the guild of terrestrial frugivores. In Guiana, as in the whole South America, they occupy ecological niches fitted by small duikers and cervids in other continents (Dubost 1968). Due to the lack of information on their biology, especially their annual reproductive cycles (Emmons and Feer 1990), we decided to analyse their main characteristics. The main objectives of this study were (1) to examine seasonal variation in reproductive patterns, (2) whether the main life history events such as gestation, birth, and growth rate were correlated with variation in food resources, (3) whether differences in reproductive patterns among species are in accordance with morphological and ecological differences, and (4) if their reproductive characteristics correspond to their places in the guild of terrestrial frugivores.

Material and methods The French Guiana forest

number per km

Tropical forest covers more than 90% of French Guiana (2–61N; 52–541W). From the viewpoint of floristic diversity, it is a primary evergreen forest, dominated by a few tree families (Sabatier and Prevost 1990). The mean day temperature is 26–27 1C, and annual mean rainfall and relative humidity vary from 2000 to 4000 mm and from 80% to 100%, respectively (data Me´te´o France). The year has a monthly mean rainfall of

241.37113.4 mm with two wet seasons (a short rainy season in December–January and a longer and more intense rainy season from March to June), separated by two drier periods, the driest lasting 5 months, from July to November (Fig. 1). In order to estimate the fruit production of the forest, we used the fruit counts made by Sabatier (1983) and Henry (1994) during 2 consecutive years in two different localities (St. Elie in 1980–1982 by Sabatier; Paracou in 1989–1990 by Henry), by the method of ground transects, with samples made every 2 weeks along a 1500 m  1 m trail. The four annual fruit samplings (i.e. 2 sites  2 years) were identical to each other. The pooled data showed that there were marked variations in fruiting, with a maximum situated between the two rainy seasons (Gayot et al. 2004). From the number of both plant species and individuals in fruit, four periods of equivalent length can be clearly distinguished: (1) February–April, the main fruiting season; (2) May–July, a period of fruit decrease; (3) August–October, the lowest fruit production season; (4) November–January, the flowering and early fruiting period. These seasonal events occur every year throughout French Guiana (Henry 1994, 1999; Barret 2001), which leads us to consider this pattern as typical for the entire sampled region.

Species studied The three species belong to two families of hystricomorph rodents: the Dasyproctidae (M. exilis Wagner, 1831, x=1.2 kg, and D. leporina L., 1758, x=4.7 kg) and the Agoutidae (A. paca L., 1766, x=7.9 kg). Apart from common taxon characters (large size, four teeth in each jaw,

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precocial young), they differ in some biological features, and form three progressive stages in body weight and gestation length at the lower limit of the guild of large terrestrial frugivores (Table 1).

Data collection and analysis All samples came from the northern half of French Guiana, from specimens hunted by native human populations for their own subsistence during several years. The reproductive organs, skulls, and stomachs of most specimens were recovered immediately after death, fixed in 10% formalin and preserved in sealed tanks. A total of 35 male and 38 female acouchies, 67 male and 93 female agoutis, and 49 male and 45 female pacas was available for this study. Data recorded for each individual included date of death, sex, and, when possible, body weight. Broad age categories were based on the presence of one (premolar only), two (premolar and first molar:o4–5.5 months), three (second molar erupted: between 4-5.5 and 12 months) or four teeth (third molar erupted:412 months). Considering that tooth eruption takes place at nearly the same age in the three species (Kleiman 1970; Collett 1981; Henry 1994), we distinguished individuals with only one, two or three teeth (less than 12 months), which were generally immature (with respect to the

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sperm production in males and the first gestation in females), from other animals, which were reproductive subadults (with four teeth, but still deciduous premolar) or adults. For males, we recorded both the weight of each testis and the presence of spermatozoa in the vas deferens of the cauda epididymis. Female genital tracts were investigated to determine the presence, number, sex and weight of embryos in each uterine horn. The age of each embryo, and consequently its corresponding conception and birth dates, was calculated with the general formula of growth of mammal embryos, established by Huggett and Widdas (1951): W 1=3 ¼ aðt  t0 Þ; where W is the weight (in grams) of the embryo of age t, a the growth rate, t the estimated age (in days) of the embryo of weight W, and t0 the minimum age at which embryos can be weighed in the species. T 0 was estimated from values obtained for comparable species. Knowing both the gestation length and the birth weight for each species, it was possible to determine its embryo growth formula: W 1=3 ¼ 0:06ðt  20Þ in acouchy; W 1=3 ¼ 0:06ðt  22Þ in agouti; W 1=3 ¼ 0:09ðt  24Þ in paca. Because few specimens were sometimes collected during a given month (e.g. four acouchies in January, five agoutis in July, five pacas in October), we pooled data by 3-month periods corresponding to the four clear seasons of fruiting defined above. Monthly data were not considered separately,

Table 1. Main characteristics of the species, according to: aKleiman (1970), bWeir (1974), cCollett (1981), d Dubost (1988), eEmmons and Feer (1990), fHenry (1994), gpers. data. Body weight range in brackets. Species

Myoprocta exilis

Dasyprocta leporina

Agouti paca

Body weight (g)

1191 (750–1450)g

4712 (4000–5800)g

7934 (5600–9800)g

Gestation (days)

99a

112b

118c

Newborn

Precocial Hairy, eyes opene,g

Precocial Hairy, eyes opene,f,g

Precocial Hairy, eyes openc,e,g

Habitat

Dry land Only mature forestsd,e,g

Dry land. Forests, cultures and open landd,e,f,g

Waterside. Forests, cultures and open landc,e,g

Shelter

Holes, burrows or fallen hollow trunksd,e,g

Rest most often on the groundd,e,f,g

Burrows or fallen hollow trunkse,g

Activity

Diurnald,e,g

Diurnald,e,f,g

Nocturnalc,e,g

Diet

98% fruitsg

87% fruits, 2% leaves, 4% fibre-stems1, 6% animalsf,g

84% fruits, 7% leaves, 8% fibre stemsg

Food reserves

Many nuts burried singly in the groundd,e,g

Many nuts buried singly in the groundd,e,g

No reserves knowne,g

Social life

Solitaryd,e,g

Mostly in paird,e,g

In pair. Travels alonee,g

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except for births and body weights. Comparisons among age categories and seasons were analysed with w2 or, due to some small samples cited above, with the non-parametric Kruskal–Wallis one-way analysis of variance by ranks KW-test. Additional comparisons between two successive seasons were made with the Mann–Whitney U-test. Correlations were established with the Spearman rank-order coefficient rs (Siegel and Castellan 1988).

Results Testis weight and sperm production In all species, the differences of testis weight among age categories were always highly significant (KW ¼ 14:8; Po0:001; n ¼ 35 in acouchy; KW ¼ 32:9; Po0:001; n ¼ 67 in agouti; KW ¼ 28:8; Po0:001; n ¼ 49 in paca). The acouchy was the species with the greatest increase of testis mass between the 2tooth and the 3-tooth age classes (5.7 times heavier vs. 3.7 and 4.4 for the agouti and paca: Table 2). The three species showed also an increase of testis mass between the 3-tooth stage and the reproductive age (respectively, 3.4 times more for the acouchy, 3.8 for the agouti and 2.6 for the paca). There were no significant seasonal variations in the average testis weight of mature individuals in any species (Table 3). However, in acouchies, the testis weight was inferior in May–July to August–October (U ¼ 23; P ¼ 0:05; n1 ¼ 8; n2 ¼ 11), as to the next season November–January. For

agoutis, it was inferior in May–July to August–October (U ¼ 11; Po0:025; n1 ¼ 5; n2 ¼ 13), as to the other seasons. Maximum testes weight was reached in August–October in acouchies and agoutis, and November– January in pacas. As with testis weight, the differences in sperm production among age categories were always significant (w2 ¼ 3:83; df ¼ 1; Po0:05 in acouchy; w2 ¼ 17:05; df ¼ 2; Po0:001 in agouti; w2 ¼ 7:44; df ¼ 1; Po0:01 in paca). Sexual maturation was reached in the 3-tooth category, which is between 4–5.5 and 12 months (Table 2). Although the differences among the three species were not significant, the acouchy had the lowest percentage of mature individuals with spermatozoa. Likewise, there were no seasonal variations in percentages of mature individuals with spermatozoa. Percentages were comparable, except in acouchy, which had a more pronounced minimum. The maximum percentage occurred in February–April in acouchy and agouti, but later (in May–July) in the paca (Table 3). Thus, a link with testis weight was not evident in these three rodents, where maximal percentages were observed almost 6 months before or after maximal testis weights. Percentage of pregnant females Females usually were first pregnant after they had erupted their second molar (3-tooth stage

Table 2. Mean testis weight (in grams, with standard deviation), and number and percentage (in brackets) of individuals with spermatozoa in the cauda epididymis, according to the age category. *Difference with the number of testes weighed, due to the absence of cauda epipidymis in one specimen collected. Age category

M. exilis

D. leporina

A. paca

o4–5.5 months (2 teeth) Testis weight % with spermatozoa

n=2 0.027 – 0.087 0/2

n=10 0.17170.030 0/10 (0%)

n=4 0.66570.098 0/4

Between 4–5.5 and 12 months (3 teeth) Testis weight % with spermatozoa

n=5 0.32770.488 1/4*

n=8 0.63170.153 1/8 (12.5%)

n=13 2.9370.50 3/13 (23.1%)

412 months Testis weight % with spermatozoa

n=28 1.12170.141 15/28 (53.6%)

n=49 2.3870.17 34/49 (69.4%)

n=32 7.5870.35 20/32 (62.5%)

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Table 3. Mean testis weight (in grams, with standard deviation), and percentage of mature individuals with spermatozoa in the cauda epididymis in different species, according to the period of the year. *Difference at Po0.05 with the following period. **Number different from that in Table 2, due to the absence of date of death for four mature males. February–April

May–July

August–October

November–January

M. exilis (n=28) Testis weight % with spermatozoa

0.8370.15 75.0

0.7170.15* 25.0

1.4170.28 63.6

1.3770.25 60.0

D. leporina (n=49) Testis weight % with spermatozoa

2.2470.26* 79.0

1.3970.30* 75.0

2.8370.35 53.9

2.5270.34 69.2

A. paca (n=28**) Testis weight % with spermatozoa

7.4270.45 69.2

8.0370.54 80.0

7.0170.72 56.3

9.6771.28 50.0

Table 4. Number and percentage (in brackets) of pregnant females, according to the age category. Age category

M. exilis

D. leporina

A. paca

o4–5.5 months (2 teeth) Between 4-5.5 and 12 months (3 teeth) 412 months

0/2 0/7 (0%) 9/29 (31%)

0/13 (0%) 2/8 (25%) 29/72 (40.3%)

1/1 3/9 (33.3%) 28/35 (80%)

— Table 4), with the exception of acouchies, in which females apparently were not sexually mature before 12 months old. Differences in percentages of pregnant females among age categories were significant in all species (w2 ¼ 3:86; df ¼ 1; Po0:05 in acouchy; w2 ¼ 9:58; df ¼ 2; Po0:01 in agouti; w2 ¼ 6:67; df ¼ 1; Po0:01 in paca). From the acouchy to the paca, there was a regular increase in the percentage of pregnant females in both the 3- and 4-tooth stages. The acouchy was the species with lowest pregnancy rates and the paca that with highest, as confirmed by the occurrence in this species of one pregnant female in the 2tooth category. In the three species, there was a regular increase of percentage of pregnant females from May–July to November–January, followed by a decrease in February–April (Fig. 2a–c). These seasonal differences progressively decreased in magnitude from the acouchy to the paca, being significant in

acouchies (w2 ¼ 10:4; df ¼ 3; Po0:02) and agoutis (w2 ¼ 18:5; df ¼ 3; Po0:001), but not in pacas. Thus, the greatest difference in percentages of pregnant females between seasons was, respectively, 100% in the acouchy, 60% in the agouti, and 39% in the paca. The theoretical dates of conception, calculated from both the date and weight of embryos collected, showed different maxima according to the species: August–October for acouchy and agouti, but later in November– January for the paca. Seasonal pattern of births and litter size February–April was the most favourable season for births, except in acouchies, where the maximum occurred 3 months earlier. Thus, from the acouchy to the paca, February–April became progressively more important for births than November–January (Fig. 2). As the percentage of pregnant females, the seasonal differences in the

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Fig. 2. Percentage of pregnant females of 3–4-tooth stages (white bars) and percentage of births (calculated from embryo weights—black bars), according to the season: (a) acouchy (n ¼ 36); (b) agouti (n ¼ 80); (c) paca (n ¼ 44). M–J — May–July; A–O — August–October; N–J — November–January; F–A — February–April. Seasonal variations significant at Po0.02 in acouchy, and Po0.001 in agouti for pregnant females, and at Po0.05 in agouti for births. ** or *Difference at Po0.01 or Po0.05 with the following period.

ARTICLE IN PRESS Seasonality of reproduction in the three largest terrestrial rodents

distribution of births decreased gradually from the acouchy (between 0% and 55.6%), through the agouti (from 5.6% to 44.4%), to the paca (8.6%–38.6%). This seasonal distribution of births was significant in agoutis (w2 ¼ 9:4; df ¼ 3; Po0:05). The litter size was equivalent in the acouchy and the agouti, with, respectively, 2.070.50 (n ¼ 18; range: 1–3) and 2.170.50 (n ¼ 32; range: 1–3) young per litter, 2 times superior to the paca (1.070.18 young; n ¼ 29; range: 1–2). In all species, the newborns are furred, with eyes open, and very precocious. They stay a short time in the nest, and may be even seen in the open as soon as few days of age in the agouti (pers. obs.). The newborn weight relative to the mother weight was comparable in the different species, except in the agouti: respectively, 9.4% in the acouchy (100/1067 g), 8.5% in the paca (700/8250 g), but only 3.2% in the agouti (160/5060 g). Thus, the relative weight of the whole litter decreased from the acouchy to the paca, as it is usual in mammals with increasing adult body weight: respectively, 18.8% in the acouchy, 8.5% in the paca, but again only 6.4% in the agouti. Knowing the gestation length, the percentage of pregnant females and the mean number of young per litter, it was possible to compute the mean number of litters and young theoretically produced by each female per year. The paca, with a higher percentage of pregnant females (Table 4), had 2 times more litters per year than the acouchy and agouti (2.5 vs., respectively, 1.1 and 1.3) and produced finally as many young per year (2.5 vs., respectively, 2.3 and 2.6).

Percentage of sexually immature individuals in the population As the number of young born per year, the mean percentage of immature individuals (o 12 months) was comparable in the three rodents: 31.5% in acouchy, 25.8% in agouti, and 32.1% in paca. This percentage fluctuated according to the seasons in all species (Fig. 3), but overall variations were only significant in acouchy (w2 ¼ 14:19; df ¼ 3;

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Po0:01). In all species, the percentage was high in May–July, but the minimum occurred at different periods: November–January in the smallest species, February–April in the agouti, and February–April and August– October in the paca. Thus, the percentage of immature individuals was significantly superior in May–July to February–April in agouti (w2 ¼ 4:44; df ¼ 1; Po0:05). Considering the mean number of young theoretically produced by each female per year and the number of reproductive females captured, it was possible to compare the number of young collected in each species with that theoretically produced during a year. A total of 77.6% of young ‘‘disappeared’’ during the first 12 months of life in agouti, contrary to acouchy and paca, where percentages were, respectively, 59.3 and 63.3. Each species apparently had its own pattern. In acouchy and paca, the young ‘‘loss’’ was more marked before 4–5.5 months than after (respectively, 60% in the 2-tooth vs. 41.3% in the 3-tooth stages, and 77.8% vs. 49.1%); in contrast, young ‘‘disappeared’’ more during the 3-tooth stage than before in agouti (respectively, 81.9% and 72.4%).

Body weight of young and mature individuals The mean body weight of immature individuals varied according to the season, significantly in acouchies (KW ¼ 8:26; Po0:02; n ¼ 31). It was lower in May–July than in August–October (U ¼ 42; Po0:025; n1 ¼ 11; n2 ¼ 16), where it was again higher than in February–April, the season with the lowest immature body weight (U ¼ 1; Po0:01; n1 ¼ 4; n2 ¼ 11). The same occurred in agoutis (KW ¼ 11:52; Po0:01; n ¼ 15), but significant variations were not recognized in pacas. By recording the different body weights available for immature individuals at the exact date where they were collected, all individuals were classified according to a single and clear weight cohort beginning in November–March in acouchies (Fig. 4a), as confirmed by several other young collected during this period with comparable body measurements (but not weighed). Thus, not any immature individual with body weight

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Fig. 3. Percentage of immature individuals (o12 months) in the population, according to the season. n of individuals in: (a) acouchy: 38; (b) agouti: 48; (c) paca: 40. Seasonal variations significant at Po0.01 in acouchy. *Difference at Po0.05 with the following period. Other abbreviations as in Fig. 2.

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inferior to 580 g (i.e. less than 3.5 months of age) was collected between July and October among the 40 weighed individuals; in contrast, no immature individual with body weight superior to 545 g was collected between November and March among 18 individuals. This phenomenon was still apparent in agouti (Fig. 4b), but not in paca (Fig. 4c). Significant seasonal changes also occurred in the body weight of mature animals in acouchies (KW ¼ 15:58; Po0:01; n ¼ 64) and agoutis (KW ¼ 8:72; Po0:05; n ¼ 26). May–July was the period with lighter body weights in acouchies and agoutis. This may be due to an increased death of old and heavy individuals, because proportion of matures in populations was lower (Fig. 3). But, contrary to immature individuals, February–April seemed the period with highest mature body weights in these two species: superior to May–July, respectively, at Po0:005 (z ¼ 2:73; n1 ¼ 11; n2 ¼ 28) and Po0:05 (U ¼ 0:5; n1 ¼ 3; n2 ¼ 5), as to August– October. Like immature individuals, there were no significant variations in pacas. Thus, in acouchy and even in agouti, there was a complete inversion in body weight fluctuations between immature and mature individuals. Correlations with fruit production Due to the small annual variations of the day length under such latitudes (35 min — Bureau des longitudes, Paris), no significant correlation between photoperiod variation and any

reproductive parameter was established. The same observation was made for temperature and humidity values. Finally, few correlations appeared with rainfall, perhaps because it shows two peaks during the year, while most reproductive parameters were unimodal. Nevertheless, there were inverse correlations between variations in testis weight and conception rates in acouchies and agoutis, and rains (rs ¼ 1; P ¼ 0:05; n ¼ 4). Because the diets of these three rodents are chiefly composed of fruits, variations of reproductive and population characteristics reported above were compared to the fruit production of the forest, evaluated in terms of number of both plant species and individuals in fruits. Testis weights did not vary according to the fruit production (Table 5). In the two largest species, percentages of individuals with spermatozoa followed changes in fruit production, but with a delay of 3 months in the paca. In the three rodents, percentages of pregnant females mirrored fruit variations with an advance of 3 months corresponding almost to their gestation length. Nevertheless, births were not synchronized with the fruit production, except in pacas. Percentages of immature individuals in the small species appeared linked to fruit variations, but not in the two largest ones. Lastly, as seen above and contrary to mature individuals, the body weight increase in immature acouchies and agoutis was negatively correlated with the fruit production. From analyses of stomach contents (pers. data), the acouchy is the most frugivorous (in

Table 5. Correlations between the reproductive characteristics of the species and the fruit production (number of plant species and/or individuals in fruit). *—rs=1; P=0.05; n=4; o—rs=1; P=0.05; n=4.

Testis weight % with spermatozoa % pregnant females (3 months in advance) % births % immature individuals (3 months of delay) Immature body weight (opposite)

M. exilis

D. leporina

A. paca

NS NS * NS * o

NS * * NS NS o

NS * * * NS NS

ARTICLE IN PRESS Seasonality of reproduction in the three largest terrestrial rodents

average 98% of dry weight of stomach contents) and has the smallest seasonal variation in fruit consumption (98–99%). The agouti is second, with an average of 87% fruit and seasonal variations ranging from 83% to 91%. The paca is third, with an average of 84% fruit, but more marked seasonal variations (from 75% to 91%). This order is the opposite, of course, with respect to other diet components. The acouchy always consumes few fibre and stems (1.6%) and negligible quantities of leaves or animals (0.2–0.4%). The agouti has a more varied diet, consuming on average 1.9% leaves, 4.3% fibre and stems (particularly in February–April, the main fruiting season, where they attain 11.9%) and 6.2% insects, or 12.4% of its non-fruit diet. The paca consumes an average of 15.4% items other than fruit, with 12.1% leaves and 7.7% fibre and stems in August–October and again 10.1% leaves and 13.9% fibre and stems in November–January, in periods of lowest and early fruiting. Thus, due to these secondary foods, each species, except the acouchy, copes with the variations in fruit production by finding other foods at different seasons: diets can vary seasonally as much as 8% in agoutis, 23% in pacas, but only 2% in acouchies, which appear the most rigid of all. There were no seasonal correlations in either species between quantities of fruits consumed and reproductive and population characteristics. But, there was a correlation between percentages of fruits consumed and seasonal variations in pregnancy rates, percentage of births and percentage of immature individuals (rs ¼ 1; P ¼ 0:05; n ¼ 4). There was an inverse relation between percentages of fruits consumed and indices of diet diversity. The acouchy, the most frugivorous rodent, had by far the lowest food diversity (Shannon index H 0 ¼ 0:95  0:16). There was an increase of this index from this species to the paca: 1.7770.07 in agouti, and 1.8870.14 in paca. But, the inverse correlations between seasonal variations in pregnancy rates, births and immature individuals, and indices of diet diversity were weaker than the direct correlations existing with percentages of fruits

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consumed, except for immature individuals (rs ¼ 1; P ¼ 0:05; n ¼ 4). In sum, most females were pregnant 3 months prior to the fruit maximum, but this was less evident in pacas (where pregnant females were also frequent during the fruit maximum) than in acouchies and agoutis. Consequently, most births occurred during the fruit maximum, except in acouchies, and to a lesser degree in agoutis, where births occurred equally during the preceding period. Lastly, most immature individuals were observed in the period following the maximum fruit production, but again less distinctly in pacas, in which many young also were born before or during the period of maximum fruit production (Fig. 5). As expected, the amplitude of the seasonal variations of these three factors decreased from the gestation to the immature individuals, but it was always greater in acouchies than in the other species (e.g. respectively, 100, 56, and 30 in acouchy; 60, 39, and 23 in agouti; 39, 30, and 21 in paca). Considering the conception as the first stage of these reproductive events, it appeared that all species had their lowest conception rates in May–July, the period of fruit decrease, but, in contrast, a high level in August–October, the lowest fruit production season. Acouchi and agouti conceptions followed this annual scheme, whereas paca conceptions were most frequent in November–January, the early fruiting period.

Discussion Sexual maturation The sexual maturation of these three large Guianan rodents takes place in the 3-tooth age class, between 4–5.5 and 12 months, as reported in several other studies: puberty reached at 6–13 months in Myoprocta pratti (Kleiman 1970), at 6 months in Dasyprocta aguti (= leporina-Roth–Kolar 1957); first conceptions at 9 months in Agouti paca (Smythe 1991). So, in apparent contrast to its lighter body weight, the acouchy is the species with the latest sexual maturation of females.

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Seasonality of reproduction The percentages of individuals with spermatozoa were never correlated to conception

rates, their maxima occurring curiously 6 months out of phase in the three large rodents. Nevertheless, the maxima of the main reproductive events (conceptions,

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percentages of pregnant females, of births, and of young) most often succeeded logically one another in the three species. The acouchy was clearly the most seasonal rodent, this character being reinforced by the presence of a single and clear age cohort among sampled young, as shown by their regular increase of average body weight. By comparing our birth data for agoutis and pacas with those available from other wild or captive specimens (Anonymous 1961; Collett 1981; Matamoros 1982; Meritt 1989; Smythe 1991; Henry 1994; pers. data), we observe that most births occur everywhere between February and April, although births in another period can appear in captivity, as expected. Between sites, there are also comparable values for the monthly maxima and minima. Similar seasonal fluctuations of reproduction are known for other South or Central American species, although maxima are not strictly the same as for the Guianan species. M. pratti shows a seasonal maximum of births 2.2 times higher than the minimum in captivity in London (Kleiman 1970). Births of D. punctata are 5.3 times more frequent in one given period in captivity in Chicago (Meritt 1983), and percentage of births of captive D. variegata fluctuate between 0% and 42% in London (Anonymous 1961). Comparable seasonality also exists in tropical terrestrial frugivores of other world’s regions. But, the more or less absolute seasonal stop of reproduction in acouchies, and to a lower degree in agoutis, is apparently rare among terrestrial frugivores of tropical forests, unlike arboreal ones (Dubost and Feer 1992). As exposed above, most specimens were obtained from local hunters, which could engender some bias, e.g. in the proportion of juveniles in the population. However, natives of tropical rainforests do not select any type of prey, shooting every encountered animal. Besides, other studies on censuses or live-captured and released individuals (Dubost 1988) confirmed the results obtained from hunted specimens, especially on the seasonality of the reproduction in these species.

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Correlations with fruit production and consumption Unlike rains, whose direct effect on reproduction is difficult to prove, the fruit production of the forest corresponds to the quantity and quality of seasonal food for frugivores, and may determine reproductive success, as it was evidenced in other South-American rodents (Bergallo and Magnusson 1999). In males, the fact that only variations of percentage of individuals with spermatozoa were apparently linked to fruit production in agoutis and pacas confirms that males are generally always in reproductive activity throughout the year in the tropics. In contrast, reproductive events of females are apparently more correlated to fruit production: percentages of pregnant females, of births, and of immature individuals in the population. The differences in reproductive seasonality between the paca on one hand and between the acouchy and the agouti on the other hand appeared linked to the relative percentage of fruits and of the other components in the diets. Since degrees of seasonal diet variations are the inverse of their degrees of reproductive seasonality, it is possible to conclude that a varied diet is apparently a positive factor for a terrestrial frugivore to exhibit a reproduction more or less continuous in Guianan forests. In contrast, the more strictly frugivorous a species is, the more it depends on a very seasonal resource, and the more the reproduction is seasonal. Another factor must be considered when studying the reproductive seasonality of rodent species. During the season of fruit abundance, some rodents cache seeds that are later used during the season of fruit scarcity. This could theoretically favour more continuous reproduction. As far we know, the tendency to cache seeds exists in acouchies and agoutis, but not in pacas (Smythe 1970; Forget 1990; Henry 1994), and this does not coincide with an increasing seasonality in the species. Smythe (1978) reported that young D. punctata suffered 70% mortality in the non-fruiting season. This mortality is not evident in French Guiana, where the lowest

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percentage of young agoutis occurs in February–April, the main fruiting season. Furthermore, body weights of young acouchies and agoutis, the most frugivorous species, increased significantly between February–April and August–October, the lowest fruit production season, which does not argue in favour of an effect of fruit reduction on young growth and survival. The apparent lack of births in acouchies and, to a lesser degree, in agoutis during the dry season could be related to the relative length and severity of this period in French Guiana. This season lasts 5 months, when the minimum number of fruit species and fruiting sites on the ground reaches only 14% of the maximum (Sabatier 1985; Henry 1994). In contrast, the most severe dry season in N–E Gabon lasts in average only 3 months, and the minimum number of fruiting species and sites is 38–45% of the maximum (Feer 1989). Annual production of young Although embryos of few days of age were difficult to detect, the observed pregnancy rates can be considered as valuable estimates of the real proportions of pregnant females. Thus, there was a regular increase in the reproductive capacities and especially in the percentages of pregnant females from the acouchy to the paca, both the average percentage of pregnant females and the number of litters per year being nearly 2 times higher for this last species in French Guiana than in other countries. Nevertheless, because the average number of young per litter is lower in pacas, in accordance with data published from same or similar species (M. pratti — Kleiman 1970; D. punctata — Meritt 1983; A. paca — Collett 1981; Matamoros 1982; Smythe 1991), the mean number of young produced by a female per year is comparable among the three species. In our samples, theoretical mean intervals between two successive pregnancies in the same female, calculated from both percentage of pregnant females and gestation lengths, were, respectively, 256 days in acouchy, 219 days in agouti, and 35 days in paca. Concerning the agouti, our data are superior

to the 115–190 days reported for captive D. leporina (= aguti — Henry 1994; Roth–Kolar 1957), and to the 40–140 days for wild D. punctata in Panama, according to Smythe et al. (1982). Such intervals permit a normal nursing of the first litter in acouchy and agouti, because this phase lasts only 42–84 days in M. pratti (Kleiman 1970, 1974), and 84–140 days in D. aguti (Roth-Kolar 1957; Kleiman 1974). This signifies that a new pregnancy does not usually occur during the suckling phase in these two species, as supposed by Weir (1971). In contrast in the paca, the interval is largely inferior to the 97–294 days reported for wild and captive animals (Collett 1981; Matamoros 1982; Meritt 1989; Smythe 1991), as well as to the 90 days reported for the suckling phase (Matamoros 1982). In this species, several females were collected both pregnant and lactating, and, according to Matamoros and Pashov (1984), a post-partum oestrus occurs in this species. Since the three species give birth annually to an equivalent number of young, the proportion of immature individuals in the population is comparable among them. Nevertheless, the rate of ‘‘disappearance’’ of young before 10–12 months is not directly proportional to their initial number, being superior in agouti to the acouchy and paca. One cannot explain this difference by the diets (the agouti occupies the second rank in percentage of fruits eaten, vs., respectively, the first and third for the acouchy and the paca), the activity rhythms (the agouti is diurnal as the acouchy), or the developmental stages of young (all species give birth to well developed and nidifugous young). One could suppose an influence of the body weight, because the seasonality of many reproductive events decreases from the acouchy, the lightest ‘‘large’’ rodent, to the paca, the heaviest. Nevertheless, this is not apparently a rule, because the spiny rat, another hystricomorph species of the same forests and weighing 170–550 g, is clearly aseasonal (Henry 1994). Apart from the seasonal fruit reduction, predation pressures could play a role in the ‘‘loss’’ of young in the populations. The agouti is a very conspicuous diurnal animal which is by far the most active on the ground,

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even during the suckling phase of young. Running capacities of agoutis at every age and stage are well known (Smythe 1978 for D. punctata; pers. obs. for D. leporina), which could be also related to the 2–3 times lower relative weight of its young and whole litter to mother’s weight in comparison with other species. Eight % of young agoutis captured were less than 1 month of age (with only one premolar), contrary to 0–0.7% in other species. The increase of ‘‘disappearance’’ of young agoutis during the 3-tooth class (82%) compared to the 2-tooth class (72%), in contrast to the other species, could also be related to predation pressure, because most young usually leave the parental territory by becoming sexually mature (Smythe 1978). This does not occur in other species, which apparently have no territories and live more solitarily. Indeed, predation appears more important in French Guiana than in the Panama and Colombia populations investigated by Smythe (1978), Collett (1981), and Smythe et al. (1982). Although reproductive performances are equal or even superior in French Guiana than in Panama and Columbia, the percentages of young (less than 1 year) in agouti and paca populations are lower in the first country (respectively, 26% vs. 44–68% for agouti; and 32% vs. 42% for paca). This could be due to the type of biotopes: those of Colombia and Panama are a mixing of savannas and gallery forests or a semi-deciduous forest, inhabited by many people and apparently without or with few natural predators, unlike the major parts of the French Guiana rainforest. This is supported by the very high densities cited by these authors for the two species (50–100 km2), compared to French Guiana: mostly 2–9 km2 (Richard-Hansen, pers. com.).

Comparison with other terrestrial mammals Among the other terrestrial rodents of French Guiana forests, two species, the murid Oryzomys capito velutinus and the spiny rat Proechimys cuvieri have been studied (Henry 1994). Both are of smaller

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body weight than the three large species (respectively, 20–70 g, and 170–550 g), have a shorter gestation length (respectively, 26 days and 61–66 days: Everard and Tikasingh 1973; Weir 1974), and life expectancy (respectively, 1 year and 2 years in the wild: Fleming 1971; Everard and Tikasingh 1973), and present very different reproductive characteristics: they are more precocious in terms of testis growth and start of spermatogenesis in males (from 2.7 months), and start of puberty in females (as soon as 1.6 and 2–3 months, respectively); they produce a much larger number of young (respectively, an average of 3.6 and 3.1 per litter, and 11.9 and 31.6 per year). There is no clear seasonality in their reproduction: in O. capito, there is no apparent birth season; in spiny rats, birth and immature percentages vary little among periods, and a seasonal increase of the mean body weight of young is lacking. In this respect, they are comparable to the small rodents of other tropical forests (Duplantier 1982; Bergallo and Magnusson 1999). The fact that Oryzomys and the spiny rat show higher seasonal diet variations than the three large rodents (fruit percentages fluctuating, respectively, between 26% and 77%, and 33% and 81%; insect percentages between 22% and 74%, and 18% and 65%), confirms the probable link existing between a seasonally variable diet and a more or less continuous reproduction in such tropical forests. At the opposite, the collared peccary Tayassu tajacu, a large frugivorous species (x=22 kg; 61.6% of fruits in diet), also studied by Henry (1994) in French Guiana, show many reproductive characteristics comparable to those of the acouchy, the paca, but especially the agouti: age at first conception; percentage of mature pregnant females; mean number of young produced per female per year; proportion of immature individuals in the population; seasonal succession of percentages of pregnant females, of births, and of young, in accordance with the fruit production. This is consistent with the places these three large terrestrial rodents occupy in the vertebrate community of neotropical forests.

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Acknowledgements The major part of the data was collected between 1989 and 1991, according to a grant of the Ministe`re des De´partements et Terri-

toires d’Outre-mer (Cordet 88-126). Many thanks to Dr. L. H. Emmons, Carrie O’Brien and the anonymous referees for their helpful comments and corrections of the manuscript.

Zusammenfassung Jahreszeitliche Fortpflanzung von den drei gro¨Xten terrestrischen Nagern im Regenwald von Franzo¨sisch Guayana Die Untersuchungen beziehen sich auf die wichtigsten Merkmale der Lebenszyklen der drei gro¨Xten terrestrischen Nager, Acouchi, Aguti und Tieflandpaka, im Regenwald von Franzo¨sisch Guayana, unter Verwendung von u¨ber mehrere Jahre wa¨hrenden Beobachtungen, die beachtenswerte Unterschiede in bezug auf Geschlechtsreife und Fortpflanzung aufzeigen. Fortpflanzung und Populationsstruktur, wie Prozentsatz tra¨chtiger Weibchen, Geburten, Auftreten von Jungen sowie deren Ko¨rpergewicht verringern sich kontinuierlich von Acouchis u¨ber Agutis hin zu Tieflandpakas. Wa¨hrend Acouchis die bei weitem am sta¨rksten ausgepra¨gte jahreszeitlich gebundene Fortpflanzung mit 56% der Geburten in den Monaten November bis Januar zeigen, konnten von August bis Oktober keine Geburten beobachtet werden. Demzufolge treten die Jungen in der Population als eine einheitliche Altersklasse auf. Eine periodische Fortpflanzung zeigen auch Agutis, wenn auch weniger ausgepra¨gt, wohingegen bei Tieflandpakas u¨ber das gesamte Jahr hinweg Junge geboren werden, ohne jegliche Bildung von einer Altersklasse. Diese Unterschiede scheinen an die jahreszeitlich bedingte Produktion von fu¨r die Erna¨hrung wichtigen Fru¨chten gebunden zu sein, wobei die am wenigsten periodische Art in der fru¨chtearmen Zeit das breiteste Nahrungsspektrum aufweist. r 2005 Elsevier GmbH. All rights reserved.

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Authors’ addresses: G. Dubost and O. Henry, Muse´um national d’Histoire naturelle, Ecologie et gestion de la biodiversite´, UMR 5173 MNHN-CNRS, 57 rue Cuvier, F-75231 Paris Cedex 05 (e-mail: [email protected].) P. Comizzoli, Smithsonian’s National Zoological Park, Department of Reproductive Sciences, Conservation and Research Center, 3001 Connecticut Avenue NW, Washington DC 20008