A ten-year demographic history of a population of howler monkeys ( Alouatta palliata ) living in a fragmented landscape in Mexico

Long-term field studies of primates are critical for our understanding of life history and the processes driving changes in demography. Here, we present the first long-term demographic data for the northernmost population of the mantled howler monkey ( Alouatta palliata ). We followed 10 groups of howler monkeys living in a highly fragmented landscape between 2000 and 2011. Forest fragmentation did not seem to play a major role in the dynamics of our population, as the population size remained relatively stable over the 10-year study period, and birth rates and inter-birth intervals were comparable to those of howler monkeys at other sites. Moreover, dispersal events were commonplace, particularly secondary dispersal (individuals emigrating from groups that they had previously immigrated into), which supports the suggestion that this may be an important component of the reproductive strategy of the mantled howler monkey. Finally, we found a marked effect of seasonality on the population dynamics of our study population. In particular, the period of lowest temperatures and resource scarcity between November and March was associated with higher mortality and reproductive inhibition, while the period of resource abundance between April and May was associated with the majority of conceptions and weaning of offspring. This, in turn, could be influencing dispersal patterns in our study area, as male howler monkeys seem to time some of their immigrations into new groups to coincide with the start of the period of higher fertility, while females preferentially joined new groups several months before the onset of this period.


A ten-year demographic history of a population of howler monkeys (Alouatta palliata) living in a fragmented landscape in Mexico
Jurgi Cristóbal Azkarate, Jacob Charles Dunn, Cristina Domingo Balcells, Joaquim Veà Baró Long-term field studies of primates are critical for our understanding of life history and the processes driving changes in demography. Here, we present the first long-term demographic data for the northernmost population of the mantled howler monkey (Alouatta palliata). We followed 10 groups of howler monkeys living in a highly fragmented landscape between 2000 and 2011. Forest fragmentation did not seem to play a major role in the dynamics of our population, as the population size remained relatively stable over the 10-year study period, and birth rates and inter-birth intervals were comparable to those of howler monkeys at other sites. Moreover, dispersal events were commonplace, particularly secondary dispersal (individuals emigrating from groups that they had previously immigrated into), which supports the suggestion that this may be an important component of the reproductive strategy of the mantled howler monkey. Finally, we found a marked effect of seasonality on the population dynamics of our study population. In particular, the period of lowest temperatures and resource scarcity between November and March was associated with higher mortality and reproductive inhibition, while the period of resource abundance between April and May was associated with the majority of conceptions and weaning of offspring. This, in turn, could be influencing dispersal patterns in our study area, as male howler monkeys seem to time some of their immigrations into new groups to coincide with the start of the period of higher fertility, while females preferentially joined new groups several months before the onset of this period.
122 We carried out the first census of our study site in 2000. Of the 55 forest fragments that are found in 123 our study site, we found 21 to be inhabited with at least one howler monkey and recorded a total 124 population of 316 individuals living in 43 groups (Cristóbal-Azkarate et al., 2005). We began studying 125 four of these groups intensively in 2000. Over the following 10 years, we studied six more groups as 126 part of a programme of interdisciplinary research, for a total of 10 groups, which provided the data for 127 our analyses (e.g.  (Table S1; further details about our demographic 135 records are available upon request). Given that the data has been pooled across several different 136 studies, there is some discontinuity, with certain groups being studied for longer and/or more 137 frequently than others (mean ± SD = 45.1 ± 29.7 monthly visits per group; Table S1). The study groups 138 inhabited eight different forest fragments, which varied in size, shape and connectivity (Fig. 1).

139
During each visit, we identified group members on the basis of characteristic patterns on the fur 153 strongly associated with one of the group females, was observed in a group, and that had a younger 154 estimated age than the time that had passed since we last visited the group.

155
To calculate the mean annual birth rate for each group, we determined the number of births that 156 had taken place per year for the mean number adult females in the group. This allowed us to control for 157 the effect of the number of females on birth rate. We defined the inter-birth interval (IBI) as the time 158 that occurred between births for any given female. 166 When an individual emigrated from the group it was born in, we defined this as `natal 167 emigration´. When an individual emigrated from a group that it had previously immigrated into, we 168 defined this as `secondary emigration´.
170 Immigration 171 We assumed a new individual had immigrated into a group when, on first sighting, its estimated age 172 was greater than the time passed since our last visit to the group (e.g., a new individual with an 173 estimated age of 12 months was observed for the first time in a group, but the group was last visited 2 174 months ago).

176 Death
177 We assumed an individual had died when at least one of the following criteria was met: 1) we found 178 the body; 2) the individual went missing while still dependent on its mother's milk and its mother 179 remained in the group; or 3) the individual went missing fully weaned, but was showing serious signs 180 of injury or disease the last time it was observed.

181
182 Disappeared 183 For some individuals it was not possible to determine with any confidence whether they had emigrated 184 or died. Therefore, we recorded these individuals as disappeared.

186 Statistical analyses
187 For the calculation of the seasonality of demographic events, IBI and birth rates, we considered only 188 those events that were registered during periods in which the study groups were observed continuously 189 and that could be assigned to a date with a maximum error of one month (see Table S1). In order to 190 control for the effect that our slightly unbalanced sampling effort could have on the seasonality data, 222 Most of the study groups showed little change in the total number of individuals and in the number of 223 adult individuals from the start to the end of the ten-year study period. However, two groups showed a 224 substantial increase in number (Table 1). Migration was the principal cause of change in group size and 225 composition, followed by births, then deaths.

227 Births
228 We registered a total of 75 births and at least two births were observed in all 10 of our groups (Table   229 1). Of these, we were able to determine the date of birth to within one month on 49 occasions.

230
The mean birth rate per group was 0.40 ± 0.33 births per female per year (N = 39 births; Table   231 2). There were groups with no births in some years, while other groups had a birth rate as high as 1 in 232 some years (indicating that all females of reproductive age gave birth in that year). We found no 233 significant differences in mean birth rate among groups (Kruskal-Wallis Test H = 5.74, p = 0.76).

234
The mean IBI was 21.61 ± 13.27 months ( PrePrints 239 Although we observed births throughout the whole year, births were clearly seasonal. Seventy 240 four per cent of births occurred between October and March (Fig. 3a), with a main peak in November 241 and a second peak in February. The bimodal r statistic was highly significant (unimodal r = 0.20, p = 242 0.14; bimodal r = 0.43, p < 0.001), suggesting a bimodal distribution and a strong effect of seasonality 243 on birth. As the gestation time of howler monkeys is 6 months, these data indicate that conceptions 244 leading to births peaked in May, after the period of energetic stress. In fact, the number of conceptions 245 leading to births was significantly lower during the period of energetic stress than in the rest of the year 246 (G = 9.9, p < 0.001).

248 Emigration
249 We recorded emigrations in all but one of our study groups, with a total of 62 individuals emigrating 250 from groups (Table 1). Thirty-four of these were adults (13 adult males and 21 adult females), 7 were 251 sub-adults (2 males, 2 females, and 3 of unknown sex), 13 were juveniles and 8 were infants.

252
We recorded 24 natal emigrations (52.8% of total number of emigrations of known origin). One 253 by an adult male, 6 by adult females, 3 by subadults, 11 by juveniles and 7 by infants. Of these, 4 left 254 the group soon after the birth of a sibling and 8 left the group soon after one or more individuals had 255 immigrated into their group.

256
We recorded 22 secondary emigrations (47.8% of total number of emigrations of known 257 origin). Nineteen of these were adults (11 males and 8 females), 1 was a male sub-adult, 1 was a 258 juvenile and 1 was an infant that transferred to the group together with her mother, and then left with 259 her after one month of permanence in the group. The mean time that the individuals spent in a group 260 prior to secondary transfer was 18.4 ± 21.1 months (range = 1 -90 months). On 16 occasions, we were not able to determine whether the emigrating individuals were born 262 in the group they emigrated from or whether they had previously immigrated into the group.
263 Accordingly these emigrations were of unknown origin and were not classified as natal or secondary.

264
Emigrations occurred throughout the year, but there were clear differences in emigration 265 patterns among the age-sex classes (Fig. 3b). Male emigration peaked in August (33.1% of cases) and 276 We recorded immigrations in the all forest fragments that we studied and in all but one of our study 277 groups (this group was only followed for one year). In total we recorded 57 individuals immigrating 278 into new groups (Table 1); 46 were adults (22 males and 24 females), 6 were sub-adults (3 males and 3 279 females), 3 were juveniles and 2 were infants. Of these, we were able to determine the date of 280 immigration to within one month in 41 cases (Table S1).

281
Immigration occurred throughout the year, but there were clear differences in immigration 282 patterns among the age-sex classes (Fig. 3c). 294 We registered a total of 18 deaths, and at least one death was registered in eight of the 11 groups (Table   295 1). Thirteen of these individuals were infants that were not weaned when they disappeared, of which 296 eight went missing before four months of age, three between four and eight months, and two at 10 297 months of age. Of these infants, we observed one death directly, which happened when the infant was 298 one month old and another howler monkey seemingly killed its mother (see below) and we assumed 299 another infant to have died shortly after its mother had died and it was observed falling in a tree. We We registered deaths in most months of the year, but there was a clear peak between November 309 and March when 75.3% of deaths occurred (Fig. 3d). There were significantly more deaths during the 310 period of energetic stress than in the rest of the year (G = 9.8, p < 0.001). However, the r statistic was 311 not significant (unimodal r = 0.08, p = 0.89; bimodal r = 0.25, p = 0.30).

312
313 Disappeared 314 We were unable to interpret the history of 27 individuals from the data, which we recorded as 315 disappeared (Table 2). . This suggests that the majority of conceptions that lead to births occur between April and 325 June (Fig. 3a), coinciding with the annual peak in fruit availability and increase in ambient temperature 326 (Figs. 2a & 2b). Accordingly our data suggests that the higher energetic stress between November and 327 March may be inhibiting the reproduction of females and that the improved conditions from April to 328 June results in an increase in fertility. Other studies have also reported that the time of conception is 329 associated with the availability of food and temperature in howler monkeys (Kowalewski & Zunino, 330 2004). This supports the idea that howler monkeys are income breeders (rather than capital breeders)