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Effects of Age on Mantled Howler Monkey (Alouatta Palliata) Behaviour

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08/02/20 Biology Reference this

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The effects of age on Mantled Howler monkey (Alouatta palliata)behaviour, Santa Rosa National Park, Costa Rica

1.0  Abstract

 

Alouatta palliata have a wide variety of behaviours, they spend the majority of their time resting followed by locomotion, feeding and social interaction. Their behaviour however can vary due to differences in the biotic environment such as different age classes. The aim of this investigation was therefore to investigate the effects of age on A. palliata behaviour. The study was conducted on seven individuals, two juveniles and five adults, during 4 days (2nd and 4th-5th of September) within Santa Rosa National Park, Costa Rica. The individuals behavioral patterns where recorded using 5-minute interval scan sampling, with the behaviours divided into six main categories: resting, locomotion, feeding, maintenance, social interaction and vocalisation. There was significant differences (all p<0.05) observed due to age in four categories: resting via sitting, locomotion, maintenance and vocalisation. Resting showed a decrease with age, with juveniles shown to spend more time in other behavioural categories, such as locomotion. This may be due to the requirements of exploration for mental development in juveniles. No other Behavioral category showed any differences between ages.

 

2.0  Introduction

Most previous studies on neotropical primates have looked at the genus Alouatta (Pavelka and Knopff, 2004) with the mantled howler monkey (Alouatta palliata) being studied in great detail (e.g. Glander 1980; Balcells and Baró 2009). The behavioural traits and lifestyles of this species is therefore well documented.  Alouatta palliata originates from Central and South America commonly occupying the dry and rainforests of Costa Rica. they form large family groups of around 10-20 individuals, forming a highly structured social hierarchy (Glander 1992). They are known to be folivorous with a diet mainly consisting of green leaves and fruit. This is demonstrated by Milton, Van Soest and Robertson, (1980), demonstrating that A. palliata spend a large proportion of their time foraging which is representative of their generally inactive lifestyle (Pavelka, and Knopff,  2004). Consequently A. palliata have also been shown to spend the majority of their daily activity resting (up to 90% of daily activity) (Estrada et al, 1999). Aside from this, Estrada, (1984) have shown that  A. palliata mainly spend the remainder of their time in locomotion or social interaction.

All species within the family primates show species-specific differences in behaviour that are influenced by abiotic or biotic conditions (Katz and Harris-Warrick, 1999: Agostini, Holzmann and Di Bitetti, 2010). Abiotic factors including seasonality (Pozo-Montuy and Serio-Silva, 2006), habitat fragmentation (Arroyo-Rodríguez and Dias, 2010) and human disturbances (Aguilar-Melo et al, 2013) have all been shown to affect Alouatta behaviour. These conditions are long lasting affecting the whole population causing changes over a large time period. Biotic behavioural influences are therefore more likely to cause changes in individuals’ behaviour within a group. For example, anatomical body size differences (Cant 1992), physiological age constraints and social status (Jones, 1983), are all leading causes of intraspecific behavioural differences within A. palliata populations.

Age can be a limitation to both body size and mentality within individuals, with many studies showing overall differences in behaviour between juvenile and adult populations (Bicca-Marques, and Calegaro-Marques 1994).  As explained by Bicca-Marques and Calegaro-Marques, (1994) juveniles express different behaviours due to the requirements of growth and mental development to successfully mature into adulthood. This can therefore cause an increase in diet specialization and feeding bouts to provide enough nutrition for growth and development (Bicca-Marques, & Calegaro-Marques, 1994). Whereas adult populations have also been shown to express different behaviours which may be due to the cost of lactation and maternal care in females and protecting territory in adult males (Harrison, 1983). A key component in the differences in behaviour between the classes has been shown to be due to social interactive behaviours (Prates and Bicca-Marques 2008). The main interactions within the adult population is due to reproductive behaviour, whereas in infants and juveniles the major interactions have been found to be the mother-child social relationships, playing and forming bonds with members of the family group (Altmann 1959;Prates and Bicca-Marques, 2008). Juveniles interact more with members of the family group to develop social and motor skills which also helps aid in mental development (Clarke, Glander and Zucker, 1998).

Size limitations, which directly correlates with age, is also a major factor that contributes to the behavioural traits of the age classes and this has been demonstrated in a lot of previous literature (Robinson and Redford, 1986;Prates and Bicca-Marques 2008). The main trend, due to body size and age differences,  is shown to be an increase in resting and decrease in locomotion with increases in age. Body size effects the use of resting positions with the use of sitting increasing with body size and thus age. As shown by Bicca-Marques and Calegaro-Marques (1998),  Alouatta use postural positions as a way of thermal regulation, with an increase in lying providing greater surface area too cool the body temperature and sitting when needing to conserve heat. This may therefore affect  postural difference between ages with juveniles having a smaller body size thus needing to conserve heat more.

Locomotive behaviour has also been shown to be affected by age with an increase in locomotion in smaller and younger individuals (Prates and Bicca-Marques 2008). As explained by Bicca-Marques and Calegaro-Marques, (1995) the smaller size in juveniles allows them to move further than adults due to them not being limited by small spaces or weak branches. Juveniles also have a more inquisitive nature increasing locomotion due to exploration (Baldwin and Baldwin 1978). This aids their mental development, allowing them to become accustomed to their environment and building up the skills needed for adult life. In turn this has been shown to increase locomotion in younger individuals (Prates and Bicca-Marques 2008). 

The aim of this study was therefore to determine if there was an effect of age on the behaviour of A. palliata in Santa Rosa National Park, Costa Rica.

3.0 Methods

3.1 Study site

Data was collected on a family group of A. palliata for three days (2nd and 4th-5th of September) between the hours of 5:30 to 17:15 (11:45hrs). The study was undertaken during the wet season with temperatures being on average 28°C, within Santa Rosa National Park, Costa Rica. The national park spans over more than 49,000 Ha (Campos and Fedigan, 2009), with the group studied having a home range around the administrative area within the national park (lat:10.836219, long:85.618315) (refer to figure 1). This area was part of the dry tropical forest with a range of native dry deciduous and semi-evergreen vegetation, including Spondias mombin and Enterolobium cyclocarpum where the group was commonly found, providing rest sites and food sources.

 

Figure 1. Map of Santa Rosa National Park showing the administrative area where the groups home range was (in red) (Source: Pinterest – Santa Rosa National Park hiking and history in Guanacaste (2018))

 

3.2 Study Species

After a preliminary study was undertaken, it was determined that the group consisted of 2 males, 3 females, a female juvenile and an infant. These age classes were classified using the studies by Glander (1980) and Balcalls and Baro (2009). The infant observed in this study has been classified as a juvenile due to the infant seeming on the verge of becoming what is classified as a juvenile in these studies, with less maternal reliance and independent locomotion and feeding observed.  There were therefore 2 juveniles and 5 adults used within this study.

3.3 pilot study

During the eight-hour pilot study the group composition, scan duration and behavioural categories were determined. The behaviour of the group was observed with each specific behaviour being grouped into 10 main behavioural categories (Refer to table 1)

3.2 Behavioural data collection.

The group was followed on their daily route from the sleeping tree in the morning (5:30am) to their rest site in the evening (5:15pm), recoding their behaviours throughout the day. The behaviours (table 1) of each individual within the group were recorded using scan sampling which was undertaken every 5 minutes. A search time of 2 minutes was also used to allow time to locate hidden individuals and record their behaviour. Where the type of behaviour was uncertain, for example moving between resting positions (sitting up etc.), the animal was allocated time within the two-minute search time to make certain the correct behaviour was recorded. Only individuals that were present within the two minutes of the scan time were recorded and any individuals that were out of sight were excluded from the scan sample.

Table 1. Ethogram of the behaviours of A. palliata recorded in this study.

Behaviour

code

Subgroup

Subgroup code

Description

Feeding

F

Feeding on leaves

FL

Feeding/chewing on leafy green foliage including sticks and bark from trees.

Feeding on fruit

FF

Feeding/chewing on fruit from trees and bushes.

Foraging

FOR

Picking at or searching through patches of fruit/leaves but not yet eating them/having put them in their mouth, and clearly walking towards a food source for example moving from one food source to another.

Locomotion

L

All locomotion

L

Where the whole body is in motion, moving throughout the trees using fore/hindlimbs and/or tail via walking running, swinging, jumping, climbing and descending. Excludes foraging behaviour.

Resting

R

Sitting

SIT

Resting in an upright position with only the fore/hindlimbs touching the tree/branch and without the stomach touching the branch.

Lying

LIE

Lying with the majority of the body including the stomach/back touching the branch. 

Vocalisation

V

All vocalisation

H

Loud deep pitched howls, likely in an antagonistic or territorial display or Small quick grunts/high-pitched squeaks that may be used in the build up to howling or during social interaction. If vocalisation is used during social interaction it will still be counted as vocalisation.

Maintenance

M

All maintenance behaviour

M

Self-maintenance behaviour including defecating, urinating, scratching and self-grooming.

Social interaction

SI

Social interactions

INTRA

Social Interactions with members of  both the same species within the family group and different species, including touching, hugging, handholding, allogrooming, sexual and maternal behaviour. This also includes aggressive behaviour  with interactions such as fighting behaviour, teeth-showing and intimidation clearly in an aggressive manner.

Excluding vocalisation and play behaviour.

Play behaviour

PLAY

All boisterous and highly locomotive interactions between individuals of the same family group that are conducted in a playful and fun manner.

                                                                                                                                                 3.3. Analysis

The sum of each the 5-minute behavioural scan samples was taken, and all the intervals taken within the hourly intervals were combined (beginning at 5:30 to 6:25 and continuing at 30 minutes past each hour), finding the totals for each behavioural category. The percentage of each behavioural category observed per hour was then also calculated and recorded to provide replicates for data analysis.

The data was analysed using IBM SPSS statistics 24, with all the data for the behavioural categories needing to be arcsine transformed to make them suitable for analysis. The rest-lie behavioural category was analysed using an independent T-test (Field, 2013) which did not need transformation due to the assumptions being met (normality and equal variance). All other behavioural categories were analysed with Mann-Whitney (Field, 2013) due to the data appearing non-normal even after transformation. All tests had a significance level of 0.05.

4.0 Results

Overall, thirty-seven data replicates were collected for each category, Juvenile and adult. The behavioural category with the most data counts was rest-lie for both age classes which showed no significant difference between adults or juveniles  (t72=0.723, p=0.472) (figure 2). The rest-sit category however did show a significant difference (z=-4.172, n=74, p<0.001) with the adult population (Median±IQR=19.57±14.31) shown to sit significantly more than juveniles (7.14±16.03) (figure 3).In contrast to this, for the locomotion category the juveniles (Median±IQR=33.33±34.93) were shown to be significantly more active than the adult population (Median±IQR=16.67±20.28) (z=3.409, n=74, p=0.001)(figure 4).

Both age classes showed no difference in the amount of duration spent feeding or foraging with no significant differences observed for feeding on leaves between adults (Median±IQR=0±2.26) and juveniles  (0±0)(z=-0.871, n=74, p=0.384), fruit between adults (Median±IQR=0±0) and juveniles (0±0) (z=0.360, n=74, p=0.719) or general foraging between adults (Median±IQR=1.79±10.17) and juveniles (0±8.71) (z=-1.296, n=74, p=0.195)(See figure 4).

Social behaviour was observed in both age classes with play behaviour primarily recorded between the juvenile and an adult. There was shown to be no significant differences in either social interaction (z=-0.883, n=74, p=0.377)  between adults (Median±IQR=0±2.09) and juveniles (0±0) or play behaviour (z=0.402, n=74, p=0.688) between adults (Median±IQR=0±1.17) and juveniles (0±3.13)(Figure 4). Vocalisation however, showed a significant difference (z=-3.366, n=74, p=0.001) being shown exclusively within the adult population (Median±IQR=0±1.98) with no juvenile individuals shown to vocalise (0±0) (figure 4).

Similar to this, the adult population (Median±IQR=2.13±3.57) were shown to spend a significantly greater percentage of time spent on maintenance compared to the juvenile population (0±0) (z=-3.616, n=74, p<0.001) (figure 4)

 

Figure 2. Mean±SE time spent in the lying down resting position (%) compared between adults (n=37) and juveniles (n=37)

Figure 3. Median±IQR time spent sitting (%) compared between juveniles (n=37) and adults (n=37)

E

A

F

B

 

G

C

 

 

 

 

H

D

 

 

 

 

Figure 4. Median±IQR of time (%) spent A:locomoting, B:feeding on Leaves, C:Feeding on fruit, D:foraging, E:Vocalisation  F:maintenance G:Social interaction and H:playing, compared between Adults (n=37) and Juveniles (n=37)

5.0 Discussion

The aim of this study was to determine the effect of age on behaviour in A. palliata. There was found to be an effect of age on resting via sitting, locomotion, vocalisation and maintenance. Adults showed a greater percentage of daily activity spent on sitting, vocalising and maintenance. Whereas for locomotion the opposite was true with juveniles shown to spend a greater proportion of time locomoting compared to adults. No other category showed a significant affect of age of the prospective behaviours.

Similar findings to what have been shown in this study, have also been demonstrated in previous studies by Prates, and Bicca-Marques (2008) who also demonstrated significant differences in sitting and locomotion.                                     Resting is one of the most important categories in regard to A. palliata behaviour due to their inactive lifestyle and this was the category with the greatest amount of time dedicated to. As shown by Korstjens, Lehmann and Dunbar, (2010) resting behaviour is essential in A. palliata due to the digestive difficulties of a folivorous diet. They therefore commit more time to resting to save energy for digestion (Pavelka and Knopff, 2004;Korstjens, Lehmann and Dunbar, 2010). As shown by Bicca-Marques and Calegaro-Marques, (1998) resting is also a key component of thermoregulation which can help in energy conservation for digestion and other activities. Resting has also been shown to differ between the ages as although there was no difference observed in lying down, there was shown to be differences in sitting and in both of these categories’ adults spent the greatest amount of time resting. Similarly, Prates, and Bicca-Marques (2008) and Bicca-Marques and Calegaro-Marques, (1994) also showed this with an increase in resting behaviour in adult individuals. This behaviour follows the trend shown in our results with juveniles shown to spend a greater proportion of time spent in other activities. This is shown for example in locomotion with juvenile individuals shown to spend a greater proportion of their time moving. This observation is supported by Bezanson (2006) and Prates, and Bicca-Marques (2008) who showed similar results. As described by Dunbar and Badam, (1998) juveniles are well suited to a highly locomotive lifestyle due to their small body size, energy and strength. It is probably likely that this increase in behaviour is due to the developmental needs in juvenile individuals with exploration behaviour being key to growth and development (Baldwin and Baldwin, 1978). Therefore, allowing juveniles to develop the motor skills needed for the requirements of foraging in adult life.  Adults on the other hand have highly developed motor skills so can therefore dedicate more time to resting to help conserve energy and dedicate time to digestion and thermoregulation.

Similarly, social interaction has previously been shown to contribute to a greater proportion of juvenile’s daily activity, compared to an adults (Bicca-Marques and  Calegaro-Marques, 1994; Prates, and Bicca-Marques 2008). It is therefore unexpected that our results show no differences between age classes in both social interaction and playing. Although not shown to be significantly different, there was shown to be a greater range in percentage time spent in social interactions in the juvenile class and the only recorded incidents of social interaction always involved the juvenile. In this instance it may be the case that the unequal sample sizes may have affected the results for social interaction.

It was also shown within the social interaction category that adults were the only class shown to be aggressive. This is demonstrated in the lack of vocalisation shown in juveniles with only adults shown to vocalise. Vocalisation is key to aggressive disputes which is shown particularly in males who use howling as a way of territorial protection (Altmann, 1959; Wang and Milton, 2003). Aggressive howling has also, only been observed in adult populations in previous studies (Altmann 1959; Sekulic,1982). Juveniles have previously been shown to be able to use vocalisation, with what has been described as “small squeak” vocalisation observed (Holzmann, Agostini and Di Bitetti, 2017). However, as Altmann, (1959) describes this is only used in play behaviour between juveniles, in which this was not observed in large frequencies in our study, or when a juvenile was lost from its mother which was also not observed. The use of vocal howling was therefore restricted to adults, used as a deterrent and in territorial displays.

The differences observed in maintenance behaviour has similarly been shown by Bezanson, (2006) who showed an increase in grooming behaviour within the adult population. Although grooming is rare in A. palliata it has been observed between infants and adults(Neville, 1972). Therefore, reducing the self-maintenance behaviour required by juveniles. It is not expected that excretion behaviour would affect either group.

It was expected that feeding levels would vary between age groups, due to the higher requirements of feeding for growth and development in juvenile individuals (Bicca-Marques, and Calegaro-Marques 1994). This has been supported by a previous study showing differences between the age classes (Prates and Bicca-Marques 2008). However, this was not shown in our results with no differences between age classes observed when feeding on fruit, leaves or general foraging. Other studies have also shown this, with no difference observed either (Bicca-Marques, and Calegaro-Marques 1994: Pavelka and Knopff, 2004). The differences between the results in previous studies may be due to the inclusion of infants, with the major differences observed  being due to infant and adult feeding (Bicca-Marques, and Calegaro-Marques 1994). All of these studies however, showed no differences in the diet preferences between age classes, which was also showed in our results. As explained by Prates and Bicca-Marques (2008) the similarity in food preference is probably due to the fact that A. palliata fed as a group, predominantly on the same tree when feeding bouts occurred. As there was little diversity in the type of food sources the group ate, then it isn’t surprising that there were no specific differences in the food consumed. As the group moved and stopped at the feeding spots together it is also not surprising that there were no differences observed in the time spent feeding between age classes.

The results from this study therefore support what has been shown in previous studies with the most time overall dedicated to resting and major differences observed between the age classes, particularly in resting and locomotion with no differences in feeding (Bicca-Marques, and Calegaro-Marques 1994; Pavelka and Knopff, 2004; Prates, and Bicca-Marques 2008). Vocalisation was not recorded in these studies, yet it has also been shown to differ between ages, supporting our findings (Altmann 1959). These results therefore back the notion that A. palliata, particularly adults, exhibit a minimal energy-expenditure lifestyle consuming similar foods and spending a large proportion of time resting (Strier, 1992; Prates, and Bicca-Marques 2008). The differences observed between the ages helps support the idea that juveniles exhibit different traits due to the requirements of growth and development in younger individuals (Prates, and Bicca-Marques 2008; Balcells and Baró 2009). Expressing a greater requirement for locomotion via exploration (Baldwin and Baldwin, 1978) and not yet developing the need for vocalisation that is required by adults (Altmann 1959). To further the understanding of how age affects Alouatta behaviour it would be interesting in future studies to include infants and subadults and compare between multiple groups.

Overall our results and that from previous literature indicate an effect of age on        A. paliatta behaviour. Implying that in future studies age classes should be viewed separately as age has been shown to affect Behavioral results.

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