Introduction of gum Arabic and guar to the diet of captive black-tufted ear marmosets

Applied Animal Behaviour Science 133 (2011) 246–253

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Introduction of gum Arabic and guar to the diet of captive black-tufted ear marmosets Rafael Pupe a , Maria Clotilde Henriques Tavares a , Marilia Barros b,∗ a b

Primate Center & Department of Physiological Sciences, Institute of Biology, University of Brasilia, CEP 70910-900 Brasilia, DF, Brazil Department of Pharmaceutical Sciences, School of Health Sciences, University of Brasilia, 70910-900 Brasilia, DF, Brazil

a r t i c l e

i n f o

Article history: Accepted 23 May 2011 Available online 17 June 2011 Keywords: Marmoset Gum Arabic Gum guar Intake Foraging

a b s t r a c t Gum plays a significant role in the feeding ecology of wild callitrichids and thus is also supplemented to several primate species in captivity. However, little is known about the feeding habits of black tufted-ear marmosets (including gummivory), in both wild and captive populations. Therefore, the present study introduced gum to the diet of adult captive black tufted-ear marmosets (Callithrix penicillata), analyzing the influence of gum type (Arabic vs. guar), solution level (50, 25 or 15% m/m gum:water) and time of provision (morning vs. afternoon). Gum intake, latency to first consumption, foraging time/frequency and inter-foraging interval were assessed, as well as changes in body weight. Marmosets were pair-tested in their home-cages and randomly divided into three groups (n = 6): control (water), gum Arabic or gum guar. Water/gum solution was given twice a day (07:30 to 08:30 and 15:00 to 16:00 h), three times a week, during 3 weeks. Each pair was thus submitted to eighteen 30-min trials, with each gum solution being evaluated on three separate occasions during the morning and afternoon periods. Latency to first consumption and foraging were observed only during the first 5-min of each trial. Although water-solubilized gum was promptly consumed, marmosets preferred the Arabic version, with a significantly higher (P < 0.01) and more efficient intake (i.e., greater foraging time/frequency and shorter interforaging intervals). Preference was most pronounced for solutions with greater gum content (i.e., 50%). Latency to first consumption (mean ± SEM range: 39 ± 21 to 94 ± 19 s) and body weight (mean ± SEM range: 318 ± 27 to 385 ± 11 g) did not differ within or between groups, and time of provision (morning vs. afternoon) did not influence the results. Intake and foraging were not recorded for the water-treated marmosets. Thus, gum is a viable dietary supplement for captive black tufted-ear marmosets, with attention needed on the type of gum provided, as well as its preparation (solubilization). © 2011 Elsevier B.V. All rights reserved.

1. Introduction Black tufted-ear marmosets (Callithrix penicillata) are arboreal, cryptic and diurnal neotropical primates occurring in central Brazil. These small-bodied animals are highly dependent on plant exudate as a food source – particularly gum (Fonseca and Lacher, 1984; Miranda and Faria, 2001; Rizzini and Coimbra-Filho, 1981; Rylands

∗ Corresponding author. Tel.: +55 61 3307 2098; fax: +55 61 3307 2098. E-mail address: [email protected] (M. Barros). 0168-1591/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2011.05.015

and Faria, 1993; Santee and Faria, 1985). In fact, gum feeding comprises approximately 50% of their daily activity (Fonseca and Lacher, 1984) and up to 70% of their diet (Rylands and Faria, 1993). C. penicillata are thus classified – along with other callitrichids – as obligate exudate feeders, having incisiform canines for tree-gouging and clawed fingers to cling vertically to substrates (Rylands and Faria, 1993). Marmosets also have important adaptations in their jaw muscles (e.g., Taylor et al., 2009) and digestive tract (Caton et al., 1996; Ferrari and Martins, 1992; Ferrari et al., 1993). The latter allows for longer gut retention and as such favors microbial fermentation of the gum consumed

R. Pupe et al. / Applied Animal Behaviour Science 133 (2011) 246–253

(Caton et al., 1996; Power and Oftedal, 1996). Fermented gum yields what would otherwise be unavailable energy from ␤-linked complex carbohydrates, aside from water and minerals (Garber, 1984; Nash, 1986; Power, 1996; Smith, 2000). In view of its importance to wild callitrichid populations, several species kept in captivity are also supplemented with gum (Caton et al., 1996; Herron et al., 2001; Huber and Lewis, 2011; McGrew et al., 1986; Power and Oftedal, 1996). This procedure is essentially viewed as a simple, fast and low-cost strategy to increase nutrient intake (Herron et al., 2001). Marmosets may have naturally high calcium requirements (King, 1978; Power et al., 1999), due to twin births and large litter weight (Leutenegger, 1973; although see Smith, 2000), as well as suffer calcium–phosphorus imbalances as a result of the insect/fruit component of their diet (Garber, 1984; Smith, 2000). In this sense, the high calcium content found in gums may have a significant benefic impact on the daily nutritional requirements of captive marmosets. Also, gum supplementation provides individuals with the opportunity to perform important species-typical repertoires, such as those related to gummivory, reducing stereotypical behaviors and increasing animal welfare. Thus, health, behavioral and breeding problems – frequently associated with captivity and/or nutrient deficiencies – decreased after the incorporation of gum to the diet of captive individuals (Herron et al., 2001). On the other hand, gum intake differs considerably within the Calltrichidae family, seen in both feral (e.g., Stevenson and Rylands, 1988) and captive animals (e.g., Power and Oftedal, 1996). In black tufted-ear marmosets, specifically, several aspects of their feeding habits still remain unknown (including gummivory), even with the recent increase in captive colonies. The present study thus focused on assessing the viability of introducing gum to the routine diet of adult captive black tufted-ear marmosets (C. penicillata). As gum composition – and possibly its palatability (Herron et al., 2001) – varies depending on the plant species/age, climate and soil conditions (Verbeken et al., 2003), different types of gum and solution levels were tested. In addition, the influence of the time of provision was also determined, as the temporal pattern of gum-feeding differs considerably among species. For marmosets, peak consumption of gum occurs early in the morning and late afternoon, while only in the afternoons for tamarins (Heymann and Smith, 1999). Therefore, the influence of gum type (Arabic vs. guar), solution level (50, 25 or 15% m/m gum:water) and time of provision (morning vs. afternoon) on gum intake, latency to first consumption, foraging time/frequency and inter-foraging interval were assessed in black tufted-ear marmosets. Body weight, before and after the study, was also determined. 2. Methods 2.1. Subjects and housing conditions Eighteen adult black tufted-ear marmosets (C. penicillata; nine males and nine females) were used, aged 18–49

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months and weighing 280–400 g at the beginning of the study. Marmosets were pair-housed at the Primate Center of the University of Brasilia in nine separate cages (2 m × 1.3 m × 2 m each) of a same colony room. Same-sex and heterogeneous pairs were tested. Subjects were either captive-born at our colony or transferred as adults from illegal trade apprehension made by the Brazilian government. Some captive-born marmosets were related, even though this aspect was not determined in the feral animals. Not all members of the housing colony were used in the experiment. The colony room – which consisted of two parallel rows of 12 cages separated by a common wire-mesh enclosed central corridor – formed an outdoor/semi-indoor housing system. Accordingly, marmosets were exposed to natural light, temperature and humidity conditions. Each homecage consisted of two parallel concrete walls (separating adjacent cages), a wire-mesh front, back and ceiling, a suspended wooden nest-box, several wooden perches at different heights, a food tray (where food bowl was placed), a PVC feeding tube hung from the wire mesh ceiling for dry food pellets, and a layer of wood-shaving on the floor. Additionally, a solid roof 50–150 cm above the wire-mesh top covered two thirds of all cages and the central corridor. Food was provided twice a day, at 07:30 and 14:00 h, consisting of a mixture of fresh pieces of fruits and vegetables, with meal-worms, crickets, boiled eggs, various nuts and/or cooked chicken breast given on alternate days. Water and dry food pellets were available ad libitum. During the experimental procedure described below, morning provisions were delayed for 1-h on the specific test days and only for the pairs being tested in the present study. Housing and maintenance conditions complied with the regulations of the Brazilian Institute of Environment and Renewable Natural Resources (IBAMA).

2.2. Gum solutions Two types of gum were tested: gum Arabic and guar (Doce Aroma; São Paulo/Brazil). As these were obtained as small pieces of crystal of different sizes, both gum types were first ground into a fine powder to facilitate subsequent weighing and solubilization procedures. Each type of gum powder was then dissolved in tridistilled water (Quartex® ) to provide three possible solution levels (50, 25 and 15% m/m gum:water). For this, pre-determined amounts of gum powder were weighed (digital scale: Myra plus© , Soehnle, USA) and placed in stainless-steel bowls (9 cm diameter × 5 cm high), to which the required amount of water was then added to yield the desired solution level. The resulting solution was manually homogenized, weighed and made available to the marmosets in the same stainless-steel bowls. These were placed inside the subject’s home-cage wire-mesh front/door, 1-m from floor level, using a specifically designed metal frame support. All gum solutions were provided in a volume greater than that expected to be consumed by the marmosets (120 mL), as determined by a pilot study. All gum solutions were freshly prepared on each test day.

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2.3. Experimental procedure

2.4. Specific behaviors scored

Marmosets were kept in their own home-cages and social environment throughout the study. Subjects were randomly assigned to one of three treatment groups: control (n = 6), gum Arabic (n = 6) or gum guar (n = 6). Controls were given the same tridistilled water used to solubilize the gum powders. Both members of a home-cage were necessarily assigned to the same treatment group and submitted simultaneously to the same procedure described below. Regardless of its group, all marmosets still received their routine daily diet. For each pair tested, gum or water was given twice a day (07:30 to 08:30 and 15:00 to 16:00 h), three times a week, during 3 weeks. Water/gum was thus provided during eighteen 30-min trials for each pair: nine were held during the morning interval and nine in the afternoon. For either the morning or afternoon trials of the gum-treated marmosets, three sessions were held using the 50% solution, three with the 25% solution and three with the 15% solution. Therefore, each gum solution level was evaluated on three separate occasions, with the order varying randomly on each test day and for each pair tested. Control subjects received only water during all eighteen 30-min trials. Regardless of the group, the order in which the marmoset pairs were evaluated was also randomly assigned on each test day. On all (nine) morning trials, water or the pre-established gum solutions (50, 25 or 15%) were prepared in the stainless-steel bowls as described above. Each bowl was then weighed to determine the initial amount of water/gum being provided to each pair. At 07:30 h, only the first of the nine pairs being tested received its predetermined bowl containing water or gum, according to the pre-established order. Immediately after the bowl was placed in this home-cage, specific behaviors (detailed below) were observed only during the first 5-min of the 30-min trial. At 07:35 h, the same procedure was repeated for the second pair to be tested. This protocol was subsequently repeated at 5-min intervals for the ensuing home-cages, until all nine pairs had received their water/gum provision and were observed. Bowls were removed 30-min after being placed in each home-cage and once again weighed to determine the amount of water/gum remaining. At 08:30 h, when the last water/gum bowl was removed, the routine daily morning provision was placed in the home-cages of the nine marmoset pairs being tested. For the (nine) afternoon trials, the same procedure as that held during the morning period was also used. The only difference was that the normal daily provisions given routinely at 14:00 h were removed at the beginning of the session and replaced in the home-cages at the end of the 30-min interval. Also, the specific solution level given in the morning for each pair and on each test day, did not necessarily correspond to that used in the afternoon. The procedure described above was approved by the Animal Ethics Committee of the University of Brasilia, complied with the ‘Brazilian Principles of Laboratory Animal Use’ (COBEA) and followed the NIH guidelines for care and use of laboratory animals.

An experienced observer (95% intra-rater reliability) recorded the following parameters during the first 5-min of each trial, using focal all-occurrences samplings: (1) latency to initiate consumption, time elapsed between the start of the 5-min session and the first ingestion of water/gum solution; (2) foraging, time and frequency spent handling and/or ingesting the water/gum solution; and (3) inter-foraging interval, average time elapsed between consecutive foraging bouts during the 5-min session. Marmosets from a same home-cage were observed simultaneously, yet scored individually. The Etholog program (version 2.2; USP, Brazil) was used to score these behaviors. 2.5. Data analyses 2.5.1. Water/gum intake For each trial, the initial amount (in g) of water/gum solution provided and that which still remained in the bowl after the 30-min trial were determined to calculate each pair’s intake. The marmoset pair consumed water/gum when differences between the initial and remaining amounts were established, since water/gum was not observed around the bowls or on the floor of the home-cages after the 30-min trials. As the solutions levels (50, 25 and 15%) for each gum type were provided to the marmosets on three separate occasions, the pair’s intake per solution tested was considered to be the total amount consumed either during the three morning or the three afternoon trials. For the control group, who received only water during the nine morning and nine afternoon trials, each pair’s intake was considered to be the total amount ingested during trials 1–3, 4–6 and 7–9 of the morning/afternoon period. Trials 1–3 were considered to be ‘equivalent’ to the three 50% solution sessions, trials 4–6 as the three 25% solution sessions and trials 7–9 as the three 15% solution sessions. 2.5.2. Latency to first consumption Latency to first consumption was scored, for each trial, as defined above. As each solution level (50, 25 and 15%) was given three times to the marmosets, latency per solution for each subject was calculated as the mean average time elapsed during either the three morning or the three afternoon trials. For the water-treated marmosets, the procedure described above for intake was also employed. Averaged values, however, were used instead of summed results. 2.5.3. Foraging time and frequency The time spent foraging during each trial was also scored as described above. Considering once again that each solution level (50, 25 and 15%) was provided to the subjects on three separate occasions, foraging time per solution for each marmoset was determined using the same summed procedure previously described for water/gum intake. In addition, foraging frequency was scored as the total number of bouts per solution for each marmoset that occurred during the three 5-min observation periods for each solution tested. Data for the water-treated marmosets

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were also calculated using the method described above for intake. 2.5.4. Inter-foraging interval A relative mean inter-foraging interval per solution was calculated for each subject. Initially, the individual latencies between consecutive foraging bouts were averaged, including the intervals for all three occasions that each specific solution was offered either during the morning or afternoon. The mean inter-foraging interval per solution of each subject was then divided by the respective total number of bouts observed during the specific time of provision (morning/afternoon). The latter aimed at standardizing the mean inter-foraging interval calculated per solution, considering that a different number of foraging bouts occurred for each solution and time of provision. Data for the water-treated marmosets were also calculated as described above. As these inter-foraging bouts corresponded to the total observation time (i.e., 300-s) and no bouts were observed, the resulting values for the control group always equaled to zero. 2.5.5. Marmoset body weight All subjects were weighed before and immediately after the experimental trials. Absolute values were used to determine the marmosets’ mean initial and final weights. 2.6. Statistical analyses Data on all parameters (i.e., intake, latency to first consumption, foraging, inter-foraging interval and weight) were normally distributed and with equal variance and thus analyzed using parametric statistics on raw nontransformed values. Significance level for all testes was set at P ≤ 0.05. As the three main aspects being tested in the present study were gum type, solution level and time of provision, data on water/gum intake, latency to first consumption, foraging time/frequency and inter-foraging interval were analyzed accordingly. Marmoset body weight was analyzed separately. 2.6.1. Influence of the time of provision As callitrichids differ in terms of the temporal pattern of their feeding behavior, particularly when exploiting exudates (i.e., time of peak consumption; Heymann and Smith, 1999), subjects from the present study were provided with water/gum in the morning (07:30 to 8:30 h) and afternoon (15:00 to 14:00 h). However, as significant differences between these two intervals were not observed (data not shown), results obtained during the morning/afternoon periods were pooled together for the subsequent analyses. Such procedure aimed at increasing the power of the analysis, with more observations made per gum type and solution level tested. 2.6.2. Influence of the gum type and solution level Plant species/age, climate and soil conditions may alter gum composition (Verbeken et al., 2003) and possibly its palatability for marmosets (Herron et al., 2001). Accordingly, two types of gum (Arabic and guar), as well as different solution levels (50, 25 and 15%), were presently

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tested and compared to water-treated animals. In view that marmosets did not consume water on any of the trials held, data observed in this group were excluded from the subsequent statistical analyses. Such procedure allowed for a more straightforward statistical analysis and interpretation of the results. Nonetheless, to facilitate comparisons, data from control subjects were still included in the graphical representation of the results. Thus, pooled data for gum intake, latency to first consumption, foraging time/frequency and inter-foraging interval were initially analyzed using a mixed design analysis of variance (ANOVA), with group (gum Arabic and guar) and solution level (50, 25 and 15%) as the independent and repeated measure factors, respectively. Degrees of freedom were corrected using the Greenhouse-Geisser method, yet only non-corrected values are presented in the results. Whenever significant, subsequent analyses were performed using the t-test (group) or one-way ANOVA for repeated measures (solution level), with the Bonferroni method to correct significance level for multiple pairwise comparisons. To assess for possible correlations between the gum types and the solution levels provided to the marmosets, gum intake, foraging time/frequency and interforaging interval were analyzed using Pearson’s correlation test. 2.6.3. Marmoset body weight Data were also analyzed using a mixed design analysis of variance (ANOVA), with group (gum Arabic, gum guar and water) and ‘before/after’ as the independent and repeated measure variable, respectively. Subsequent tests and adjustments were held as described above for the remaining parameters. 3. Results 3.1. Influence of the time of provision As stated above, the amount of water/gum consumed, latency to first consumption foraging time/frequency and inter-foraging interval observed during the morning interval did not differ significantly from that measured in the afternoon (data not shown). 3.2. Influence of the gum type and solution level 3.2.1. Gum intake Gum Arabic-treated marmosets consumed a significantly greater amount of this dietary component than those who received gum guar [F(1,10) = 22.41, P < 0.01], with no effect seen in terms of the three solution levels tested [F(2,10) = 3.77, P = 0.10; Fig. 1]. The observed differences between the gum Arabic and guar groups were dependent, however, on the specific solution provided to the animals, as a significant group × solution level interaction was observed [F(2,20) = 6.05, P < 0.05]. Accordingly, only when the 50% solution was given did gum Arabic-treated marmosets consume a significantly larger amount of this food item than the group provided with gum guar, as indicated by post hoc analyses [t(1) = 16.50, P < 0.001]. Also, the amount consumed was positively correlated to the per-

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*

30

water

Arabic

Arabic

guar

20

guar

200

Foraging frequency

300

water

*

10

100 0

0

300

1200

200

800

Foraging time (s)

Latency 1st consumption (s)

Amount consumed/pair (g)

400

100

0 25

0

15

Fig. 1. Top: mean (+SEM) amount of water, gum Arabic and gum guar consumed per pair (in g) summed during the nine (three morning + three afternoon) 30-min trials and for each solution tested; bottom: mean (+SEM) latency for marmosets to initiate consumption (in s), averaged over the nine (three morning + three afternoon) sessions and scored during the first 5-min of each trial and solution tested (50, 25 and 15% m/m gum:water). Water-treated marmosets were not included in the statistical analyses (refer to section 2.7.2); n = 6/group; *P < 0.05 vs. guar.

centage of gum in the solution for the Arabic group [r = 0.74, P < 0.05], while no significant effect was seen in the gumguar treated animals [r = −0.42, P = 0.26]. Tridistilled water used to solubilize the gum powder and as a control was not consumed by the marmosets during the entire study (Fig. 1). 3.2.2. Latency to first consumption A similar latency to initiate consumption (Fig. 1) was detected between the two gum-treated groups [F(1,10) = 0.70, P = 0.42] and the three solution levels tested [F(2,10) = 2.38, P = 0.13], with no significant group × solution level interaction [F(2,20) = 1.81, P = 0.20]. As water was not consumed during the study, latency to first consumption in the control group corresponded to the maximum observation period (300-s) of each trial. 3.2.3. Foraging time and frequency Marmosets who were given gum Arabic demonstrated a significantly greater number of foraging bouts than those who received gum guar [F(1,10) = 10.04, P < 0.001], with no effect seen in terms of the three solution levels tested [F(2,10) = 1.78, P = 0.19; Fig. 2]. The difference between these groups was dependent, however, on the specific solution provided to the animals, as a significant group × solution level interaction was observed [F(2,20) = 4.10, P < 0.05]. Again, only when the 50% solution was given did gum Arabic-treated marmosets have a significantly higher foraging frequency than the gum guar group, as indicated by post hoc analyses [t(1) = 4.94, P < 0.001]. Correlations between the frequencies of foraging bouts and

30

Inter-foraging interval (s)

50

400

20

10

0

*

*

50

25

** 15

Fig. 2. Top: mean (+SEM) number of foraging bouts when water, gum Arabic or gum guar was provided, summed during the nine (three morning + three afternoon) sessions and scored during the first 5-min of each trial and solution tested; middle: mean (+SEM) time spent foraging (in s), summed during the nine (three morning + three afternoon) sessions and scored during the first 5-min of each trial and solution tested. Bottom: mean (+SEM) interval between consecutive foraging bouts, averaged for each trial and then over the nine (three morning + three afternoon) sessions, relative to its respective foraging bout frequency, and scored during the first 5-min after the provisions were made available (50, 25 and 15% m/m gum:water). Water-treated marmosets were not included in the statistical analyses (refer to section 2.7.2); n = 6/group; *P < 0.05 vs. guar; **P < 0.05 vs. respective 50% and 25% solution.

solution levels were not significant for both groups [Arabic: r = 0.43, P = 0.07; guar: r = −0.45, P = 0.06]. The total time marmosets spent foraging during the first 5-min after the provisions were placed in their homecages (Fig. 2) did not differ significantly between the two gum-treated groups [F(1,10) = 0.43, P = 0.53] and the three solution levels tested [F(2,10) = 0.63, P = 0.53], with no significant group × solution level interaction [F(2,20) = 3.13, P = 0.07]. Foraging time, however, was negatively correlated to the percentage of gum in the solution for the guar treated animals [r = −0.54, P < 0.05], with no significant effect for the gum-Arabic group [r = 0.30, P = 0.23]. Foraging continued throughout the 30-min interval in which gum was provided to the marmosets (informal observation). As water was not consumed during the study, foraging time

R. Pupe et al. / Applied Animal Behaviour Science 133 (2011) 246–253 Table 1 Body weight of marmosets (in g), before and after, the provision of water, gum Arabic or gum guar. Experimental group

Body weighta Before

After

Water Gum Arabic Gum guar

352 ± 13 358 ± 07 334 ± 12

385 ± 11 361 ± 06 318 ± 27

a

Mean ± SEM.

and frequency were not observed in the (water) control group. 3.2.4. Inter-foraging interval The mean interval between consecutive foraging bouts during the first 5-min after the provisions were made available, relative to their respective bout frequencies (Fig. 2), differed significantly between the two gum-treated groups [F(1,10) = 8.73, P < 0.01] and the three solution levels tested [F(2,10) = 5.73, P < 0.05]. A significant group × solution level interaction was also observed [F(2,20) = 5.98, P < 0.05]. Thus, when the 50% and 25% solutions were given to the gum Arabic-treated marmosets, inter-foraging intervals were significantly shorter than those of the gum guar group, as indicated by post hoc analyses [50%: t(1) = −8.83, P < 0.05; 25%: t(1) = −8.17, P < 0.05]. In addition, interforaging intervals were significantly shorter when the 15% solution was offered, compared to the other two solution levels, although only within the gum guar-treated animals [gum Arabic: F(2,5) = 0.39, P = 0.69; guar: F(2,5) = 4.22, P < 0.05]. This parameter was negatively correlated to the percentage of gum in the solution for the guar group [r = −0.71, P < 0.05], while no significant effect was seen in the Arabic-treated animals [r = 0.19, P = 0.44]. As water was not consumed during the study, foraging bouts were not observed in the control group. 3.3. Marmoset body weight Marmoset body weight, determined prior to and immediately after the 3-week study period (Table 1), did not differ significantly between the control, gum Arabic and gum guar groups [F(2,16) = 2.97, P = 0.08] or the two measurements [F(1,16) = 0.84, P = 0.37], with no significant group × before/after interaction [F(1,32) = 3.57, P = 0.06]. 4. Discussion In the present study, adult captive black tufted-ear marmosets promptly consumed water-solubilized gum, whereas intake and foraging were not recorded when a control solution containing only water was offered. Other neotropical species also seem highly partial to gum Arabic supplements in their diets (Caton et al., 1996; Herron et al., 2001; McGrew et al., 1986; Power and Oftedal, 1996), but no information is yet available for gum guar. Also, consumption and foraging bouts were observed throughout the 30-min provision interval for both gum types (informal observation), suggesting that motivation due to nutrient deficiency and/or high food preference played a

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secondary role in the marmosets’ preference/palatability. In fact, longer feeding time promotes overall activity and leads to an improvement in animal welfare (Morgan and Tromborg, 2007). Although gum Arabic was generally preferred over gum guar, a significantly greater amount of the former was only consumed for the 50% solution, as was the number of foraging bouts; i.e., for the highest gum:water ratio tested. In fact, gum Arabic intake was negatively correlated with its percentage in the solution, even if significant differences were not observed between the three solution levels tested within either type of gum. The time spent foraging and total number of bouts were also similar among the solution levels, with a significantly shorter latency between consecutive foraging bouts when gum Arabic-treated marmosets were given the 50% and 25% solutions, compared to the gum guar group. Such foraging profile thus indicates that marmosets not only consumed a greater amount gum Arabic, but also did so more efficiently, particularly when a more concentrated (viscous) sample was used. Similar results for this type of gum have been reported (Herron et al., 2001; Lacher et al., 1981, 1984). On the other hand, marmosets seemed less capable of separating manageable amounts of gum guar from the bowl and spent a lot of time chewing (informal observations). Gum guar intake and foraging time/frequency were indeed negatively correlated with its percentage in the solution. Thus, gum type and solution level seemed to influence its intake and foraging. Several aspects may have contributed to this result, including those inherent to each gum type, such as consistency, color and odor, aside from its flavor. In this sense, water-solubilized gum Arabic not only yielded a homogeneous golden-brown viscous/liquid solution, but the experimenter could perceive a distinct honey-like odor as well. Several types of gum harvested by wild marmosets have similar characteristics (e.g., Stevenson and Rylands, 1988). On the other hand, water-solubilized gum guar yielded a sticky white heterogeneous paste, with no perceivable odor. Although handling time negatively influenced food preference in different callitrichid species (Rosati et al., 2006), Caldwell et al. (2009) reported that captive common marmosets preferred sticky/chewable food items (e.g., marshmallow). Given this discrepancy, the distinct coloring of the solubilized gums tested could be an additional influencing factor in the present study. In callitrichids, as with other primates, visual stimuli guide foraging (e.g., Bicca-Marques and Garber, 2004), with females having preferential access to restricted food sources (e.g., Box, 1997; Yamamoto et al., 2004). However, in the present study, latency to first intake was similar for both gum types, all three solution levels and in males/females. Therefore, other aspects possibly contributed to the intake, foraging and latency results observed, including the use of gum-naïve and related individuals, as well as a simple and novel task (Addessi et al., 2007; Day et al., 2003; Yamamoto et al., 2004), in addition to the gums’ odor, flavor and nutritional value. These results should be interpreted cautiously, as only the first 5min of each 30-min trial was scored and the fact that some individuals were related. Further studies are thus need, not only assessing a greater number of behavioral parameters

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during a longer period, but also systematically varying certain aspects of the intended gum supplement to determine which features exert the most significant role on the marmosets’ palatability. On the other hand, the time of provision (i.e., morning vs. afternoon) did not influence any of the parameters presently scored. Callitrichids specialized in gummivory engage in feeding and gum-harvesting behavior early in the morning and late afternoon (Alonso and Langguth, 1989; Canale et al., 2008; Ramirez et al., 1977). Those who do not possess morphological adaptations, such as tamarins, consume gum late in the afternoon to maximize energy attainment by increasing gut retention time (Heymann and Smith, 1999). Changes in body weight were also not observed between and within all three experimental groups. Initial body weight was well above the 250 g minimum indicated for the species (Peters and Guerra, 1998; Stevenson and Rylands, 1988), with gum only being provided during eighteen 30-min trials held over a 3-week period. Thus a ceiling effect and/or insufficient exposure may have occurred, with a more prolonged and extensive supplementation regime being suggested in future studies. Body weight is frequently used for clinical evaluations (Ludlage and Mansfield, 2003) and to assess new maintenance routines (Rennie and Buchanan-Smith, 2006). Nonetheless, the introduction of novel foods may influence behavior and/or other clinical parameters, without necessarily altering body weight. In captivity, food is generally provided at predictable hours, has a standardized composition oftentimes different from what is explored by wild individuals and requires a minimal effort to obtain, limiting foraging opportunities (Morgan and Tromborg, 2007). Such aspects more often than not lead to stress and stereotyped behaviors in various animals kept in captive conditions, including birds, rodents, livestock, carnivores and primates (reviewed in Morgan and Tromborg, 2007). Thus dietary enrichment, typically implemented in the form of food supplements, reduces nutritional deficiencies, while allowing animals to engage in species-typical behaviors. For marmosets, specifically, the introduction of gum seems to be a viable strategy. However, to induce appropriate feeding behaviors, this dietary component should be provided in a more naturalistic context, such as within holes in tree-branches/trunks placed in the animal’s home-cage. Future comparisons between both strategies (i.e., bowls vs. tree-holes) should provide important data on the use of specific procedures for dietary enrichment in this small primate. 5. Conclusion The provision of gum is a viable dietary supplement for captive black tufted-ear marmosets, as demonstrated for other primates. Special attention should not only be given to the specific type of gum provided – as the Arabic version was preferentially consumed by the marmosets – but to its preparation as well, considering that concentrated solutions had a higher and more efficient intake. Also, supplying gum to marmosets may be held in the morning and/or afternoon, according to the routine maintenance

procedures of each particular colony. Specific variations in the dietary enrichment protocol to be implemented should be carefully tested in future studies, including a more naturalistic approach on how to provided the animals with the gum supplement. Nevertheless, dietary enrichment through food supplementation, in this and other animal species, can ultimately increase captive management and animal welfare. Acknowledgements This study was supported by CAPES/DAAD/PROBAL (324/09 to MB). RCP received a master’s fellowship from CAPES/Brazil and MB a researcher fellowship from CNPq/Brazil (311621/2009-0). These funding sources had no involvement in the study design, data collection, analysis or interpretation, writing the manuscript or decision to submit it for publication. The authors would like to thank Dr. C. Uribe for assistance in running the statistical analyses and Drs. D. Teixeira and R. de Oliveira, as well as G. Vieira and A.P.N. da Silva, for their excellent care of the animals. The comments and suggestions of two anonymous reviewers also contributed to the final version of this manuscript. The experiments described herein complied with regulations of the Brazilian Institute of Environment and Renewable Natural Resources (IBAMA), as well as the ‘Brazilian Principles of Laboratory Animal Use’ (COBEA), and was approved by the Animal Ethics Committee of the University of Brasilia. References Addessi, E., Chiarotti, F., Visalberghi, E., Anzenberger, G., 2007. Response to novel food and the role of social influences in common marmosets (Callithrix jacchus) and Goeldi’s monkeys (Callimico goeldii). Am. J. Primatol. 69, 1210–1222. Alonso, C., Langguth, A., 1989. Ecologia e comportamento de Callithrix jacchus (Primates: Callitrichidae) numa ilha de floresta Atlântica. Rev. Nordestina Biol. 6, 105–137. Bicca-Marques, J.C., Garber, P.A., 2004. Use of spatial, visual, and olfactory information during foraging in wild nocturnal and diurnal anthropoids: a field experiment comparing Aotus, Callicebus, and Saguinus. Am. J. Primatol. 62, 171–187. Box, H., 1997. Foraging strategies among male and female marmosets and tamarins (Callitrichidae): new perspectives in an underexplored area. Folia Primatol. 68, 296–306. Caldwell, C.A., Watson, C.F.E., Morris, K.D., 2009. Exploiting flavour preferences of common marmosets to increase palatability of a dry pellet diet. Appl. Anim. Behav. Sci. 116, 244–249. Canale, G., Braga, A., Gondim, L., Santee, D., 2008. Seqüência de comportamentos de Callithrix penicillata durante a gomivoria. In: Ferrari, S.F., Rímoli, J. (Eds.), A Primatologia no Brasil, vol. 9. Sociedade Brasileira de Primatologia, Aracaju, Brazil. Caton, J.M., Hill, D.M., Hume, I.D., Crook, G.A., 1996. The digestive strategy of the common marmoset. Callithrix jacchus. Comp. Biochem. Physiol. 114, 1–8. Day, R.L., Coe, R.L., Kendal, J.R., Laland, K.N., 2003. Neophilia, innovation and social learning: a study of intergeneric differences in callitrichid monkeys. Anim. Behav. 65, 559–571. Ferrari, S.F., Martins, E.S., 1992. Gummivory and gut morphology in two spympatric callitrichids (Callithrix emiliae and Saguinus fuscicollis weddelli) from Western Brazilian Amazonia. Am. J. Phys. Anthropol. 88, 97–103. Ferrari, S.F., Lopes, M.A., Krause, E.A.K., 1993. Gut morphology of Callithrix nigriceps and Saguinus labiatus from Western Brazilian Amazonia. Am. J. Phys. Anthropol. 90, 487–493. Fonseca, G.A.B., Lacher, T.E., 1984. Exudate-feeding by Callithrix jacchus penicillata in semideciduous woodland (cerradão) in central Brazil. Primates 25, 441–450.

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