Enriching Zoo-Housed Ring-Tailed Lemurs (Lemur catta): Assessing the Influence of Three Types of Environmental Enrichment on Behavior
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Subjects and Study Sites
2.2. Enrichment Types
2.3. Data Collection
2.4. Data Analysis
3. Results
3.1. Time Budget
3.2. Generalized Linear Models (GLMs)
4. Discussion
4.1. Time Budget
4.2. Environmental Enrichment Effect
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Subject | Year of Birth | Sex | NDS |
---|---|---|---|
Milly | 1993 | Female | 3.667 |
Bekili | 2000 | Female | 2.500 |
Andribe | 2000 | Female | 2.417 |
Mandrare | 2001 | Female | 1.167 |
Ankarana | 2005 | Male | 1.586 |
Sakalava | 2006 | Female | 3.667 |
Category 1: Locomotion | Description |
Locomotion | An individual ambulates on the ground or on a tree. |
Category 2: Resting | Description |
Resting | An individual remains inactive |
Category 3: Foraging | Description |
Foraging | An individual searches for and eats food with nose over the ground or terminal branch parts. |
Feeding | An individual eats food provided by keepers. |
Category 4: Stress-related behaviors | Description |
Self-grooming | An individual cleans its own fur. |
Scratching | An individual repeatedly and rapidly moves its hind limb digits over its own fur. |
Yawning | An individual stretches mouth wide open without vocalizing in non-feeding, non-resting social context. |
Category 5: Affiliative behaviors | Description |
Sit in contact | Two or more individuals are sitting in reciprocal contact. |
Proximity | Two individuals are far apart for a length not exceeding that of an arm. |
Grooming | An individual cleans another one’s fur with dental comb and/or tongue. This behavior could be made or received. |
Reciprocal grooming | Two individuals grooming each other. |
Play | Two or more individuals play together. The most common forms of social play are the “rough and tumble”, which can include, for example, play slaps, play bites etc., and the “play run”, where one subject chases another one. |
Category 6: Agonistic behaviors | Description |
Bite | An individual bites another one. |
Charge | An individual sprints < 5 m toward partner. |
Cuff | An individual strikes partner (or attempt). |
Full cuff | Same as cuff but some fur is pulled out. |
Chase | An individual chases another one. |
Muzzle | An individual has physical contact with the antagonist, but still not serious. it is used in minor situations. The animal gives a slap to the other with a quick swipe of the muzzle. |
Stare | An individual widens eyes during mutual gazing with partner. |
Go towards | An individual walks in a straight line towards the subject involved in the conflict. Often it assumes a gait with almost exaggerated and bold movements, moves with straight and rigid legs, keeps its head and tail very high and straight and continues to stare at the subject towards which it is heading. |
Jump fight | Two individuals face each other on the ground in a race of jumping on two legs, holding their arms up and out, jumping around each other and trying to scratch, hit and bite the opponent. |
Dismiss | An individual causes a lower-ranking subject to move from a certain point by a short vocalization. |
Avoid | When an individual avoids interacting with another one, or when it changes its moving direction or goes far away from the latter. |
Check scared | An individual who is being pursued stops and turns to look at his pursuer. The subject is in an alert position with his ears straight forward and with his eyes wide open and fixed on his pursuer. |
Jump away | An individual leaps away from nearby partner (2 m) |
Run away | An individual who is being chased runs away by running or jumping on branches trying to get as far away from his pursuer as possible. |
Be displaced | An individual walks away after gazing at approaching conspecific. |
Glance | An individual gazes rapidly toward and away from the partner. |
Category 7: Explorative and scent-marking behaviors | Description |
Skin lick | An individual licks a partner’s palms, soles, eyelids or nostrils. |
Wrist mark | An individual scars arboreal substrate with carpal spur near antebrachial gland. |
Wrist to pit | An individual rubs antebrachial gland against axillary gland. |
Genital mark | An individual holds/rubs genitalia against arboreal substrate. |
Urine mark | An individual urinates on the substrate with the hindquarters down and the tail raised like a question mark. |
Anoint tail | An individual passes the ventral surface of the wrists and arms along the tail held between the legs and held erect in front of the back. |
Wave tail | An individual arches his tail over his head and waves it in the direction of a conspecific to expand the smell, usually made after the anoint tail. |
Sniff body | An individual places the nose less than 3 cm from the partner’s body, excluding the nose and the genital area. |
Sniff genital | An individual places his nose less than 3 cm from the genital area and licks it. |
Category 8: Self-maintenance | Description |
Sun bathing | An individual sits upright in an area with sunlight, with the belly-side directed towards the sun and arms open. |
Urinate | An individual eliminates urine without a specific posture but with a lowered tail. |
Defecate | An individual eliminates faces without a specific posture. |
Category 9: Abnormal repetitive behaviors | Description |
Locomotory pacing | An individual walks/runs repeatedly along the same route. |
Head trough-back | An individual repeatedly tosses its head in a circular motion. |
Overgroom | An individual cleans itself or another individual excessively, resulting in bald patches of fur. |
Self-injurious | An individual uses teeth, claws or nails to harm to itself. |
Category 10: Vigilance | Description |
Vigilance | An individual observes the surrounding environment while is sitting or standing. |
Category 11: Inter-specific interactions | Description |
Human–lemur interaction | An individual pays attention to, approaches, moves away from, etc., visitors, keepers or the observer. |
Animal–lemur interaction | An individual pays attention to, approaches, moves away from, etc., other animals, such as peacocks and dogs. |
Category 12: Out of sight | Description |
Out of sight | An individual is not visible to the observer. |
Predictors | Estimates | SEM | C.I. | ꭓ2 | p |
GLMM1 (locomotion) | |||||
Intercept a | 3.476 | 0.450 | 2.589, 4.363 | a | a |
Age | −0.048 | 0.015 | −0.077, −0.019 | −3.217 | 0.001 |
NDS | 0.009 | 0.066 | −0.122, 0.139 | 0.131 | 0.896 |
Condition_E1 b | 0.362 | 0.311 | −0.252, 0.975 | 1.163 | 0.245 |
Condition_E2 b | 0.146 | 0.306 | −0.457, 0.750 | 0.479 | 0.632 |
Condition_E3 b | 0.137 | 0.318 | −0.489, 0.764 | 0.433 | 0.665 |
Condition_NE b | −0.023 | 0.315 | −0.644, 0.598 | −0.073 | 0.942 |
Day of week_weekend b | 0.091 | 0.094 | −0.094, 0.277 | 0.971 | 0.331 |
Ambient temperature | −0.041 | 0.014 | −0.067, −0.014 | −2.965 | 0.003 |
Condition_E1 × age b | −0.004 | 0.019 | −0.042, 0.034 | −0.214 | 0.830 |
Condition_E2 × age b | −0.002 | 0.019 | −0.039, 0.035 | −0.087 | 0.931 |
Condition_E3 × age b | −0.002 | 0.020 | −0.041, 0.036 | −0.109 | 0.913 |
Condition_NE × age b | 0.007 | 0.019 | −0.031, 0.045 | 0.379 | 0.705 |
Condition_E1 × NDS b | 0.064 | 0.086 | −0.106, 0.233 | 0.742 | 0.458 |
Condition_E2 × NDS b | 0.147 | 0.085 | −0.021, 0.315 | 0.730 | 0.084 |
Condition_E3 × NDS b | 0.095 | 0.088 | −0.078, 0.269 | 1.080 | 0.280 |
Condition_NE × NDS b | 0.110 | 0.088 | −0.063, 0.283 | 1.252 | 0.210 |
GLMM2 (stress-related behavior) | |||||
Intercept a | 0.967 | 0.779 | −0.569, 2.503 | a | a |
Age | −0.075 | 0.022 | −0.119, −0.031 | −3.387 | 0.001 |
NDS | 0.037 | 0.095 | −0.151, 0.224 | 0.386 | 0.670 |
Condition_E1 b | −0.901 | 0.613 | −2.109, 0.308 | −1.470 | 0.142 |
Condition_E2 b | −1.590 | 0.506 | −2.588, −0.592 | −3.142 | 0.002 |
Condition_E3 b | −0.904 | 0.553 | −1.994, 0.187 | −1.634 | 0.102 |
Condition_NE b | −1.369 | 0.566 | −2.485, −0.253 | −2.420 | 0.016 |
Day of week_weekend b | −0.568 | 0.243 | −1.048, −0.088 | −2.334 | 0.020 |
Ambient temperature | 0.030 | 0.024 | −0.018, 0.077 | 1.231 | 0.218 |
Condition_E1 × age b | 0.004 | 0.037 | −0.070, 0.078 | 0.102 | 0.919 |
Condition_E2 × age b | 0.072 | 0.030 | 0.013, 0.131 | 2.395 | 0.017 |
Condition_E3 × age b | 0.032 | 0.034 | −0.035, 0.099 | 0.944 | 0.345 |
Condition_NE × age b | 0.059 | 0.034 | −0.009, 0.126 | 1.704 | 0.088 |
Condition_E1 × NDS b | 0.045 | 0.163 | −0.277, 0.367 | 0.274 | 0.784 |
Condition_E2 × NDS b | 0.227 | 0.143 | −0.055, 0.509 | 1.587 | 0.113 |
Condition_E3 × NDS b | 0.051 | 0.151 | −0.248, 0.350 | 0.337 | 0.736 |
Condition_NE × NDS b | 0.096 | 0.160 | −0.219, 0.411 | 0.604 | 0.546 |
GLMM4 (affiliative behavior) | |||||
Intercept a | −1.679 | 0.882 | −3.418, 0.061 | a | a |
Age | 0.002 | 0.021 | −0.039, 0.042 | 0.089 | 0.929 |
NDS | 0.358 | 0.116 | 0.130, 0.587 | 3.094 | 0.002 |
Condition_E1 b | −0.605 | 0.569 | −1.727, 0.517 | −1.063 | 0.288 |
Condition_E2 b | −1.204 | 0.659 | −2.503, 0.095 | −1.827 | 0.068 |
Condition_E3 b | −0.493 | 0.587 | −1.651, 0.665 | −0.839 | 0.401 |
Condition_NE b | 0.162 | 0.615 | −1.051, 1.376 | 0.264 | 0.792 |
Day of week_weekend b | −0.075 | 0.220 | −0.508, 0.358 | −0.343 | 0.732 |
Ambient temperature | 0.053 | 0.027 | −0.001, 0.107 | 1.920 | 0.055 |
Condition_E1 × age b | 0.007 | 0.029 | −0.050, 0.064 | 0.237 | 0.813 |
Condition_E2 × age b | 0.049 | 0.037 | −0.025, 0.123 | 1.311 | 0.190 |
Condition_E3 × age b | 0.023 | 0.032 | −0.041, 0.086 | 0.706 | 0.480 |
Condition_NE × age b | −0.032 | 0.033 | −0.098, 0.033 | −0.978 | 0.328 |
Condition_E1 × NDS b | 0.115 | 0.169 | −0.218, 0.449 | 0.680 | 0.496 |
Condition_E2 × NDS b | −0.076 | 0.209 | −0.488, 0.337 | −0.362 | 0.718 |
Condition_E3 × NDS b | −0.075 | 0.179 | −0.428, 0.278 | −0.417 | 0.677 |
Condition_NE × NDS b | −0.084 | 0.178 | −0.435, 0.266 | −0.474 | 0.636 |
GLMM5 (agonistic behavior) | |||||
Intercept a | 3.712 | 2.550 | −1.327, 8.751 | a | a |
Age | −0.126 | 0.041 | −0.207, −0.044 | −3.052 | 0.002 |
NDS | −0.260 | 0.148 | −0.552, 0.032 | −1.758 | 0.079 |
Condition_E1 b | 2.317 | 0.720 | 0.898, 3.736 | 3.220 | 0.001 |
Condition_E2 b | 1.759 | 0.697 | 0.384, 3.134 | 2.522 | 0.012 |
Condition_E3 b | 1.666 | 0.757 | 0.174, 3.159 | 2.201 | 0.028 |
Condition_NE b | 1.824 | 0.727 | 0.391, 3.257 | 2.509 | 0.012 |
Day of week_weekend b | −0.421 | 0.630 | −1.664, 0.822 | −0.668 | 0.504 |
Ambient temperature | −0.158 | 0.090 | −0.336, 0.020 | −1.750 | 0.080 |
GLMM6 (explorative and scent-marking behavior) | |||||
Intercept a | 1.879 | 0.932 | 0.040, 3.717 | a | a |
Age | −0.019 | 0.026 | −0.071, 0.032 | −0.739 | 0.460 |
NDS | 0.316 | 0.140 | 0.040, 0.592 | 2.257 | 0.024 |
Condition_E1 b | 2.003 | 0.645 | 0.732, 3.275 | 3.108 | 0.002 |
Condition_E2 b | 1.339 | 0.655 | 0.048, 2.631 | 2.045 | 0.041 |
Condition_E3 b | 1.467 | 0.662 | 0.162, 2.772 | 2.217 | 0.027 |
Condition_NE b | 1.545 | 0.719 | 0.127, 2.964 | 2.149 | 0.032 |
Day of week_weekend b | 0.102 | 0.216 | −0.325, 0.529 | 0.471 | 0.637 |
Ambient temperature | −0.075 | 0.029 | −0.132, −0.018 | −2.607 | 0.009 |
Condition_E1 × age b | −0.052 | 0.037 | −0.125, 0.022 | −1.389 | 0.165 |
Condition_E2 × age b | −0.033 | 0.037 | −0.107, 0.041 | −0.882 | 0.378 |
Condition_E3 × age b | −0.032 | 0.038 | −0.107, 0.043 | −0.839 | 0.402 |
Condition_NE × age b | −0.051 | 0.043 | −0.135, 0.033 | −1.196 | 0.231 |
Condition_E1 × NDS b | −0.323 | 0.179 | −0.677, 0.031 | −1.802 | 0.072 |
Condition_E2 × NDS b | −0.226 | 0.185 | −0.592, 0.139 | −1.223 | 0.221 |
Condition_E3 × NDS b | −0.274 | 0.186 | −0.642, 0.093 | −1.471 | 0.141 |
Condition_NE × NDS b | −0.357 | 0.199 | −0.750, 0.035 | −1.796 | 0.073 |
GLMM7 (foraging) | |||||
Intercept a | 1.871 | 0.832 | 0.230, 3.512 | a | a |
Age | −0.012 | 0.025 | −0.062, 0.037 | −0.493 | 0.622 |
NDS | −0.006 | 0.117 | −0.237, 0.224 | −0.054 | 0.957 |
Condition_E1 b | 0.120 | 0.539 | −0.864, 1.264 | 0.371 | 0.711 |
Condition_E2 b | −0.430 | 0.536 | −1.488, 0.627 | −0.802 | 0.422 |
Condition_E3 b | −0.796 | 0.636 | −2.050, 0.457 | −1.253 | 0.210 |
Condition_NE b | 0.299 | 0.056 | −0.806, 1.404 | 0.534 | 0.593 |
Day of week_weekend b | −0.559 | 0.250 | −1.053, −0.066 | −2.235 | 0.025 |
Ambient temperature | −0.035 | 0.026 | −0.087, 0.016 | −1.355 | 0.176 |
Condition_E1 × age b | 0.016 | 0.035 | −0.054, 0.086 | 0.442 | 0.658 |
Condition_E2 × age b | 0.056 | 0.036 | −0.016, 0.127 | 1.536 | 0.125 |
Condition_E3 × age b | 0.008 | 0.039 | −0.070, 0.085 | 0.196 | 0.845 |
Condition_NE × age b | 0.027 | 0.038 | −0.048, 0.103 | 0.714 | 0.475 |
Condition_E1 × NDS b | −0.075 | 0.163 | −0.396, 0.246 | −0.461 | 0.645 |
Condition_E2 × NDS b | −0.055 | 0.169 | −0.388, 0.279 | −0.323 | 0.747 |
Condition_E3 × NDS b | 0.155 | 0.190 | −0.219, 0.529 | 0.816 | 0.414 |
Condition_NE × NDS b | −0.206 | 0.173 | −0.546, 0.135 | −1.192 | 0.233 |
Predictors | Estimates | SEM | ꭓ2 | p |
E1 vs. BL | 2.317 | 0.720 | 3.220 | 0.010 |
E2 vs. BL | 1.759 | 0.697 | 2.522 | 0.080 |
E3 vs. BL | 1.666 | 0.757 | 2.201 | 0.170 |
NE vs. BL | 1.824 | 0.727 | 2.509 | 0.083 |
E2 vs. E1 | −0.558 | 0.385 | −1.451 | 0.581 |
E3 vs. E1 | −0.651 | 0.414 | −1.572 | 0.501 |
NE vs. E1 | −0.493 | 0.404 | −1.222 | 0.727 |
E3 vs. E2 | −0.093 | 0.455 | −0.204 | 1.000 |
NE vs. E2 | 0.065 | 0.434 | 0.149 | 1.000 |
NE vs. E3 | 0.158 | 0.455 | 0.346 | 1.000 |
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Caselli, M.; Messeri, P.; Dessì-Fulgheri, F.; Bandoli, F. Enriching Zoo-Housed Ring-Tailed Lemurs (Lemur catta): Assessing the Influence of Three Types of Environmental Enrichment on Behavior. Animals 2022, 12, 2836. https://doi.org/10.3390/ani12202836
Caselli M, Messeri P, Dessì-Fulgheri F, Bandoli F. Enriching Zoo-Housed Ring-Tailed Lemurs (Lemur catta): Assessing the Influence of Three Types of Environmental Enrichment on Behavior. Animals. 2022; 12(20):2836. https://doi.org/10.3390/ani12202836
Chicago/Turabian StyleCaselli, Marta, Patrizia Messeri, Francesco Dessì-Fulgheri, and Francesca Bandoli. 2022. "Enriching Zoo-Housed Ring-Tailed Lemurs (Lemur catta): Assessing the Influence of Three Types of Environmental Enrichment on Behavior" Animals 12, no. 20: 2836. https://doi.org/10.3390/ani12202836
APA StyleCaselli, M., Messeri, P., Dessì-Fulgheri, F., & Bandoli, F. (2022). Enriching Zoo-Housed Ring-Tailed Lemurs (Lemur catta): Assessing the Influence of Three Types of Environmental Enrichment on Behavior. Animals, 12(20), 2836. https://doi.org/10.3390/ani12202836