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<strong><em>Enrichment Effects on Lemur Behavior and Exhibit Visibility</em></strong>
<em> Lemur catta and Eulemur fulvus rufus</em>
<em> Smithsonian’s National Zoological Park</em>
<em>Melba Brown, Thomas Morere, Lawrence Anderson and Jane Steil</em>

<strong>Introduction</strong>

Visitors to The National Zoo’s Lemur Island (photo 1) are treated to a scenic view of plant life and a towering waterfall. The island is a mixed-species exhibit that features 2.2 Ring-tailed Lemurs, <em>Lemur catta</em> (photo 2); 1.1 Red-fronted Lemurs, <em>Eulemur fulvus rufus</em> (photo 3); 0.0.100+ Turtles (Red-eared Sliders, <em>Trachemys scripta elegans</em>; Yellow-bellied Sliders, <em>Trachemys scripta script</em>; and Hybrid Sliders, Painted Turtles, <em>Chrysemys picta</em>; 0.0.3 Box Turtles, <em>Terrapene carolina</em>); 0.0.2 Bullfrogs, <em>Lithobates catesbeiana</em>; Toads, <em>Anaxyrus sp</em>; and 0.0.1 Northern Brown Snake, <em>Storeria dekayi</em>. The indoor facilities include 7 off-exhibit enclosures with a runway along one side and has cross chute capabilities. The lemurs stay indoors in the evening and during harsh weather. When on exhibit, however, the lemurs spend a significant amount of time away from public view on Olmstead Walk, the zoo’s main thoroughfare. The back of the island attracts the lemurs more than the front. Visitor traffic behind the exhibit is low and visitor frustration is often expressed by the question, “Where are the lemurs?”

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To explore this particular management challenge, this study looked at the effects of gustatory, olfactory, visual and tactile enrichment presented on the island. The research objectives were to determine the activity budgets for the lemurs; determine their exhibit space and surface use; introduce and evaluate enrichment on Lemur Island; and, increase the lemurs’ visibility. This paper presents the results relating to activity budgets and enrichment effects on lemur behavior and exhibit visibility. The exhibit space and surface use results will be published in another publication.

Prior to this study, when the lemurs were offered food items on the island, they were difficult to shift indoors when needed. Also, due to a previous rodent problem on the island, prepared food is not offered to them while on exhibit. They do, however, forage on a variety of plants growing in and near the exhibit such as Scarlet Curls Willow (<em>Salix matsudana</em> x <em>S. alba</em>), Common Plantain (<em>Plantago major</em>), Ground Ivy (<em>Glechoma hederacea</em>), Crape Myrtle (<em>Lagerstroemia sp.</em>) flowers and dried leaf litter. Of particular note is their preference for new leaf growth on the Scarlet Curls Willow and Common Plantain herb. This tendency towards eating new plant growth has been seen in semi-free-ranging ring-tailed lemurs (Dierenfeld and McCann, 1999).

Several reasons expressed by staff as to why the lemurs prefer the back of the island include fear of turtles and hawks, presence of trees and shade availability, heated huts, ground cover; and a general anticipation of entering the building for the PM feeding. The entryway into the indoor facility is located at the back of the island. One additional reason for the preference could be that the boulders along the front of the exhibit may get too hot during warmer weather and the lemurs limit their time walking on them.

Informal preliminary observations revealed that the lemurs, when on exhibit, were motivated to move and explore the island in search of foraging material (leaves, tree buds, small plants and leaf litter). Thick vegetation is concentrated on the back and sides of the island. The front of the island consists primarily of boulders, a waterfall and pool. There is sparse vegetation as well as limited shaded areas along the front of the exhibit. Their basic preference for the back of the island may simply be due to the higher concentration of foliage. The lemurs have been observed along the front of the exhibit but only for relatively short periods of time in comparison to their time spent elsewhere.

<span style="font-weight: bold; text-align: left;">Animals and Method</span>

Lemurs are prosimians that are native to Madagascar and the Comores Islands. They live in varied habitats. They are folivorous and will ingest fruit, insects, soil and other matter (Simmen et al., 2006). One of the main physical characteristics of lemurs is a moist nose and a high level of olfaction. They have scent glands and use chemical communication to transmit specific information between individuals and groups. Ring-tailed lemurs have striking black and white tails. Males and females look similar but closer inspection reveals distinctive features. The Lemur Island ring-tailed lemurs range in age from 12 years to 23 years. Red-fronted Lemurs are a subspecies of Brown Lemur, Eulemur fulvus. Males and females are sexually dichromatic. In photo 3, the male is in the foreground and the female is in the background. The red-fronted lemurs are 19 and 26 years-old.

The research objectives were explored by placing 4 forms of enrichment along pre-determined, as well as random locations on the island and quantifying the information gathered by establishing the lemurs’ activity budgets without the enrichment and then comparing this baseline data to their activity budgets once the enrichment items were in place. An emphasis was placed on exhibit location to determine how effective the enrichment was as far as increasing animal visibility. To facilitate island observations and measure visibility, the island was divided into quadrants and coded as Q1 (front left); Q2 (rear left); Q3 (rear right); and Q4 (front right.)

The behaviors observed and recorded were Rest, Move, Forage, Groom, Other and Not Visible. For the purpose of this study, we defined ‘Forage’ as the actual act of solid or liquid consumption.

<strong>Enrichment</strong>

Browse: Each day, a wheelbarrow full of browse [Maple — <em>Acer platanoides</em> (Norway), <em>Acer saccharinum</em> (sugar), <em>Acer japonica</em> (Japanese red)], Bamboo — <em>Phyllostachys aureosulcata</em> (yellow groove,) <em>Phyllostachys aurea</em> (golden) or <em>Phyllostachys bisettii</em>, <em>Pseudosasa japonica</em> (arrow), Bradford Pear (<em>Pyrus calleryiana</em>) and/or Mulberry — <em>Morus alba</em> (white) and/or <em>Morus rubra</em> (red) was divided and placed in different locations (photo 4).

2.) Fresh Rosemary (<em>Rosmarinus officinalis</em>) Sprigs: Each day, 7-9 sprigs were placed in different locations (photo 5). Prior to being put on the island, the sprigs were rubbed to release more of their herbaceous scent. Ring-tailed lemurs have been observed in the wild ingesting herbs (Soma, 2006).

3.) Ginger (<em>Zingiber officinale</em>) Essential Oil in Cholla Wood: Essential oils are extractions from plant parts (petals, roots, leaves, bark). Cholla wood is the skeletal part of a cholla cactus (<em>Opuntia sp.</em>). Each day, 7-10 drops of essential oil were placed along each piece of cholla wood (photo 6). Eight pieces of wood were used for this phase. The highly-scented wood was placed in different locations on the island. At the end of each day, the wood was collected and placed in a plastic bag and the next day, additional drops were added so that each consecutive day of the study, the scent on the wood became more concentrated.

4.) Clay-rich Soil: The island soil is dry and very compact and not readily available or attractive to the lemurs as evidenced by preliminary observations. Each day, 31bs of soil was divided into piles and placed in different locations (photo 7). The enrichment soil was collected and processed to remove any unwanted matter. The soil was stored in a refrigerator prior to use. Primates have been heavily documented as engaging in geophagy (Krishnamani and Mahaney, 2000) (Ganzhorn, 1987) (Pinkus, Susan, Smith, James N.M. and Jolly, Alison, 2006).

The Group Scan-sampling Methodology was used for this project. The research team used a stopwatch and data collection sheets for coded entries. For each part of the study, the observers conducted five, 30-minute observations at 3-minute intervals per day for four days between the hours of 10:00am – 2:30pm (1000hr-1430hr). The 3-minute interval was determined to be the best one after conducting preliminary trials with 1-minute and 2-minute intervals. When inclement weather prevented observations, the study continued on the next scheduled day. Temperature and weather conditions were noted on the data sheets: sunny, cloudy, partly sunny or partly cloudy. Four additional observers were involved in data collection to help reduce observer bias. The total observation hours were 50 hours per species. There were 20 observation days. The data were analyzed and entered into histograms with a 5% standard deviation. The information is presented in percentages of time spent engaged in observed activities. The unpaired t test was used to determine significance.

<strong>Results</strong>

Chart 1 illustrates the activity budget results for the ring-tailed lemurs. The majority of time was spent resting (51%). In comparison, a field study of Malagasy ring-tailed lemurs reported a similar resting budget result (53.7%) (Simmen et al., 2010). The ring-tailed lemurs had significant movement behavior (23%) and grooming behavior (14%). They were not visible a lower percentage of time (9%). Foraging was the least frequent behavior (3%).

Chart 2 illustrates the activity budget results for the red-fronted lemurs. The resting behavior was the dominant behavior (60%). In comparison, a field study of red-fronted lemurs reported a lower resting budget result (47%) (Overdorff, 1996). The 27% increase seen in our lemurs may be a result of the weather and/or age. The red-fronted lemurs were not visible 33% of the time which is more than three times that of the ring-tailed lemurs. This is understandable due to the small sample size: n=2. The movement behavior (3%), grooming behavior (1%), and foraging behavior (2%) results were low.

The ring-tailed lemur Chart 3 illustrates their baseline activity as it relates to the enrichment. The resting behavior and ginger/cholla enrichment result was found to be extremely significant (P = 0.0002); and, the resting behavior and soil enrichment result was very significant (P = 0.0096). The movement behavior with ginger/cholla enrichment resulted in a very significant behavioral decrease (P = 0.0094). The foraging results show some degree of activity increase with the forms of enrichment that could be consumed, namely browse, rosemary and soil. The grooming behavior and ginger/cholla enrichment result shows a significant decrease in this behavior (P = 0.0162). The grooming activity and soil enrichment resulted in a significant decrease in the behavior as well (P = 0.0050). There was, however, an increase in the grooming behavior with the rosemary enrichment. The chart illustrates a level of visibility increase with each form of enrichment.

The red-fronted lemur Chart 4 illustrates their baseline activity as it relates to the enrichment. There was an increase in resting behavior in the presence of rosemary (P = 0.618), ginger/cholla and soil. There was a significant increase in the movement behavior (P = 0.0428) with browse enrichment. The chart shows an increase in foraging activity in the presence of browse, rosemary and soil. The grooming behavior with browse enrichment resulted in a significant increase in the behavior (P = 0.0435). The chart shows an increase in visibility with each form of enrichment. Rosemary was particularly effective in increasing visibility (P = 0.0073).

<strong>Discussion</strong>

The activity budget results for the ring-tailed lemurs were unexpected. One assumption was they were not visible a significant amount of time when on exhibit. The study showed they were not visible 9% of the time. During the summer, the trees on the island have full canopies and when the lemurs are resting in them, they can be difficult to see until they are pointed out by interpreters. Another assumption was they consumed plenty of island vegetation. The results of the study showed a low percentage of time engaged in vegetation consumption. The activity budget results for the red-fronted lemurs support the assumption that they were not visible a significant amount of time (33%). They spent most of their time resting (60%) which could have been a factor of weather extremes and/or age. Also, they moved less than expected which could have been explained by the weather as well. Like the ring-tails, the red-fronted lemurs did not spend a significant amount of time foraging (2%). One thing that was noted consistently during the observations was both groups tended to forage most when they were initially released on the island and early in the growing season. They ate fresh buds on trees, consumed dried leaves and nibbled on low-lying new growth.

The ring-tailed lemurs’ responses to the enrichment forms compared to the baseline activity provided interesting information. The resting behavior increased in the presence of browse, ginger/cholla and soil; and, the resting behavior decreased with the rosemary. They were very attracted to the rosemary and they were observed carrying the sprigs around the island. Their movement showed a slight decrease with the browse and rosemary enrichment and more of a decrease in the presence of ginger/cholla and soil enrichment. Their foraging behavior increased with each form of edible enrichment. They were observed eating the enrichment browse. Also, they readily consumed the soil and were observed increasing their intake of island vegetation. These observations support one of the reasons suggested for geophagy which is to detoxify the system by absorbing tannins and other components found in plants (Johns and Duquette, 1991). The grooming behavior decreased in the presence of browse, ginger/cholla and soil; and, increased with the fragrant rosemary. As was noted above, the ring-tailed lemurs carried the rosemary around the exhibit and the fresh herb, undoubtedly, left its strong scent on their hands and fur which, most likely, caused an increase in the grooming behavior. The other behaviors showed a slight increase with the browse, rosemary and soil. They were not visibly interactive with the ginger/cholla enrichment, even though the scent was prevalent. There were observed instances of displacement among the lemurs which resulted in less enrichment time for particular individuals. There was an increase in visibility with each form of enrichment, in particular, the soil. The ring-tailed lemurs were most visible with the soil present and they were very engaged in soil consumption.

The red fronted lemurs’ responses to the enrichment forms compared to the baseline activity results yielded interesting information as well. The chart indicates that they rested less and moved more, foraged more and groomed more with the browse enrichment. They were observed eating the browse. They became more active and were much more visible. A possible reason could be related to an increase in energy levels with the desired foraging matter available. The chart shows an increase in their foraging behavior in the presence of the enrichment forms that were edible, similar to the ring-tailed lemur results. Of note was their increase in other behaviors in the presence of soil. They were observed ingesting the soil. Again, there were instances of lemur displacement and a degree of competition. The red-fronted lemurs did not physically interact with the ginger/cholla enrichment. The strong concentration of scent may have had a repellent effect. Like the ring-tailed lemurs, the red-fronted lemurs were more visible with each form of enrichment offered.

In conclusion, the presence of varietal enrichment offered on Lemur Island can have a measurable impact on the activity and visibility of the lemurs. Seasonality was a significant factor in this study. The project was conducted in May, June and July of 2011 with high temperatures and humidity. At times, the lemurs were less active than expected most likely due to the weather conditions. Noteworthy, though, was their heightened attraction to the clay-rich soil. A further study may take a closer look at the interactions of the lemurs with clay-rich soil and its impact on island vegetation consumption.

<strong>Acknowledgements</strong>

Smithsonian’s Access to Opportunities Program: – Krista Flores and Emily Shapiro; Ivymount School – great support from Lu Merrick, Laura Klingler, Donna Morere and John Monti; The Primate Unit for great support: Lisa Stevens for project approval, Megan Anderson for being the back-up organizer, Amanda Bania, Marty Dearie, Laurie Thompson, Heather Harl, Becky Malinsky, Erin Stromberg and KC Braesch for lemur shifting and enrichment placement; Eric Kliebert for digging the soil; Heidi Hellmuth – for enrichment support; Brian McLaren, Melinda Whicher &amp; Suzy Alberts – Lemur Island plant IDs; Department of Nutritional Resources for collecting and delivering varietal browse and fresh rosemary – Mike Maslanska, Bill Clements, Karen Lisi, Lisa Schneider, Albert Olsen, Tyrone Savoy, Eric Smith, Bernard Graham, Deb Grupenhoff, Matt Neff, Laurie Smith and Sara Allison; Polly Lasker – NZP Librarian; Dr. Sara Zehr, Research Manager, Duke Lemur Center for species information; Reptile Department – Matt Evans for IDs; Amma Tabirih and Patrice Payne for administrative support; Anthony Hiza and Greg Ose - sounding boards; The Lemurs – Thank you to the red-fronted lemurs - Red Oak and Flare; and the ring-tailed lemurs - Andromeda, Myrto, Ninna and Gelon!

<strong>Bibliography</strong>

Dierenfeld, Ellen S. and McCann, Colleen M. 1999. Nutrient composition of selected plant species consumed by semi free-ranging lion-tailed macaques (<em>Macaca silenus</em>) and ring-tailed lemurs (<em>Lemur catta</em>) on St. Catherines Island, Georgia, U.S.A. <em>Zoo Biology</em>, 18:481-494.

Ganzhorn, Jorg U. 1987. Soil consumption of two groups of semi-free-ranging lemurs (<em>Lemur catta</em> and <em>Lemur fulvus</em>), <em>Ethology</em>, 74, 146-154.

Johns, Timothy and Duquette, Martin. 1991. Detoxification and mineral supplementation as functions of geophagy. <em>American Journal of Clinical Nutrition</em> 53:448-456.

Krishnamani, R and Mahaney William C. 2000. Geophagy among primates: adaptive significance and ecological consequences. <em>Animal Behavior</em>, 59, 899-915.

Overdorff, Deborah J. 1996. Ecological correlates to activity and habitat use of two prosimian primates:(<em>Eulemur rubriventer</em>) and (<em>Eulemur fulvus rufus</em>) in Madagascar. <em>American Journal of Primatology</em>, 40 :327-342.

Pinkus, Susan, Smith, James N.M. and Jolly, Alison. 2006 Feeding competition between introduced (<em>Eulemur fulvus</em>) and native (<em>Lemur catta</em>) during the birth season at Berenty Reserve, Southern Madagascar. <em>Ring-tailed Lemur Biology</em>, 119-140.

Simmen, Bruno et al. 2010. Total energy expenditure and body composition in two free-living sympatric lemurs. <em>PloS One</em>, Volume 5, Issue 3.

Simmen, Bruno et al. 2006. Plant species fed on by (<em>Lemur catta</em>) in gallery forests of the southern Domain of Madagascar. <em>Ring-tailed Lemur Biology</em>, 55-68.

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<strong>BHC Comments by Enrichment Options Co-Editor Richard Kotarsky:</strong>

Thanks Melba, James, Lawrence and Thomas for sharing your paper with the AAZK membership! This paper is another excellent example of a successful goal-directed enrichment initiative that can be used to solve management issues such as visibility of a popular exhibited species. You did an excellent job with the research into the species’ natural histories and natural behaviors; then designing a plan working towards encouraging a specific behavioral goal such as increased activity and visibility for the zoo visitors. Using the ethogram as a tool for your observations to determine the success of the enrichment and the specific goals for each species is an excellent way to quantify and qualify the results. Lastly, your results clearly show that the presence of goal-based varietal enrichment and something as simple as giving variable choices offered daily on the Lemur Island can have an obvious significant impact on the activity and visibility of the lemurs. Thanks again Melba, James, Lawrence and Thomas. I greatly enjoyed your paper.