Human impact on biodiversity loss is evident worldwide — from deforestation, the bushmeat and pet trades, to the loss of animals critical to the very survival of the forests themselves — seed dispersers and pollinators. However, hope for species preservation is not entirely beyond our grasp.
Along with natural habitat protection, one of the greatest conservation tools we have is maintaining healthy, breeding, captive populations of endangered animals. Perhaps even, one day, they might be released to ‘re-stock’ depleted wild populations – a drastic measure within the field of conservation biology.
Save them, breed them, keep them safe and then, if there is still a ‘there’ to put them back into, put them back there.” — Gerald Durrell, founder of the Jersey Zoo
What is wild animal ‘re-stocking’?
There are three primary classifications of ‘re-stocking’ terminology, as defined by Strum and Southwick (1986):
- Introduction: Places individuals into habitats where that species has never before occurred.
- Reintroduction: Places individuals (either wild-caught or captive) into a suitable habitat that currently lacks that species.
- Translocation: The capture of wild animals from one part of their natural distribution so as to move them to another part.
Further classifications within the “reintroduction” category may be used to provide the most precise information about a program’s intended goals. As described by Viggers et al., (1993) and Cheyne (2009):
- Re-establishment: Using captive-born animals to “re-establish” an already extinct population.
- Stocking-reintroduction: Supplementing a declining population in a natural area with captive-born animals.
- Population reintroduction: Using wild-born (though captive-raised) animals to re-establish an already locally extinct population.
Unfortunately, many (and historically, most) reintroduction attempts of captive-born animals have been unsuccessful (Beck et al., 1994) with the released animals often falling victim to predation. The reintroduction process is also very expensive and time consuming (Vickery and Mason, 2003). As captive environments offer food stability and safety, captive-born animals are often naïve to the dangers in the wild and may, over many generations in captivity, lack the very basic behaviors necessary for survival exhibited by their wild counterparts. Additionally, forest-living animals rely on their abilities to navigate complex, three-dimensional habitats for acquiring food and securing shelters, such that many captive enclosures are unable to match.
Nevertheless, the conservation potential is enough to drive researchers to keep trying – through strategic training of the animals and planning of the reintroduction site.
How is re-stocking done right?
For maximizing the success potential of captive-born reintroductions, Kleiman (1989) outlines a series of prerequisite steps, including:
- Selecting self-sustaining captive populations.
- Choosing a suitable habitat for reintroduction.
- Eliminating factors that caused species decline in the first place (and have the potential to cause continued species decline).
- Training of captive individuals pre-and-post release (i.e., a “soft” reintroduction).
- Long-term fieldwork with the reintroduced population.
- Ongoing collaboration with local communities and governments.
Carrying Capacity of the Area
A necessary component to maximize reintroduction success potential is a strong understanding of the carrying capacity of the area. In ecology, ‘carrying capacity’ can refer to the quantity and quality of the habitat necessary to support and feed growing populations (e.g., Steenweg et al., 2016). In practical terms, the natural carrying capacity must be balanced with the realities of unpredictable deforestation, leading to significant reductions in forest size and quality, often in a very short period of time.
Behavioral Flexibility of the Animal
When selecting a captive species to be reintroduced into an area, you must consider whether the animal is behaviorally specialized or if it can be more flexible. Behavioral flexibility may be a critical trait for the animal’s ability to adapt to new environments. Species that are flexible in their niche breadth (the ways in which they live, move, and find food) have a greater survival advantage when faced with habitat modifications (Souza-Alves et al., 2021). The adoption of crop-raiding strategies by primates in human-modified spaces is an example of this.
An Example Species: Ring-tailed Lemurs
As an example species, ring-tailed lemurs (Lemur catta) are renowned for their ability to adapt to a wide range of habitats, both natural and human-maintained/impacted. They are often classified as opportunistic frugivore-folivores, consuming a wide array of fruits, leaves, flowers, bark, sap, and even soil and insects.
Ring-tailed lemurs even feed on many human-introduced species of plants, including the tamarind tree (Tamarindus indica), which provides a reliable food source during the dry season when many endemic plants are scarce. The ability of ring-tailed lemurs to consume such a diversity of plant species and plant parts across its many habitat types can be described as, “a key to the species’ survival in a time of ecological crisis across its geographic range” (Gould and Gabriel, 2015; p. 320) and may strengthen the case for attempting reintroductions with this species.
Broad Genetic Representation in the Group
Once the most suitable species is selected, the makeup of the captive group is extremely important – how many young, how many breeding males and females? It is necessary for the group to have broad genetic representation and be able to “endure the loss of many animals over a long period while reintroduction techniques…are perfected” (Kleiman, 1989; p. 154).
Pre-release training by zoo staff to prepare captive animals for reintroductions is essential for success. Such training (use of environmental enrichment) may include: hiding provisioned foods, allowing carnivores to hunt and kill prey, and anti-predator training (e.g., how do they react to fake snakes?). Environmental enrichment for captive animals can restore “…the contingency between the performance of behavior (foraging for example) and the appropriate consequence (such as finding food)” (Shepherdson, 1994; p. 168).
A Success Story: Golden Lion Tamarins
The greatest reintroduction success of a primate species is that of the lion-tailed tamarin (Leontopithecus rosalia) of the Golden Lion Tamarin Programme. An initiative begun in the 1970s, it involved participation from captive breeding programs from around 30 zoos in an effort to save the dwindling populations in Brazil (Kleiman et al., 1986).
Reintroductions of 146 captive-born (and five wild-born) animals took place between 1984 and 2000. The program involved post-release provisioning (food supplementation), monitoring, and veterinary support. Although a number died, their offspring demonstrated greater success in their abilities to travel in the trees and forage on the native plants (Stoinski et al., 2003).
As a result of these efforts, the lion-tailed tamarin is the only species of primate to have their conservation status improved from Critically Endangered to Endangered (Moraes et al., 2017).
‘Soft Release’ Training Sites and Free-Ranging, Captive Habitats for Lemurs
Duke Lemur Center
Perhaps one of the best-known captive facilities to maximize true environmental enrichment is the Duke Lemur Center (Durham, NC). Established at Duke University in 1966 (known then as the Field Station for Animal Behavior, having moved from New Haven, CT), its Director, Dr. Elwyn Simons, aimed to establish, “an effective second line of defense against extinction” (Wright, 2008; p. 287).
Today, the DLC has a reputation as a “living laboratory” for the “non-invasive study of rare primates” (Yapuncich et al., 2019). During the warmer months, many of its lemurs have access to roam the Duke Forest within gated mixed-species, Natural Habitat Enclosures. While still provisioned daily with fresh produce and primate chow, the lemurs feed on leaves, berries, and even insects within the forest. Since its founding, the DLC has recorded life history records for approximately 4,200 individual strepsirrhines (including lemurs and galagos; Zehr et al., 2014), with representatives from 13 species currently in residence.
St. Catherines Island
A private forested barrier island off the coast of Savannah, Georgia has been home to a population of zoo-born ring-tailed lemurs since 1985. This island was host to a unique ‘soft’ introduction between 1985 and 1986 when 12 ring-tailed lemurs from New York’s Bronx Zoo were released with the aim of ‘training’ them to re-establish ‘wild-type’ behaviors, while providing them with provisioned foods as a buffer.
Although these behaviors were not immediately apparent upon release, the lemurs eventually began to increase the time they spent traveling and foraging, and demonstrated the ability to reject naturally growing toxic plants (Keith-Lucas et al., 1999). The hope of this introduction was to study the groups’ ability to adapt to a new environment with the goal of one day, reintroducing future groups to Madagascar to restock wild populations (Coleman, 2007).
Many generations later, ring-tailed lemurs still reside on this island and have been the subjects of many research studies. At its height, 93 individuals lived on the island (Burgess, 2015). The population size has decreased, however, as many individuals have been sent to zoological parks with no new individuals being sent as replacements. Today, the island is home to approximately 30 lemurs.
In addition to feeding on the naturally occurring plants in the Duke Forest and on St. Catherines Island, the lemurs are exposed, to some degree, to predation-risks (e.g., birds of prey). Therefore, the lemurs receive both active and passive anti-predator training. These factors have made the DLC and St. Catherines Islands important sites of pre-release training.
Reintroduction of Captive Lemurs: A Test Case
Betampona Natural Reserve in Eastern Madagascar
In 1997, three male and two female captive-bred black-and-white ruffed lemurs (Varecia variegata) from the Duke Lemur Center were reintroduced into the Betampona Natural Reserve (Eastern Madagascar) in an effort to re-stock what was the current, dwindling population (then estimated at 35 individuals; Welch and Katz, 1992) with a fresh group of genetically distinct cohorts (Britt et al., 1998).
How were the animals selected?
The selection of individuals best suited for this extraordinary mission was arduous and included:
- Individuals from a well-represented founder line (part of the American Zoo and Aquarium Associations Species Survival Plan).
- Individuals who were old enough to act independently from their parents.
- Individuals who were raised (in captivity) by their parents (rather than hand-reared by zoo staff).
- Individuals deemed ‘behaviorally competent’.
- Individuals who had previously successfully reproduced or lacked any physical or medical reasons which would make reproduction difficult.
- Individuals who passed multiple, rigorous veterinary screenings.
What happened to the original lemurs?
The selected lemurs were flown to Madagascar (accompanied by a veterinarian), quarantined, and fitted with radio transmitter collars prior to their release in the forest (Britt et al., 2004a,b). They were provisioned with Monkey Chow (LabDiet® 5038 Monkey Diet) following their release as they adjusted to foraging the natural vegetation (Britt and Iambana, 2003). Following the release, a team of scientists monitored the lemurs to learn: how well they adapted to the forest, if they were feeding on the natural plants, and, what (specifically) they were feeding on. Unfortunately, and not wholly unexpectedly, a fossa (Crytoprocta ferox), a natural predator of lemurs, killed one of the females. The remaining lemurs seemed to adjust fairly well to their new habitat (Britt et al., 1998).
Were additional lemurs released at the same site?
Additional groups were released in 1998 (one male and three females from the Los Angeles Zoo; Los Angeles, CA and Hogle Zoo; Salt Lake City, Utah) and 2001 (three males and one female from the Santa Ana Zoo; Santa Ana, CA), having been given periods of pre-release training on St. Catherines Island and the Duke Lemur Center.
Ten of these 13 lemurs survived for more than a year. In 2003, it was reported that only five were still surviving – five had been lost to predation by fossa, one died of malnutrition, one disappeared from the Betampona Reserve, and one was withdrawn. However, this program was successful as one of the males successfully integrated into a wild group (and subsequently sired offspring) and one of the released females successfully reproduced with a wild male (Britt et al., 2004a,b).
Esteemed primatologist, Dr. Patricia Wright, describes this important conservation effort and the role of the Duke Lemur Center:
The outdoor habitat enclosures at the Duke Center played a most important role in these introductions, since the reintroduced lemurs, even those that did not come from Duke were all first given ‘boot camp’ training in ‘living wild’ in the center’s enclosures” (Wright, 2008; p. 303).
The efforts of this extraordinary project were brought to the world through a documentary called, “Operation Lemur: Madagascar” (In the Wild), narrated by the famous British comedian John Cleese as he joined the scientific team into Madagascar.
Was the Betampona Release a Success?
YES. Although a considerable amount of work (and expense) goes into preparing captive-born animals for reintroductions, the program itself goes beyond the individual. For many primate reintroduction programs, the need is dire to increase wild population numbers and, with this, genetic diversity. While many of the reintroduced black-and-white ruffed lemurs died, two of the 13-member cohort successfully reproduced and integrated with wild members of the Nature Reserve.
As described by one of the lead scientists, Dr. Adam Britt, and colleagues:
…not only can we expect the figures for overall survival to improve, but more importantly, the project has achieved its goal of reinforcing the existing wild populations through matings between the released animals and their wild conspecifics. It is felt that by anybody’s definition this can be regarded as a success” (Britt et al., 2004b; pp. 654-655).
Importantly, Dr. Britt and colleagues (2004b) outline many of the difficulties associated with the project, which future efforts would do well to address, including:
- Difficulties associated with finding suitable candidates.
- Very few soft release training sites.
- Knowing before release how the lemurs may behaviorally respond to the new environment.
- Awareness of the social organizations of the wild population prior to attempts integrate captive-born conspecifics.
- The significance of genotype in animal selection.
- How ‘success’ might be best assessed.
Should we try again?
While the captive environment offers food stability and safety to its animals, its positive welfare may have negative impacts on its animals’ ability to survive in their natural habitats. Nevertheless, such critical behaviors, including: foraging capabilities, awareness of predators, and success navigating through spatially complex substrates (like trees), can be taught to animals through enrichment training and introductions into naturalistic (though human-maintained) environments.
Flexibility in both feeding strategies and food sources could serve as important ecological buffers for endangered species (like ring-tailed lemurs), while conservation efforts in Madagascar and abroad are underway.
Could we try again?
Absolutely. An excellent species to try with would be the ring-tailed lemur – a species that spends a considerable amount of time on the ground, has feeding flexibility, and adapts well to many different habitats.
Do I think we should try again?
In my personal opinion… Absolutely. However, it will take a considerable amount of work. First and foremost, the support from and an equal collaboration with the Malagasy government, which, over the decades, has done a phenomenal job in establishing many protected forests for the country’s endemic species. Next, community-level scientific and conservation-based collaboration with those living adjacent to any proposed release sites, as consistent and long-term monitoring of the released animals is critical.
Following the recommendations outlined by Kleiman (1989) and Britt et al. (2004b), we (as a conservation-focused, scientific community) should:
- Expand areas of ‘soft release’ sites which best reflect the habitat types the reintroduced animal will encounter.
- Fully research the proposed release site, including: its size, carrying capacity, times and lengths of food shortage, distance from cropland or towns, other species living there that may compete with (or predate on) your released animals, and (crucially), how often poachers or illegal loggers are seen in the area.
- Implement environmental enrichment early on in zoos – hiding food to encourage foraging and promoting predator awareness (e.g., playing the sounds, providing the scents, or showing pictures of predators they may encounter). Exposure brings experience and experience promotes survival.
- Have a plan in place for who will monitor the animals and for how long.
- Expect that the offspring of the founding cohort of reintroduced animals (should they successfully reproduce) will fare better than their parents.And finally…
- Gather support. Conservation efforts are only successful when the wider public is involved. Everyone can help and everyone can cheer these animals on.
About the Author
Stephanie Canington is a Ph.D. Candidate in the Center for Functional Anatomy and Evolution at the Johns Hopkins University School of Medicine. She studies the evolution of zoo care, the natural history of primates, feeding ecologies of lemurs in wild and human-maintained habitats, and factors which may best predict success in animal reintroduction projects. Stephanie has conducted multi-year fieldwork on both St. Catherines Island and at the Duke Lemur Center.
Beck, B. B., Rapaport, L. G., Price, M. S., & Wilson, A. C. (1994). Reintroduction of captive-born animals. Pp. 265-286 In: Creative Conservation. Springer, Dordrecht.
Britt, A. (2000). Diet and feeding behaviour of the black-and-white ruffed lemur (Varecia variegata variegata) in the Betampona Reserve, eastern Madagascar. Folia Primatologica, 71(3), 133-141.
Britt, A., & Iambana, B. R. (2003). Can captive-bred Varecia variegata variegata adapt to a natural diet on release to the wild? International Journal of Primatology, 24:987-1005.
Britt, A., Welch, C., & Katz, A. (1998). The first release of captive-bred lemurs into their natural habitat. Lemur News, 3:8-11.
Britt, A., Welch, C., & Katz, A. (2004a). Can small, isolated primate populations be effectively reinforced through the release of individuals from a captive population? Biological Conservation, 115:319-327.
Britt, A., Welch, C., Katz, A., Iambana, B., Porton, I., Junge, R., … & Haring, D. (2004b). The re-stocking of captive-bred ruffed lemurs (Varecia variegata variegata) into the Betampona Reserve, Madagascar: methodology and recommendations. Biodiversity & Conservation, 13(3), 635-657.
Burgess, T. (2015). Female Social Rank and Steroid Production in Semi-Free Ranging Lemur Catta on St. Catherines Island, Georgia. Unpublished Masters Thesis.
Cheyne, S. M. (2009). The role of reintroduction in gibbon conservation: opportunities and challenges. The Gibbons, 477-496.
Coleman, L. B. (2007). An Evaluation of the Natural and Provisioned Feeding Rates of Semi-Free Ranging Ringtailed Lemurs (Lemur catta) on St. Catherines Island, GA. Unpublished Masters Thesis.
Gould, L., & Gabriel, D. N. (2015). Wet and dry season diets of the Endangered Lemur catta (ring‐tailed lemur) in two mountainous rocky outcrop forest fragments in south‐central Madagascar. African Journal of Ecology, 53:320–330.
Keith-Lucas T, White FJ, Keith-Lucas L, Vick LG. (1999). Changes in behavior in free‐ranging Lemur catta following release in a natural habitat. American Journal of Primatology, 47:15-28.
Kleiman, D. G. (1989). Reintroduction of captive mammals for conservation. BioScience, 39(3), 152-161.
Kleiman, D. G., Beck, B. B., Dietz, J. M., Dietz, L. A., Ballou, J. D., & Coimbra-Filho, A. F. (1986). Conservation program for the golden lion tamarin: captive research and management, ecological studies, educational strategies, and reintroduction. In Primates (pp. 959-979). Springer, New York, NY.
Moraes, A. M., Ruiz-Miranda, C. R., Ribeiro, M. C., Grativol, A. D., Carvalho, C. D. S., Dietz, J. M., … & Galetti, P. M. (2017). Temporal genetic dynamics of reintroduced and translocated populations of the endangered golden lion tamarin (Leontopithecus rosalia). Conservation Genetics, 18(5), 995-1009.
Shepherdson, D. (1994). The role of environmental enrichment in the captive breeding and reintroduction of endangered species. In Creative conservation (pp. 167-177). Springer, Dordrecht.
Souza-Alves, J. P., Chagas, R. R., Santana, M. M., Boyle, S. A., & Bezerra, B. M. (2021). Food availability, plant diversity, and vegetation structure drive behavioral and ecological variation in Endangered Coimbra-Filho’s titi monkeys. American Journal of Primatology, 83:e23237.
Steenweg, R., Hebblewhite, M., Gummer, D., Low, B., & Hunt, B. (2016). Assessing potential habitat and carrying capacity for reintroduction of plains bison (Bison bison bison) in Banff National Park. PloS one, 11:e0150065.
Stoinski, T. S., Beck, B. B., Bloomsmith, M. A., & Maple, T. L. (2003). A behavioral comparison of captive-born, reintroduced golden lion tamarins and their wild-born offspring. Behaviour, 137-160.
Strum, S. C., & Southwick, C. H. (1986). Translocation of primates. In Primates (pp. 949-957). Springer, New York, NY.
Vickery, S. S., & Mason, G. J. (2003). Behavioral persistence in captive bears: implications for reintroduction. Ursus, 35-43.
Viggers, K. L., Lindenmayer, D. B., & Spratt, D. M. (1993). The importance of disease in reintroduction programmes. Wildlife Research, 20(5), 687-698.
Welch, C., & Katz, A. (1992). Survey and census work on lemurs in the natural reserve of Betampona in eastern Madagascar with a view to restocking. Dodo, 28:45-58.
Wright, P. C. (2008). Decades of Lemur Research and Conservation. In Elwyn Simons: A Search for Origins (pp. 283-310). Springer, New York, NY.
Yapuncich, G. S., Kemp, A. D., Griffith, D. M., Gladman, J. T., Ehmke, E., & Boyer, D. M. (2019). A digital collection of rare and endangered lemurs and other primates from the Duke Lemur Center. PloS one, 14:e0219411.
Zehr, S. M., Roach, R. G., Haring, D., Taylor, J., Cameron, F. H., & Yoder, A. D. (2014). Life history profiles for 27 strepsirrhine primate taxa generated using captive data from the Duke Lemur Center. Scientific Data, 1:1-11.