Ploughshare Tortoise in Northwestern Madagascar

A ploughshare tortoise. Photo by Durrell Wildlife Conservation Trust

The ploughshare tortoise (Astrochelys yniphora) is also known as the angonoka tortoise, the Madagascar tortoise, or the Madagascar angulated tortoise. This tortoise is endemic to the dry tropical forests of Northwestern Madagascar, particularly around Baie de Baly (Baly Bay) National Park. The distribution for these tortoises is very small; they inhabit approximately a 25 to 60 km2 range and have five discontinuous subpopulations scattered around the bay area (Leuteritz and Pedrono 2020). The IUCN Red List classifies these reptiles as critically endangered; approximately only 440-700 individuals exist in the wild (Leuteritz and Pedrono 2020). Because of this, the ploughshare tortoise is often declared to be the world’s rarest tortoise (Mandimbihasina et al. 2019). The ploughshare tortoise is on the brink of extinction in the wild for two main reasons: habitat conversion and the illegal pet trade market.

1. How Habitat Conversion Affects the Ploughshare Tortoise

Madagascar is home to some of the most endangered ecosystems in the world. It has been estimated that the country has lost more than 80% of its forest; around half of them have been lost since the late 1950s (Butler 2000). Madagascar is an extremely impoverished nation that relies heavily on the agricultural productivity. Because of this, dry forests in Madagascar are often converted into agricultural and pastoral lands.

A major threat to the ploughshare tortoise is the burning of dry forests for them to be converted to agricultural and pastoral lands. This causes their food supply of bamboo scrub, forbs, shrubs, and herbs to decrease, forcing the tortoise go extra lengths to find food (Mandimbihasina et al. 2019). Additionally, these fires can often cause damages to the tortoise, even causing fatalities in the already small populations.

Historical and current ranges of the ploughshare tortoise. Figure by Durrell Wildlife Conservation Trust

A common trade route among poachers is NW Madagascar → Nairobi → Bangkok. Photo by Turtle Conservancy.

2. How the Illegal Pet Trade Affects the Ploughshare Tortoise

Like many other endangered species worldwide, the ploughshare tortoise is a target for illicit trading. According to Mandimbihasina et al. (2018), the ploughshare tortoise was historically exploited for food and its shell to be used as an instrument. However, demand has shifted to exploitation as a pet. Despite the tortoise being protected under Malagasy law since the 1960s, the demand for the ploughshare tortoise has skyrocketed, especially since then (Mandimbihasina et al. 2018).

The price of the tortoise on the black-market ranges from USD 45,000 to USD 50,000 (Mandimbihasina et al. 2018). Unfortunately, the exploitation of the ploughshare tortoise is exacerbated by extreme poverty and droughts that have

reduced agricultural productivity (Schwarz et al. 2017). The extremely high prices of a ploughshare tortoise, even a small juvenile, has led local people hunting them from wild areas and even protected areas and selling them to buy rice and corn to feed their families (Schwarz et al. 2017). Additionally, the protections on the tortoise are not always enforced because of corruption, lack of resources, and officers’ lack of motivation to enforce regulations.

3. Current Conservation Efforts

The conservation efforts to protect the ploughshare tortoise relies on scientific investigations, local communities’ involvements, or a mix of the two. A common effort used to help improve the numbers of endangered reptiles is the use of captive breeding. However, all captive breeding programs have not had the same success. Studies have been done to understand the ecophysiological responses of tortoise reproduction and to find out how diverse the genetics of the remaining tortoises are.

A. Ecophysiological Responses of Tortoise Reproduction

Due to their rarity, little is known about the ploughshare tortoise’s reproductive physiological changes. Currylow et al. (2017) aimed to:

Characterize baseline and season patterns of stress and reproductive hormones
Understand if they related to body condition and activities
Understand if captivity affects stress, reproduction, and body condition
Find out which environmental factors influence herpetofauna health and behaviors in captive breeding management.

The researchers obtained samples from wild tortoises and tortoises in captive breeding programs from northwestern Madagascar and western United States (California) from 2013-2015. They did monthly sampling of 79 tortoises in the Durrell Wildlife Conservation Trust captive breeding program in Madagascar, 12 tortoises in the Turtle Conservancy in California, and 54 tortoises that were found in the wild. They divided the tortoises by adult females, adult males, and subadults. Due to the small population size in the US, the researchers did not include the population in most statistical comparisons, but they included them in the mean values and any visual graphs for comparisons.

Figure 1: Hormone concentrations in male Astrochelys yniphora populations. Figure by Currylow et al. (2017).

In the male populations, the researchers found no significant difference in corticosterone (CORT) concentrations; however, CORT levels were higher in tortoises in the captive Malagasy program in December. Additionally, the male Malagasy captive individuals exhibited higher basal CORT levels when they sired nests when compared to males who have not sired nests (Currylow et al. 2017). Testosterone (T) levels varied between months and populations (Currylow et al. 2017). Males in the US captive program exhibited higher T levels than all other populations (Currylow et al. 2017).

In the female populations, the researchers found the US captive females had significantly higher and more variable monthly CORT concentrations than Malagasy captive females (Currylow et al. 2017). Estradiol (E2) levels in Malagasy captive females had lower E2 levels than wild females and the US captive females (Currylow et al. 2017). Lastly, progesterone (P) concentrations showed to be similar as well; Malagasy captive females showed lower P averages than both US captive females and wild females (Currylow et al. 2017).

Figure 2: Hormone concentrations in female Astrochelys yniphora populations. Figure by Currylow et al. (2017).

Environmental conditions that regulate the ploughshare tortoises’ activities are temperature, humidity, and cover (Currylow et al. 2017). Wild females were able to find warmer locations in vegetation in December than in wild males, who were often resting in the open (Currylow et al. 2017). Humidity was less differentiated but wild tortoises selected more warmer temperatures than those in captivity (Currylow et al. 2017). Parturition over the last 15 years has shifted earlier in the year, meaning that climate change may shift reproductive timing. When comparing the US captive tortoises and the Malagasy captive tortoises, the Malagasy captive tortoises are the only program that has had reproductive success. Researchers believe the change in hemispheres, dramatic climate differences, and the lack of other adult males could be the reason why the US captive tortoises have not reached reproductive success (Currylow et al. 2017).

Figure 3: The four locations where samples were collected were Cap Sada, Beheta, Betainalika, and the Western Complex
(Ambatomainty, Andrafiafaly, and Andranolava). Figure from Mandimbihasina et al. (2019)

B. Genetic Diversity in Remaining Populations

The intense harvesting of the ploughshare tortoise for the illicit pet trade can have serious consequences on the genetic diversity of the tortoise. However, the effects of the illegal trading have not been well understood yet. The study done by Mandimbihasina et al. (2019) aims to find there has been a decrease in genetic diversity among the fragmented tortoise populations. The researchers collected samples from 183 unique individuals from four different localities. To find out whether the long-term exploitation of the ploughshare tortoise has resulted in a decrease in genetic diversity; genomic DNA was used (Mandimbihasina et al. 2019). With this data, captive breeding programs can have a better attempt at maximizing the genetic diversity in their programs

In their test for mitochondrial DNA, the researchers found significant genetic variation among the different subpopulations (ΦST = 0.17238, p < 0.001) but most of the variation was within the subpopulations themselves, at 83.3% (Mandimbihasina et al. 2019). Researchers recovered nine haplotypes with a nucleotide diversity of π = 0.01097 (Mandimbihasina et al. 2019). Figure 4 shows the results of a Bayesian analysis of the haplotypes. Genetic diversity was calculated for all four sites but there was no statistical difference between H0, He, and Hf between the whole dataset and subsets. The greatest amount of diversity was found in the Western Complex, with He= 0.758 and Rt= 7.6 (Mandimbihasina et al. 2019). However, the Western Complex also had the highest inbreeding coefficient at FIS= 0.137, demonstrating a possible Wahlund effect (Mandimbihasina et al. 2019). The presence of a genetic bottle neck was not shown when all the subpopulations were combined nor when separated by locality (Mandimbihasina et al. 2019).

Because of the historical exploitation of the ploughshare tortoise, researchers thought that there would be a decrease in genetic diversity; however, He levels appeared to be normal, ranging from 0.612 to 0.758 (Mandimbihasina et al. 2019). These numbers are similar to other threatened or endangered tortoises. For the subpopulations, allelic richness (Rt) was 4.846 to 10.131. However, despite the normal He levels, the Western Complex seems to be losing alleles, as it has the highest FIS value (Mandimbihasina et al. 2019). However, delayed age of reproduction, habitat loss, and juvenile loss could lead to further loss of alleles.

Figure 4: Bayesian tree from mitochondrial D-loop analysis. Figure from Mandimbihasina et al. (2019).

C. Policy Based Conservation and Local Involvement

The ploughshare tortoise is protected under Malagasy law. Baly Bay, the area that it habituates, was declared as a national park in 1997, bringing along several protections against habitat degradation. Patrols are now stationed at the national park and actively search for any signs of poachers, bush fires, and invasive pests. Researchers and organizations invested in the endangered tortoises in Madagascar are currently petitioning for better intelligence between Malagasy, Malaysian, and Thai conservation agencies (Schwarz et al. 2017). In addition, they ask for an increase in penalties for illegal trading, establishing checkpoints between Malaysia and Thailand, and species-identification programs for law enforcement (Schwarz et al. 2017).

Patrols guarding an area with ploughshare tortoises. Photo by Turtle Conservancy.

Additionally, NGOs have had successes in getting local communities to be involve in conservation efforts. The Durrell Wildlife Conservation Trust established their captive breeding program in 1987 and has had local communities’ involvement through employment, education, and special programs (Durrell Wildlife Conservation Trust 2020). Located in Ampijoroa, Madagascar, the captive breeding center is the first in the world to have success in breeding and releasing tortoises in the wild (Durrell Wildlife Conservation Trust 2020). The Durrell Wildlife Conservation Trust employs anti-poaching patrols around key sites to deter potential poachers (Durrell Wildlife Conservation Trust 2020). Local school children learn about the importance of conserving the ploughshare tortoise and participate in tortoise releasing events as well (Durrell Wildlife Conservation Trust 2020). To identify tortoises that were bred and raised in captivity, conservation groups decided to mark tortoise shells with numbers (Sierra Club 2018). With this in mind, it has the potential to deter potential black-market buyers and help law enforcement identify which tortoises were illegally extracted from captive breeding sites and from the Baly Bay National Park.

Local communties advocate for ploughshare tortoise protection. Photo by Durrell Wildlife Conservation Trust

Staff member marking a tortoise shell for identification. Photo by Durrell Wildlife Conservation Trust.

All in all, conservation methods for the ploughshare tortoise are complex and quite frankly, can be difficult to implement. The Malagasy government must strictly enforce anti-habitat degradation laws and enforce anti-poaching measures. Continued long-term management of their natural habitat and tortoises is essential for increasing their numbers. Organizations must keep genetic diversity and physiological responses in mind when establishing captive breeding programs. Lastly, community involvement is often the key to preventing poaching efforts as well. With all factors in mind, there is hope for the ploughshare tortoise.

Citations:

Butler, R. 2000, June 9. Forests in Madagascar. https://rainforests.mongabay.com/20madagascar.htm.

Currylow, A. F. T., A. Mandimbihasina, P. Gibbons, E. Bekarany, C. B. Stanford, E. E. Louis, and D. E. Crocker. 2017. Comparative ecophysiology of a critically endangered (CR) ectotherm: Implications for conservation management. PLOS ONE. 1-29. https://doi.org/10.1371/journal.pone.0182004

Durrell Wildlife Conservation Trust. 2020. Ploughshare tortoise. https://www.durrell.org/wildlife/species-index/ploughshare-tortoise/.

Leuteritz, T., and M. Pedrono. 2020. IUCN Red List of Threatened Species: Astrochelys yniphora. https://www.iucnredlist.org/species/9016/12950950.

Mandimbihasina, A. R., C. L. Frasier, R. A. Hagenson, B. A. D. Robertson, S. E. Engberg, R. E. Lewis, L. G. Woolaver, E. Razafimahatratra, L. L. Rabetafika, and E. E. Louis. 2019. Conservation genetics of Madagascar’s critically endangered ploughshare tortoise (Astrochelys yniphora). Conservation Genetics 21:109–121. https://doi.org/10.1007/s10592-019-01236-7

Mandimbihasina, A. R., L. G. Woolaver, L. E. Concannon, E. J. Milner-Gulland, R. E. Lewis, A. M. R. Terry, N. Filazaha, L. L. Rabetafika, and R. P. Young. 2018. The illegal pet trade is driving Madagascar’s ploughshare tortoise to extinction. Oryx 54:188–196. https://doi.org/10.1017/S0030605317001880

Schwarz, D., D. Newton, and C. Ratzimbazafy. 2017. Assessment of the international illicit wildlife trade in the critically endangered Malagasy tortoise species Astrochelys yniphora and Astrochelys radiata. SALAMANDRA 53:163–166. http://www.salamandra-journal.com/index.php/home/contents/2017-vol-53/1818-schwarz-d-d-newton-c-ratzimbazafy/file

Sierra Club. 2018, August 20. Please (Don’t) Take a Number. https://www.sierraclub.org/sierra/2018-4-september-october/opening-photo/please-dont-take-number.