Dietary Requirements of Asian turtles


Zoo animal nutrition is a work field that still is largely unexplored. In recent years more and more is being discovered but very much still is to be researched. Research on nutrition of reptiles is a part that seems to be even less explored.

Diets fed to captive reptiles often are based solely on experience of keepers and hardly ever on facts about nutritional requirements of the animals in question. Many captive reptiles live lives that are significantly shorter than their life expectancy and nutrition related diseases are not uncommon.

Early 2002 thousands of Asian turtles of several different species, destined for a food market in Hong Kong were impounded. Several European and North American Zoos were asked to take in animals from this impoundment. Because the species concerned are relatively unknown their captive husbandry was also hardly explored.

The European Zoo Nutrition Centre (EZNC) was asked to include a dietary advice for the five species Cuora amboinensis, Heosemys grandis, Heosemys spinosa, Orlitia borneensis and Siebenrockiella crassicollis as very little was known about their captive maintenance. Due to time pressure this advice was conducted in a very short time. After several months the need rose for a more detailed and practical advice. To come to this advice a study is done by two students Animal Management (B.Sc. Course) at the Van Hall Institute, Leeuwarden, and The Netherlands. Due to limited time and the diversity of the turtle species mentioned before this study focuses only on the nutritional requirements of the two species said to be primarily herbivorous; Cuora amboinensis and Heosemys spinosa (Ernst & Barbour, 1989, Mertens, 1971). Data on the other three species and the way in which nutritional recommendations are accepted in zoos will be analysed in further studies.

This study will include a comparison between the nutritional values of the in-situ diet of Cuora amboinensis and Heosemys spinosa conducted from literature, and the nutritional ex-situ values conducted from questionnaires and literature.

We hope that this report will aid in a better insight in the nutritional requirements of Cuora amboinensis and Heosemys spinosa and give a nutritional advice that is practically applicable in the captive management of these species.

Martine Helmink
Siebren Kuperus
Leeuwarden, August 2002


In December 2001 several thousand Asian turtles were confiscated, all of these animals were destined for a food market in Hong Kong. In January 2002 a part of these animals was sent to Europe to be housed at zoos and private keepers and participate in captive breeding programs. At distribution of these animals the European Zoo Nutrition Centre (EZNC) gave an advice about the nutrition of the five most common species in the shipment; Cuora amboinensis, Heosemys grandis, Heosemys spinosa, Orlitia borneensis and iebenrockiella crassicollis. Because time was limited the advice given could not be as thoroughly researched as wishful. In contact with the Van Hall Institute in Leeuwarden it was decided to have the dietary requirements of these turtles further researched by Animal Management students in a final thesis project.

Because of time limitations only the two species known in literature as herbivorous have been included in this report; the Malayan box turtle (Cuora amboinensis) and the Spiny turtle (Heosemys spinosa). Remaining species will be further researched in other projects led by EZNC. During the five months in which the project took place data was gathered on in-situ nutrition by means of a literature study. Found data was compared to the composition of diets fed by zoos and private keepers obtained by means of a questionnaire. With the comparison the base is made for an advice about captive feeding of the animals.

Reported nutrition of Cuora amboinensis shows average diets to be largely omnivorous in captivity, in some cases the part of the diet consisting of animal matter reaches nearly 100%, with no apparent ill effects. Because of reproductive success and successful long term maintenance observed in animals fed omnivorous diets it is carefully concluded that Cuora amboinensis is in fact highly omnivorous by nature, or for some reason highly tolerant to large amounts of animal matter in its diet. Reported nutrition of Heosemys spinosa in captivity closely meets the nutritional requirements found for herbivorous tortoises. Captive Heosemys spinosa are fed diets consisting largely of fruits. The preference for fruits possibly reflects the natural diet because the species by nature is a forest inhabitant. Seeds found in wild caught Heosemys spinosa back up this theory.
Supplements are used by most keepers, in several reported diets the amount of supplements fed could easily result in over dosage of several minerals and vitamins, some of which are known to be toxic when given in high amounts.
Energy intake calculated from reported diets generally is very low. According to questionnaire results Cuora amboinensis consume roughly 0,25 MJ GE per kg bodyweight per week. Literature values report the ME of inactive reptiles to be nearly twice as high. Heosemys spinosa shows an intake of roughly 0,65 MJ GE per kg bodyweight per week. This intake closely meets literature on energy demands. However, no indications have been found about the part of Gross Energy that can be utilised for Metabolic Energy requirements in turtles, or reptiles in general.

Diet recommendations are given based on findings in the report and consist primarily of most commonly fed food items. Some advice is given on feeding frequency and way of presenting the diet. Selective feeding should be prevented to make sure nutritional quality of the food consumed meets the animal’s requirements.


This research project was mainly supported by EZNC and the Van Hall Institute, which are both situated in the Netherlands. Therefore we like to thank Dr. Ir. W.L. Jansen, and J. Nijboer BSc from EZNC and T.R. Huisman BSc and B.B.H. van Wijk BSc MSc from the Van Hall Institute for their advice and general support. Thanks to Ms. S.Y. Colenbrander and Ms. F.A.J. van Vliet for their general support throughout the process.

Special thanks go out to the following persons for the great amount of work and effort contributing to this project:

P.P. van Dijk TRAFFIC Southeast Asia
M. Kerlen ESF Studbook keeper Cuora amboinensis
H. Zwartepoorte Reptile curator Rotterdam Zoo, President NSV and ESF

And the following institutions and private keepers for returning the questionnaire:

Bristol Zoo Gardens Cliffton United Kingdom
Brno Zoo Brno Czech Republic
Chester Zoo Upton by Chester United Kingdom
Lodz Zoo Lodz Poland
Moscow Zoo Moscow Russia
Perth Zoo South Perth Australia
Rotterdam Zoo Rotterdam The Netherlands
Zoo de Lisboa Lisboa Portugal
Zoologischer Garten Halle Halle Germany

M. Kerlen ESF studbook The Netherlands
R. Luybaert ESF studbook The Netherlands
G. Pol ESF studbook The Netherlands
T. Storcken ESF studbook The Netherlands
J. Stumpel ESF studbook The Netherlands
H. van der Voorde ESF studbook The Netherlands

This report could not have been completed without the help of each of the above.

Martine Helmink
Siebren Kuperus

List of abbreviations and symbols



Calcium : Phosphorus ratio.

The Convention on International Trade in Endangered Species of wild flora and fauna.

Dry matter.

European Association of Zoos and Aquaria.

European Studbook Foundation.

European Zoo Nutrition Centre.

Gross Energy.

The world conservation union.

Metabolic Bone Disease.

‘Nederlandse Schildpadden Vereniging’ (Dutch Turtle/Tortoise Society).


Ulcerative Shell Disease. Most commonly referred to as ‘shell disease’.


On December 11h 2001 in China a large number of turtles was confiscated. These animals were destined for a market in Hong Kong where the approximately 10.000 individuals were to be sold for human consumption. Most of these animals belonged to the species Cuora amboinensis, Heosemys grandis, Heosemys spinosa, Orlitia borneensis and Siebenrockiella crassicollis. The animals were all taken from their wild habitat in the Indonesian region, they could not be placed back into the wild and were therefore placed in a Hong Kong animal rescue centre to await their further destiny. The international Turtle Survival Alliance requested the European Association of Zoos and Aquaria (EAZA) office to look for permanent housing for at least a part of the confiscated animals.

The curator of reptiles at Rotterdam Zoo, president of the Dutch turtle/tortoise society (NSV) and president of the European Studbook Foundation (ESF) Mr. Henk Zwartepoorte is one of the initiators of the impoundment and still largely involved with the well being of the animals.

On January 9th 2002 two representatives of Rotterdam Zoo, Holland; Mr. Zwartepoorte and veterinarian Mr. Schaftenaar travelled to Hong Kong to assess the health of the animals and select specimens fit enough to travel to Europe. About 1000 turtles were transported to Amsterdam airport on the 17th of January and in Holland they were checked over and if needed, treated for health problems before they were further distributed amongst European zoos and private studbook members (EAZA. 28-03-2002; pers. comm. H. Zwartepoorte).

The main focus of this study is on Cuora amboinensis and Heosemys spinosa. Since a lot of zoos had no experience in keeping these species, EZNC (the European Zoo Nutrition Centre) was asked to give a practical advice on how and what to feed the animals.
EZNC is a department of EAZA and was founded by Dr.Ir. W.L. Jansen, (Jagran BV), and J. Nijboer, BSc (Rotterdam Zoo). The primary targets of EZNC and other relevant information about the organisation is given in Appendix I.

A preliminary advice was given by EZNC to accompany the animals when they were distributed through Europe (see Appendix II). Some months after this advice was given out, in March 2002 the time had come to review the given advice and to thoroughly study the subject so that a practical and definite advice could be given. Apart from this there is also a need to know what participating zoos do with nutritional recommendations such as given at the distribution of these turtles. This study is performed to answer these questions and took place between March and September 2002.

The main goal of this study is to give a nutritional advice that meets the nutritional requirements of Cuora amboinensis and Heosemys spinosa as close as possible and that will be practically applicable in an ex-situ situation.
In order to achieve this main goal this study will aim to answer the following main research question, further specified by the following sub-questions.

What diet composition in terms of nutrients and ingredients is best applicable in captive management of the species Cuora amboinensis and Heosemys spinosa?
  • What is the composition of the in-situ diet of Cuora amboinensis and Heosemys spinosa in regards to ingredients and nutrients and how can the nutritional value of this diet be reproduced in an ex-situ situation?
  • What is the most successful ex-situ diet that is currently fed?
In order to give a nutritional advice it is necessary to know the nutritional requirements of the turtle species studied as accurate as possible. To gain insight in the natural diet composition and feeding behaviour the following question and sub-questions need to be answered:
  1. What is known about in-situ living >i>Cuora amboinensis and Heosemys spinosa?
  • What is the natural habitat of Cuora amboinensis and Heosemys spinosa?
  • What is known about the digestive system of Cuora amboinensis and Heosemys spinosa?
  • What is known about the natural diet and feeding behaviour of Cuora amboinensis and Heosemys spinosa?
To gain insight in the current situation of ex-situ nutrition in these species the following question and sub-questions are answered:
  1. What is known about the way in which Cuora amboinensis and Heosemys spinosa are kept ex-situ?
  • What is the composition and nutritional value of the diets currently fed to Cuora amboinensis and in captivity?
  • Which diets are fed at institutions that have a good reproduction success?
  • What nutrition related diseases and deficiencies occur amongst Cuora amboinensis and Heosemys spinosa in captivity?

Description of <i>Cuora amboinensis</i> and <i>Heosemys spinosa</i>

This chapter describes the taxonomical position of the species Cuora amboinensis and Heosemys spinosa. For both species a description of their natural habitat and distribution is included. An indication is given on the current number existing in the wild and their conservation status.
This paragraph aims to answer the fist two parts of sub-question one:
  • What is the natural habitat of Cuora amboinensis and Heosemys spinosa?
  • What is known about the digestive system of Cuora amboinensis and Heosemys spinosa?

<i>Cuora amboinensis</i> Taxonomy and description

The taxonomical position of Cuora amboinensis is one that is argued about. It is placed in the family of Emydidae by some (Dijk, pers. comm.), whereas others place it in the Family of Bataguridae. In recent times it is most commonly accepted to belong to the family of Bataguridae (Dijk, pers. comm.) therefore this is the position we accept in this report. Table 1.1. describes the place of Cuora amboinensis in the animal kingdom.

Table 1.1 Taxonomy of Cuora amboinensis (Daudin, 1802).

(Colijn, 20-04-2001; Dijk, 2002)

Adult Cuora amboinensis attain a length of up to 20 cm with a high arched carapace (Ernst & Barbour, 1989). While researching more than 200 preserved specimens, Rummler and Fritz (1991) found the largest specimen to measure 217,5 mm (Rummler & Fritz, 1991). The carapace is uniformly dark brown to black, the plastron is yellow to light brown (Ernst & Barbour, 1989).

The species is described to occur from the Nicabar Islands, Bangladesh and Assam south through Burma, Thailand, Kampuchea, Vietnam, and Malaya, and east in Indonesia to Sulawesi and Ambinia. It also reaches the Philippines and Celebes (Ernst & Barbour, 1989).
Figure 1.2 shows the distribution of Cuora amboinensis and each of its subspecies.

Currently three subspecies are described:

Cuora amboinensis amboinensis (Daudin, 1802), (Terra typica: Island of Ambon, Moluccas)
The nominate form occurs on the Philippines, Mollucas, and Sulawesi. It is characterised by a flat, broad carapace with a distinct margin, and a plastral pattern with larger dark blotches than in the other subspecies. The carapace ratios for the subspecies C. a. amboinensis are shown in table 1.2 (Rummler & Fritz, 1991).

The populations of the Philippine Islands differ from other C. a. amboinensis through extremely narrow light head stripes, more extensive dark plastral blotches and different most common plastral formulae (Rummler & Fritz, 1991).

Cuora amboinensis kamaroma (Terra typica: 50 km north of Bangkok, Thailand)
This subspecies lives on the South-East-Asian continent and Borneo. It has a highly domed and narrower carapace than the other subspecies without a well-developed margin. The carapace ratio for the subspecies C. a. kamaroma is shown in table 1.2 (Rummler & Fritz, 1991).

Cuora amboinensis couro (Schweigger, 1812), (Terra typica: Java)
This subspecies occurs on Sumatra and Java. This subspecies is though to be derived from a former intergrade population between C.a. amboinensis and C.a. kamaroma having intermediate characteristics. The shell is of intermediate shape with or without an indistinct margin. The carapace ratio for the subspecies C. a. couro is shown in table 1.2 (Rummler & Fritz, 1991).

Table 1.2 Carapace ratio of Cuora amboinensis amboinensis, Cuora amboinensis kamaroma and Cuora amboinensis couro.

(Rummler & Fritz, 1991).
Table 1.2 indicates physiological differences between the three subspecies. The numbers above suggest the shape of the animals of each subspecies, especially the matter in which the carapace is domed. This difference in carapace shape is thoroughly described in an article by Filella (2000). A personal view of the authors is that the matter in which a carapace is domed could give an indication about the niche each subspecies fills. A more domed carapace limits the speed of a swimming individual but is stronger in withstanding predators or trampling hoofs of land animals. As a result of this the shape of the carapace could indicate the in-situ lifestyle of its bearer, possibly also indicating differences in diet.

<i>Cuora amboinensis</i> Habitat

Cuora amboinensis is a semi-aquatic turtle that inhabits lowland water bodies with soft bottoms and slow current, such as marshes, swamps, ponds, pools, streams and manmade flooded rice paddies. Although highly aquatic it is often found far from water. Ernst and Barbour (1989) refer to an article by Taylor (1920) stating that juveniles are entirely aquatic (Ernst & Barbour, 1989).

<i>Cuora amboinensis</i> Status

In 2000 this species was listed vulnerable on the Red List (Asian Turtle Trade Working Group) it was listed a CITES Appendix II species 19/07/00. Despite this, large numbers were still exported from Indonesia (18,000) and Malaysia (50,000) in 2001 (CITES, 01-04-2002)
Vietnam exported a total of 13440 animals between 1994 and 1999. Animals exported within the Asian region are most likely to be destined for consumption. Animals exported to America and Europe are often sold as pets (Dijk, Stuart & Rhodin, 2000).

<i>Heosemys spinosa</i> Taxonomy and description

The species Heosemys spinosa is placed in the family Emydidae, this position seems to be commonly accepted, in contrast to that of Cuora amboinensis.
Table 1.3. describes the place of Heosemys spinosa in the animal kingdom.

Table 1.3 Taxonomy of Heosemys spinosa (Gray, 1831).

(Sellmann, 01-01-1999).

This species can attain a carapace length of up to 22 cm (Ernst and Barbour, 1989). Herman (1993) describes two approximately 19-year-old specimens that both measured 203 mm, which is confirm with the mentioned maximum (Herman, 1993). The plastron of young animals is marked with a distinct ‘ray-pattern’, this is most distinct in half grown animals that are 12-15 cm in length and disappears with older age leaving a uniform blackish brown colour in fully grown animals (Mertens, 1971). On the outside of the carapace this species has spiny edges. In adult animals spines become less distinct and often disappear due to growth and wearing down, making them much smoother than juveniles. This species ranges from Tenasserim, Burma and southern Thailand southward through Malaysia to Sumatra and Borneo (Ernst and Barbour, 1989). Figure 1.4 shows the distribution of Heosemys spinosa.

No subspecies have been recognised in the species Heosemys spinosa, although great morphological differences seem to occur (Kerlen, pers. comm.). A carapace ratio for this species does not seem to be available.

<i>Heosemys spinosa</i> Habitat

Herman (1993) mentions this species lives primarily in rainforest streams at altitudes of 170 up to 1000 m, it is thought to be mostly diurnal and sluggish. This species is often reported to be both aquatic and terrestrial (Herman, 1993). Mertens (1971) quotes an article by MÒller (1906) stating that young animals are aquatic and adults terrestrial (Mertens, 1971).

<i>Heosemys spinosa</i> Status

In 2000 this species was listed Vulnerable on the Red List of IUCN. Despite high demand on the food market the number of animals traded in Indonesia has declined by 50% over a very short period of time, indicating rapid decline of the natural population. Its high demand in the food market, its scattered small populations and a low reproductive output are reason for a proposed endangered status (Dijk, Stuart & Rhodin, 2000). Information on capture- or export numbers is not available, this species does not appear in CITES legislation and therefore is not protected by international law, no numbers are available on capture or export. (CITES, 01-04-2002).


This chapter contains the methods that were used during this study. Why methods were chosen and the way they were applied on the matter researched. First a selection is made about the subjects researched. This selection is followed by an explanation about the way in which each research question will be studied. Finally the various groups of participants are differentiated.


In this study data about the captive management two confiscated Asian turtle species were collected:
Cuora amboinensis; Malaysian Box Turtle
Heosemys spinosa; Spiny Turtle

A study was done to find the nutritional requirements of these two species, making it possible to give a nutritional advice for their captive management. The two species have been selected from the entire group of species because of expected dietary similarity. In literature both are said to be primarily herbivorous (Ernst & Barbour, 1989; Mertens, 1971). A literature review was carried out to compare in-situ data with collected ex-situ data about these species.


In order to give an advice about the nutritional requirements and the correct diet of Cuora amboinensis and Heosemys spinosa several questions needed to be answered. This paragraph describes the process used to answer these questions.
  • What is the natural habitat of Cuora amboinensis and Heosemys spinosa?
  • What is known about the digestive system of Cuora amboinensis and Heosemys spinosa?
  • What is known about the natural diet of Cuora amboinensis and Heosemys spinosa?
These questions were answered by a literature review and by contacting herpetological specialists. A part of the literature review was conducted at the library of the natural historic museum 'Naturalis'. Throughout the review references were found in books, articles and on the Internet. Relevant publications were ordered through the library of the Van Hall Instituut and processed in different parts of the report.

To gain insight in the captive diets of Cuora amboinensis and Heosemys spinosa the following questions were composed:
  • What is the composition and nutritional value of the diets currently fed to Cuora amboinensis and Heosemys spinosa in captivity?
  • Which diets are fed at institutions that have a good reproduction success?
  • What nutrition related diseases and deficiencies occur amongst Cuora amboinensis and Heosemys spinosa in captivity?
These questions were answered using data gathered by a questionnaire. The set-up of this questionnaire is explained in the next paragraph. It was sent out to zoos keeping the species and to the ESF studbooks that are being kept for the species Cuora amboinensis and Heosemys spinosa.
57 Zoos were contacted; of which 18 keep animals from the Hong Kong impoundment. ESF studbook keepers have not given out data on the number of participants.

In order to give the nutritional advice that was set out as the main goal of this project two questions were to be answered:
  • How can knowledge about the composition of the in-situ diet be applied in an ex-situ situation?
  • What is the most successful ex-situ diet?
These questions were answered by comparing the natural, in-situ, situation with data on ex-situ keeping of these animals and successes or failures in ex-situ keeping.
Comparison was made on a dry matter basis as is often done in zoo nutrition. This data was then processed further to make it possible to compare on energy basis. All diets were screened and compared on the following nutritional qualities:

Gross Energy
The intake of food is determined by the energy content. This means an animal will eat to satisfy its energy requirements, all other nutritional requirements need to be balanced with energy. The most accurate picture is given by looking at Metabolisable Energy (ME). However, since no indications were found as to how these turtles utilise proteins, fats, carbohydrates and crude fibre, the Gross Energy (GE) content of the diets is used in calculations and comparisons. Gross Energy values were used as given in literature, where needed it was calculated from levels of Crude Protein, Crude Fats, Carbohydrates and Crude Fibre as shown in Appendix VIII.

Crude Protein
Protein is important for the growth and repair and is also a source of energy (M. Knight, 1976). In turtles protein is also required for the growth of the carapaces scutes and the horny covering of the beak (Zwart, 2000). No indications have been found on the amino acid requirements of turtles, or reptiles in general.

Crude Fats
Fats have a high energy density, something that often is not wanted in turtle diets (Dennert, 2001). However fats do serve as a carrier for several vitamins (such as vitamin A and D, discussed below) and essential fatty acids (Palika, 1997). Data on essential fatty acids in turtle nutrition does not seem to be available.

Carbohydrates are the most important suppliers of energy, furthermore they can be converted to bodily fat, useful when a diet contains limited amounts of fat.

Crude Fibre
Herbivorous diets largely consist of crude fibre. Fibre is needed to activate the colon and is therefore crucial in the digestive process. Apart from this fibre can also supply energy to herbivorous animals that utilise hindgut fermentation.

These nutritional values are researched in every nutritional study and are of major importance for the maintenance of the animals.

Reptiles very often suffer from calcium deficiencies due to malnutrition or wrong maintenance. (See also: Phosphorous and Vitamin D3) A lack of calcium is compensated by resorption from calcified body parts, resulting in bone-, and (in case of turtles) shell deformities (Zwart, 2000).

Phosphorous plays an important role in the same bodily functions as mentioned under calcium. Apart from this it also is important in many enzyme systems. Excess of phosphorous may lead to symptoms similar to that of calcium deficiencies (Zwart, 2000).

Calcium : Phosphorous
For optimal usage of both calcium and phosphorous the ratio of the two minerals is very important. A wrong ratio can have the same results as a lack, or overdose of either of the two (Zwart, 2000).

Vitamin A
It is an essential vitamin for growth but the best known function of vitamin A is its influence on the functioning of the vision. Terrapins are often seen suffering from vitamin A deficiency due to insufficient nutrition (Zwart, 2000). Basically vitamin A is available in two main forms; as Retinol, which is the actual vitamin, and as b-carotene that can be utilised in an animal's body in the production of vitamin A (Retinol).

Vitamin B1
Vitamin B1 aids in different bodily functions such as enzymatic digestion and the working of the nervous system (Burger, 1995).

Vitamin D3
Vitamin D3 is essential in the absorption of previously mentioned calcium and phosphorous. Apart from utilising it in its original form as present in the diet, reptiles can also convert cholesterol into vitamin D3 by means of UV-B radiation coming from natural sunlight, or special light sources (Zwart, 1990).

Vitamin E
Vitamin E is an important factor for reproduction success and growth. This vitamin is especially important in the forming of eggs and the strength and shape of the young that is to grow in it. (Dennert, 2001)

Requirements of mentioned nutrients are researched in chapter 3, with additional calculation methods in Appendix VIII.

Procedure Literature review

In-situ data and part of ex-situ data was gained by a literature review. The literature was collected at the libraries of the van Hall Institute, the Library ‘Naturalis’ in Leiden and by searching on the Internet. Table 2.1 shows the search engines and keywords that were used in the Internet search.

Table 2.1 Internet search engines, keywords used and dates of reference.

With searching criteria as listed above several written sources were found, in their turn supplying more useful references for the literature review.

Procedure Questionnaire

In order to study the captive management of the five turtle species private keepers and zoos needed to be questioned about the data on their population, enclosure and the diets of the animals kept. A questionnaire was designed to collect the information of concerning institutions.

The questionnaire used to get these and other data was based on a questionnaire made by Schils and Smeets (2001) who researched the dietary needs of Aldabra Giant Tortoises (Dipsochelys dussumieri) (Schils & Smeets, 2001). Because the study by Schils and Smeets had a good response the questionnaire for this project was made in a similar style. The original questionnaire about Aldabra Giant Tortoises was altered to match the five turtle species. Institutions were asked to fill in the questionnaire separately for each species.
Some questions in the original questionnaire by Schils and Smeets proved to be difficult to answer by participating zoos (Huisman pers. comm.) In an attempt to overcome some of the problems encountered in the Aldabra Giant Tortoise study the new questionnaire was more simplified. Questions asking for food amounts now ask specifically for grams, thus limiting the chance of getting answers that are too diverse to be compared in analyses.

In this study three groups of keepers of Cuora amboinensis and Heosemys spinosa were recognised; those that do not keep animals from the impoundment (keepers of non-Hong Kong animals), those that do keep Hong Kong animals (keepers of Hong Kong animals) and private owners of Cuora amboinensis and Heosemys spinosa participating in ESF studbooks. Different questionnaires were made for these three groups, making it possible to ask for specific data on the animals kept.

1. Keepers of non-Hong Kong animals
The questionnaire made for keepers of animals that are not from the Hong Kong impoundment consisted of:
  • Introduction: This part was made to get general information about the animals. Information about their sex, age and weight is asked to get insight in the demographics of the population.
  • Housing conditions: These were asked to get insight in enclosure size, temperature and UV-radiation, this is done to reflect back to successful or unsuccessful keeping of the species.
  • Feeding information: This was asked to get insight in feeding regime, amounts and ingredients of diets fed.
  • Reliability: In order to estimate the reliability of given information questions were included about using nutritional programs and measuring/weighing of the diet and supplementations.
  • Diet success: In an attempt to judge the successfulness of a diet questions are asked about reproduction success and overall health of the animals kept. Reproduction success is measured by clutch sizes, numbers of eggs fertilised, number of young, and first month/first year mortality of the young produced.
The institutions keeping one or more of the species were looked up at the ISIS abstracts homepage, reptile section (ISIS, 02-05-2002). The e-mail addresses of these institutions were provided by Rotterdam Zoo.

2. Keepers of Hong Kong animals
The keepers of animals coming from the Hong Kong impoundment were also asked the questions described above. However, to get insight in the acceptance of nutritional advice such as was given at the distribution of these confiscated turtles an additional set of questions was included in this questionnaire. This part of the questionnaire dealt with the following topics related to the information-flow within the organisation:
  • Distribution advice: A number of questions were asked to get insight in the difference between the diets fed at the institutions and the advice that was given by EZNC at distribution.
  • Organisation: A number of questions are included in order to see which people in zoo organisations receive the given nutritional advices, who processes them and who should receive such advices.
  • Advice: Institutions are asked for their opinion about the format in which they would like to see the nutritional advices given to them.
The addresses for keepers of Hong Kong-animals were provided by Mr. Henk Zwartepoorte.

3. Private keepers
A number of reptiles kept in private collections are managed in studbooks. These studbooks are co-ordinated by the European Studbook Foundation (ESF). ESF Studbook keepers for the species Cuora amboinensis and Heosemys spinosa were asked to participate in this study in order to get insight in the situation private keepers maintain. ESF studbook members have been approached through these studbook keepers only.
Even though several members of these studbooks have received animals from the impoundment, the questionnaires used were similar to those sent to zoos not keeping Hong Kong animals. This difference was made because the specific questionnaires designed for keepers of Hong Kong animals dealt with the information-flow within the organisation. Private keepers would not have been able to answer most of these questions, therefore the choice was made to eliminate this part for private keepers all together.

Procedure Distribution

All questionnaires were sent by e-mail to eliminate the cost of postal services and to reduce the time lost by shipping and handling of regular mail.
The questionnaires were accompanied by an introducing letter, making up the message part of the e-mail. This part explained the need of the study and the way it was conducted. This letter was signed by Dr. Ir. Walter Jansen and Joeke Nijboer, B.Sc. who assigned the project, and by Mr. Henk Zwartepoorte, closely involved with the implementation of the project. These names were included to emphasise the importance and value of the project.
The questionnaires also contained an example document, describing the situation of Cuora amboinensis at Rotterdam Zoo. This was done to clarify the way the questionnaire was to be filled out.
For the complete questionnaire and the introducing letter see Appendix III.

Processing of questionnaire data

The data that was gathered by the questionnaires was stored and processed in Excel tables. In these tables all given data was processed and nutritional compositions of individual ingredients were used to calculate the composition of the total diet. To define the ingredient composition of the food items fed Nevo (2001), Souci (1986), Zootrition ì, Dietary Management Software (2001), Dierenfeld et al. (1996), Mader (1996), Markwell & Hurley (2001) and other publications were used. When the nutritional composition of ingredients could not be found comparisons with similar food items were made. The same was done when a few of the wanted nutrient values were missing in otherwise useable data. A few calculations had to be made to fill in missing nutritional values. Appendix VIII shows the assumptions and calculations made.

The ingredients and nutritional compounds of the diet fed by each zoo and private keeper are discussed in chapter 4 and completely given in Appendix IV.

Processing of literature data

Data on nutritional requirements of the animals was simplified to one easily comparable list of data. This simplifying was done by calculating all demands for an average representative of the particular species into demand per MJ GE of food. For these calculations average food intake and energy demand were withdrawn from the questionnaires and a standard bodyweight of 1000 grams was assumed.

Demands for nutrients are given on different levels by different authors. Several calculations had to be made to come to the same level (per MJ GE). Examples of different calculations made are given next:
  • Calculating the amount of an energy-supplying nutrient with existing demand as a percentage of total energy supply, assuming ME = GE.
Crude protein = 15%GE/ (average energy density) = demand CP (g)= (15% * 1,00 MJ)/ (0,02412 MJ/ g) = 6,22 g
  • Calculating phosphorous demand /MJ GE from known calcium/MJ demand and Ca/P ratio:
Phosphorus = 0,714 (max Ca)/ 1,25 = 0,571 g /MJ GE
  • Calculating vitamin demand/ MJ GE from known mg/kg level:
Demand mg/MJ GE = Demand mg/kg * weight food (kg)/ energy content food (MJ GE)

Vitamin B1 = 4,4 mg/kg x 0,09266/ 0,367 = 1,11

In-situ diet

This chapter describes the digestive strategy and feeding behaviour of Cuora amboinensis and Heosemys spinosa as well as those of comparable species. This chapter will answer the last part of sub-question one:
  • What is known about the natural diet and feeding behaviour of Cuora amboinensis and Heosemys spinosa?

<i>Cuora amboinensis</i> Digestive system

Very little is known about the digestive system of Cuora amboinensis. Being herbivorous it is very likely to utilise hindgut fermentation and thus have large intestine with a relatively large capacity. (Dennert, 2001). No specific information on the digestive system of Cuora amboinensis could be found.

<i>Cuora amboinensis</i> Ingredients and nutritional contents of the natural diet

Cuora amboinensis often is referred to as being largely herbivorous in the wild (Ernst & Babour, 1989; Mudde, 1981, 1982). Liat & Das (1999) specifically mention wild animals to eat aquatic insects, molluscs, crustaceans, fungi and worms, next to the bulk that is made up by plant matter. However no indication is made as to what part of the diet is made up of this animal matter (Liat & Das, 1999). The first faeces that were produced by Hong Kong impounded Cuora amboinensis consisted of compact plant mass. This mass contained a lot of long fibres, indicating the presence of grasses and/or reed in the natural diet at time of capture (Kerlen pers. comm.).

<i>Cuora amboinensis</i> Feeding behaviour

According to Liat and Das (1999) wild Cuora amboinensis are semi-aquatic, feeding both on land and in water. It is also said to be a good swimmer suggesting that it is capable of catching insects and crustaceans that Liat and Das also mention as part of the diet of Cuora amboinensis (Liat & Das, 1999).

<i>Heosemys spinosa</i> Digestive system

No literature seems to be available on the digestive system of Heosemys spinosa. It is likely Heosemys spinosa utilises hindgut fermentation for the digestion of vegetable matter.

<i>Heosemys spinosa</i> Ingredients and nutritional contents of the natural diet

Smith (1931) who is cited in Mertens (1971) found indications of the natural diet of Heosemys spinosa. The species is described to feed entirely upon vegetable matter (Mertens, 1971). Kerlen, who received five Heosemys spinosa from the Hong Kong impoundment, reported the presence of seeds in the first faeces that were produced in captivity (Kerlen pers. comm.). The seeds involved have not been identified, they are shown in figure 3.1. The presence of these seeds indicates that the natural diet of these animals at time of capture (November/December 2001) at least partly consisted of seed bearing plants.

<i>Heosemys spinosa</i> Feeding behaviour

Liat and Das (1999) report this species to be a poor swimmer. As a result of this it is unlikely this species relies heavily on deep-water plant species as a part of its natural diet (Liat & Das, 1999).

Comparison to similar species

A limited amount of literature was found on the species Cuora amboinensis and Heosemys spinosa. To extend the amount of data the search was expanded to similar species.
The choice of this study to collect data of similar species was based on the assumption that the diets of herbivorous freshwater turtles are basically the same. Freshwater areas in similar climate zones throughout the world are likely to contain similar plant species, thus providing similar ingredients to the turtle’s diets.

Digestive system

The very short length of the large intestine relative to that of the small intestine in several herbivorous freshwater turtles suggests that they might not rely heavily on a large-intestine micro flora. Because aquatic vegetation does not need as much structural support as does terrestrial vegetation and therefore has less lignified complex carbohydrates, freshwater turtles could gain sufficient nutrition by digesting only the soluble cell contents of the plant matter and passing the cell wall fraction undegraded (Bjorndal & Bolten, 1990.)

Ingredients and nutritional contents of the natural diet

Bjorndal and Bolten (1993) performed a study on the digestive efficiencies in herbivorous and omnivorous freshwater turtles on plant diets. This research was done with two turtle species in Florida, the herbivorous freshwater turtle Pseudemys nelsoni and the omnivorous freshwater turtle Trachemys scripta scripta. The natural diets of both Pseudemys nelsoni and Trachemys scripta scripta contain the aquatic plants duckweed, Spirodela polyrbiza, and hydrilla, Hydrilla verticillata. These plants respectively represent floating and submersed aquatic vegetation in the natural habitat of these species. These two groups are said to be the most diverse in components amongst aquatic plants, thus giving an indication of extremes in the vegetation that make up the diet (Bjorndal & Bolten, 1993).
The composition of the aquatic plants duckweed, Spirodela polyrbiza, and hydrilla, Hydrilla verticillata are given in table 3.1.

Table 3.1 Composition of duckweed (Spirodela polyrbiza)
and hydrilla (Hydrilla verticillata) in Florida (USA).
Note: ND, no data.
(Bjorndal & Bolten, 1993).

In another research by Bjorndal & Bolten (1990) they found out that Pseudemys nelsoni on a diet of hydrilla, has very high digestibility’s for dry matter, organic matter, energy, and cell walls, and a lower digestibility for nitrogen (table 3.2 ). A high cell wall digestibility indicates the presence of a gut micro flora (Bjorndal & Bolten, 1990).

Table 3.2 Diet composition and digestive efficiencies
of Pseudemys nelsoni feeding on Hydrilla verticillata.

During this study it was concluded that the daily energy gain for the herbivorous species was significantly lower on the duckweed diet than on the hydrilla as a result of the reduced energy digestibility of duckweed and equivalent intakes of the two diets. The herbivorous species Pseudemys nelsoni gained significantly more nitrogen on a daily basis on the duckweed diet than the omnivorous Trachemys scripta scripta. This is caused by the fact that both intake and nitrogen content of the duckweed diet were higher than that of hydrilla (Bjorndal & Bolten 1993).

For the herbivore species (Pseudemys nelsoni), hydrilla provided more energy whereas duckweed yielded more nitrogen. For herbivores that feed on mixed diets of fruit and foliage, it has been suggested that they select fruits as an energy source and foliage as a source of nitrogen. Herbivores may make similar dichotomous selections among different foliage, which emphasises the need to evaluate more than one currency (e.g., both energy and nitrogen) in studies of diet selection (Bjorndal & Bolten, 1993).

Feeding behaviour

According to Parmenter and Avery (1990) the importance of environmental temperature regimes can not be overstated in regards to the feeding ecology of slider turtles (Trachemys scripta spp.) All physiological processes in relation to the digestive process go faster at increasing temperatures. In the closely related Chrysemys picta a rise of body temperature proved to increase the efficiency of energy assimilation significantly. The same species showed a dramatic decrease in digestive turn over time at increasing temperatures.

As a result of these processes food intake proved to be significantly higher too. In the range of 15-30 °C the food intake increased more than fourfold (Parmenter & Avery, 1990). Figure 3.2 shows the digestive turnover time in laboratory specimens of Chrysemys picta. Figure 3.3 shows the effect of temperature on ingestion of laboratory specimens of Trachemys scripta scripta.

Figure 3.2 The effect of temperature on the digestive turnover time in laboratory specimens of Chrysemys picta (Parmenter & Avery, 1990).

Figure 3.3 The effect of temperature on ingestion in laboratory specimens of the slider turtle Trachemys scripta scripta (numbers on top of bars represent sample size; n)
(Parmenter & Avery, 1990).

Nutritional requirements


According to Mader (1996) energy requirements of reptiles are strongly depended on the temperature of their surroundings and the related body temperature (Mader, 1996). Figure 3.2 already showed the intake of aquatic turtles at different temperatures. Food intake in basic is determined by the amount of energy needed (Burger, 1993). As a result of this figure 3.2 thus shows an increasing need for energy when temperature rises. Mader (1996) determines daily energy requirements by estimation from research data, extrapolation from domestic species and by practical experience (Mader, 1996).

A Standard Metabolic Rate (SMR) describes the energy needed to meet the cost of essential work done by the cells and the organs of the individual (Burger, 1993).
The SMR of turtles in MJ/day is estimated by Mader (1996) to be 0,1344*(W ). Where W is bodyweight in kg. The outcome of this formula must be multiplied by a number between 1,1 and 2,5 according to activity (Mader, 1996). Although Energy requirements of reptiles also are heavily influenced by temperature (Parmenter and Avery, 1990) and, as in every animal, by physiological status (Schmidt-Nielsen, 1997) this is not included in the equation.
This equation is determined in animals at 30°C, a temperature that, according to Mc Arthur is within the preferred temperature range of Asiatic Box turtles (27-30 °C) (Mc Arthur, 1996).
Dennert (2001) mentions the Metabolic energy of reptiles to be; ME = 0,042*(W )
This value also must be corrected for level of activity. Dennert describes those as follows:

Animals at rest/sleeping: x 1,25
Adults with little activity: x 1,50
Adults active: x 2
Growing animals, little activity: x 2
Egg carrying animals: x 2
Animals under stress: x 2-2,5.
(Dennert, 2001)


Protein levels advised by Mader (1996) are shown in table 4.1. This table clearly shows the difference in protein amounts advised for herbivores and carnivores (Mader, 1996).
Zwart (2000) reported that the recommendations concerning the protein content of the food differ between 5% in the Californian desert tortoise (Gopherus agassizii) and 13% in snapping turtles (Chelydra spp. and Macroclemmys spp.). However, mentioned in the same article is an extensive study on red-eared terrapins (Trachemys scripta elegans) fed a diet containing 24-27% protein (Zwart, 2000). No indications were given whether these levels are for an ‘as fed’ diet or on Dry Matter basis. Comparing levels to those advised by Mader (1996) listed below it is likely to deal with levels in the diet ‘as fed’.

Mader (1996) describes the fat requirements for reptiles as a part of the Metabolisable Energy (ME) (Mader, 1996). The values given by Mader (1996) are shown in table 4.1. Again there is a large difference between the demands of herbivorous and carnivorous animals.

Carbohydrate levels in reptile diets as advised by Mader (1996) are given in table 4.1 (Mader, 1996

Table 4.1 Estimated nutritional energy requirements
for captive reptiles as percentage of ME.

Not much is mentioned about fibre requirements of turtles. Zwart (2000) does mention the need of roughage because of its influence on the motility of the intestinal tract (Zwart, 2000). This is a quality that fibre is known for in many different animal species.
Mader (1996) also emphasises the importance of fibre for the gut motility. Herbivorous turtles are said to need at least 12% of DM to consist of fibre, where 20-30% would be closer to optimal (Mader, 1996).

Calcium is of major importance in many metabolic processes in the body. Calcium requirements are said to be somewhere between 428 and 714 mg/MJ. These values are based on experiences with domestic mammals and birds, exact requirements are not available (Mader 1996). Zwart (2000) mentions a level of 1% Calcium in dry matter (Zwart, 2000).

Calculating back from Calcium/ Phosphorous ratio’s as given by Zwart (2000) results in a phosphorous requirement of 0,7-1,7% in dry matter. Something that Zwart (2000) also backs up by stating that a 0,8% level of phosphorous in dry matter is adequate (Zwart, 2000).
Mader (1996) states reptiles’ diet should contain 0.6-1% Phosphorus (DM), a level that is in line with the range given by Zwart (2000).

Calcium/ Phosphorous ratio
Regardless of the actual levels of calcium and phosphorous separately, the ratio between the two is of great importance. Exact requirements of this ratio are not know in full grown animals, but from a great number of observations and extrapolations of other animals it is concluded that a calcium contents of 1,0% in combination with a phosphorus content of 0,8% (in dry matter) are adequate, meaning a Ca/P ratio of 1,25:1 (Zwart, 2000).
Also stated by Zwart (2000) is a diet containing 1,4 to 2,0% calcium in the dry matter at a Ca:P ratio of 1,2:1 or even 2:1 (Zwart, 2000). The Ca/P ratio is something that is rather disputable, ranging to as high as 4:1 or even 6:1 (McArthur, 1996) Although the higher values are likely to apply to egg producing animals, something that is also seen in birds (Huisman, pers. comm.).

Vitamin A
The daily requirement of vitamin A of chelonians is estimated to be 400 IU/kg bodyweight being 2.800 IU/kg bodyweight per week (Zwart, 2000). Dennert (2001) gives a vitamin A requirement of 1.500 IU/kg bodyweight per week (Dennert, 2001). Vitamin A is Retinol, b-carotene often is mentioned as being vitamin A. However it is actually pro-vitamin A that chelonians utilise in the production of vitamin A (Retinol). Hypervitaminoses can occur in the intake of Retinol, b-carotene is not toxic and does not pose a problem if given in high amounts.
If one is to look at amounts of b-carotene it is important to realise that 6 IU of b-carotene are needed to produce 1 IU of Retinol. (See also Appendix VIII).

Vitamin B1
Zwart (1990) proposes a vitamin B1 concentration ranging between 4.4 and 11 mg/kg food (Zwart, 1990).

Vitamin D3
The nutrient requirement in vitamin D3 is related to the Ca:P ratio in the food. There is still no exact data available on the vitamin D3 requirement. If the data from higher vertebrates and other reptiles is extrapolated the vitamin D3 requirement varies between 10 and 100 IU per kg bodyweight per day, being 70-700 IU per kg BW per week. The higher estimation is said likely to be somewhat too high (Zwart, 2000). Dennert (2001) advices 150 IU / kg bodyweight every week (Dennert, 2001). Mader (1996) gives a level of 200-1.000 IU/ kg dry matter in the diet (Mader, 1996).Vitamin D3 can also be produced by the reptiles’ own body under influence of UV-B radiation coming from unfiltered sunlight or special UV-B lighting (Bruins, 1999). In this process cholesterol is transformed into vitamin D3 (Zwart, 1990).

Vitamin E
Dierenfeld (1989) advices a vitamin E level between 1142 and 5709 mg/MJ (Dierenfeld, 1989).

A summarisation of all parameters mentioned above is given in table 4.2.

Table 4.2 Summarised requirements of general turtle diets.

The requirements summarized in table 4.2 can be calculated for both species when a ‘standard’ animal is chosen to fill in missing data. In table 4.3 the requirements of Cuora amboinensis are given assuming the animal weighs 1000 grams, weekly diet fed is 92,66 g, of which 22,93 g is dry matter, and the amount of Gross Energy is 0,367 MJ. Is set to 1000 grams for easy calculating and comparison, other values are averages derived from questionnaire diets given by zoos and private keepers (see Appendix IV and table 5.8).

Table 4.3 Dietary requirements for Cuora amboinensis, assuming bodyweight is 1000 grams, diet as fed is 92,66 grams, dry matter is 22,93 grams and Gross Energy content is 0,367 MJ.

Assumptions for Heosemys spinosa are based on a bodyweight of 1000 grams, and ‘as fed’ weight of the diet of 507,71 grams with a dry matter of 71,96 grams and a GE content of 1,024 MJ. Weight is set to 1000 grams for easy processing and comparison, other values are derived from questionnaire diets given by zoos and private keepers (See Appendix IV and table 5.10).

Table 4.4 Requirements for the diet of Heosemys spinosa assuming bodyweight is 1000 grams, diet as fed is 507,71 grams, dry matter is 71,96 grams and Gross Energy content is 1,024 MJ.

Food related diseases, deficiencies and illnesses

In case of malnutrition animals are likely to eventually show this by a changing physiological condition. This paragraph explains the disorders most commonly associated with poorly fed turtles, and reptiles in general.

A deficiency in proteins may occur when an inadequate diet is fed in captivity that consists exclusively of the outer leaves of salad and fruits. Periods of protein deficiency may lead to disturbance in growth of scutes of the carapace and the horny covering of the beak as well as to failure in reproduction (Zwart, 2000).
Protein over dosage can lead to growth problems such as pyramiding shell scutes, unproportionated limbs and shell size and overweight (Mc Arthur, 1996) gout (Zwart, 2000) and according to Palika (1997) cited in Schils and Smeets (2001) it can even cause kidney failure.
When the diet composition suddenly changes an overfeeding with proteins could occur. This overfeeding may lead to disturbance of the intestinal flora, with production of abnormal products, diarrhoea and large amounts of gas (Zwart, 2000).

Disturbance in the fat metabolism does occur. Yellow fat disease and in addition also a few cases of focal degeneration of fat tissues have been described in red-eared terrapins (Trachemys scripta elegans) (Zwart, 2000).

Hypovitaminosis A (vitamin A deficiency) in terrapins
A deficiency in vitamin A is most common in omnivorous and carnivorous terrapins. If older animals that are caught in the wild are transferred to a deficient diet in captivity they may develop clinical signs after a period of several months to one year, depending on the reserves in vitamin A. Vitamin A deficiency may lead to gastrointestinal disturbance such as anorexia, diarrhoea or even excessive salivation. Bulging and swelling of the eyelids are clinical signs of hypovitaminosis A. Reptiles that suffer from hypovitaminosis are likely to be deficient in other vitamins and minerals as well (Zwart, 2000).

Hypovitaminosis B1 (vitamin B1 deficiency)
Only a few indications of hypovitaminosis B1 occurring in tortoises and terrapins are know. A deficiency in vitamin B1 may lead to anorexia, poor growth and chronic loss of weight in spite of sufficient uptake of food. A clinical sign is that the eye is retracted in the orbita (Zwart, 2000).

Hypovitaminosis D3 (vitamin D3 deficiency)
When a vitamin D3 deficiency occurs a change in the diet is essential. The vitamin D3 deficiency was solved in reacted in red-eared terrapins (Trachemys scripta elegans) by feeding a product (Carmix, Hope farms, Woerden, the Netherlands) containing 11,65% Ca, 0,4% P and 20.000 IU vitamin D3. This was applied by rubbing the product intensely into pieces of meat (Zwart, 2000). Vitamin D3 is produced under the influence of UV-B radiation. Correct lighting in captivity or the presence of unfiltered sunlight overcomes the need of supplementation with vitamin D3 (Bruins, 1999; Mc Arthur, 1996).

Calcium deficiency
A deficiency in calcium leads to nutritional osteodystrophia fibrosa. The clinical signs of osteodystrophia fibrosa are a breakdown of the original bone and the production of a fibrocollagenous connective tissue. Osteodystrophia fibrosa can be prevented by feeding selected greens and fruits. Greens, which have a Ca:P ratio higher than, or close to 1, are preferable (Zwart, 2000). Examples of such greens are: dandelion (2,64), endive (1,86) and pak-choi (2,00) (Mader, 1996; Souci, 1986; Nevo, 2001).

Problems with Calcium, Phosphorous and vitamin D3 are popularly known as rachitis (Göltenboth & Klös, 1995) or MBD (Metabolic Bone Disease) (Davies & Davies, 1997) both are terms often used to describe deficiency diseases associated with a shortage in calcium or vitamin D3 or an unequal ratio of calcium and phosphorous. This disorder is associated with weak and soft bones, often surrounded by connective tissue. Animals suffering an advanced stage of MBD often have deformed body parts, turtle sufferers are easy recognisable by soft shells (Davies & Davies, 1997).

In several species of tortoises and terrapins litophagy, the uptake of stones occurs. Regular uptake of larger masses of stones leads to intestinal obstruction (Zwart, 2000).

Geophagy is the uptake of sand and is to some degree physiological in tortoises and contributes to a firmer substance of the faeces. But an exceptionally high uptake of sand may lead to intestinal impaction and atony and eventually causing death of an individual (Zwart, 2000).

Ex-situ diet

This chapter describes the diets fed to Cuora amboinensis and Heosemys spinosa in captivity. Diets mentioned in literature about captive management and gathered data on diets fed by zoos and private keepers are given. With this information sub-question two will be answered:

  • What is known about the way in which Cuora amboinensis and Heosemys spinosa are kept ex-situ?

Literature ex-situ diets of the <i>Cuora amboinensis</i>

Despite the fact that wild Cuora amboinensis are mostly referred to as herbivorous, this species often is fed a carnivorous diet in captivity. An article by Hofstra (1994) describes a diet used for captive bred young C. amboinensis. These animals are fed on a diet of mealworms, heart, beef (whole pieces as well as minced and mixed with Gistocal), earthworms, dry cat food, cod filet and large quantities of pulverised chicken egg scales. The author feeds his adult animals almost exclusively on dry cat food (Hofstra, 1994).
Mudde (1981) also is aware of the fact that literature describes this species as herbivorous. According to his experience the animals are more carnivorous and occasional plant eaters, which is an experience, he has with most aquatic turtles. His animals were fed shrimp, earthworms, slugs and snails (both terrestrial and aquatic). Less popular were meat (no specification) and fish, where only tiger barbs (Barbus tetrazona) were accepted. The author does note the fish have to be largely immobilised by cold temperatures or a low water level for the turtles to catch them. Guppies (Poecilia reticulata) were never accepted, neither live or dead, even though a population of this species constantly lived in with the animals. Plant matter was accepted by his group of C. amboinensis and the author mentions apple, banana, and cucumber as well as floating plants kept in the enclosure (Mudde, 1981).In a 1982 article by the same author he describes all things ever accepted in the diet of this species, no quantities or frequencies are mentioned though;
Animal matter: Shrimps, commercial dry turtle food, soaked dry cat food, canned cat food, pieces of day-old chicks, meat (no mentioned of which animal), pike (Esox lucius), cod (Gadus morhua), smelt (Osmerus eperlanus), coalfish (Pollachius virens), worms, mealworms, crickets, wax worms, mosquito larvae, Daphnia, Mysis, snails, slugs, Gammarus, woodlice (Porcellio scaber).
Plant matter:banana, cucumber, several water plants, boiled rice, beans, peas, soaked corn and even shrimp crackers, wholebran biscuits and popped corn were accepted (Mudde, 1982).

Literature ex-situ diets of the <i>Heosemys spinosa</i>

Limited information is published about the captive diet of this species. A report by Herman (1993) describes the diet of three captive Heosemys spinosain the Zoo of Atlanta (USA) and the offspring they produced. The animals had a preference for tomatoes (Lycopersicon esculentum). Tomatoes were the only things that were accepted in the first year of captivity. After this year other fruits and vegetables were also accepted. Finally mixed salads were given, consisting of several fruits, vegetables and collard greens (no species were mentioned). Animals also accepted chopped, skinned mice that were presented occasionally. Why these mice were skinned is not mentioned. Eventually the author mentions the quantity of mice in the diet was drastically cut back because of the animals becoming obese (Herman, 1993).An article by MÒller (1906) describes a captive youngster that feeds on fruits, salads and aquatic plants (including duckweed). Apart from this the turtle also accepted animal matter such as earthworms, mealworms and red meat (Muller, 1906).

Diets fed by Zoos and Private keepers

This paragraph describes the results from the questionnaires that were sent to zoos and private keepers of Cuora amboinensis and Heosemys spinosa. Zoos and private keepers that sent back the questionnaire and data on the overall response of the questionnaire are given in Appendix V.

This paragraph will answer the sub-question:

  • What is the composition and nutritional value of the diets currently fed to Cuora amboinensis and Heosemys spinosa in captivity?


This paragraph will show the difference and resemblance between ingredients fed by zoos and private keepers. For Cuora amboinensis 4 zoos and 6 private keepers returned the questionnaire. For Heosemys spinosa the questionnaire was returned by 6 zoos and 1 private keeper. The values gathered by the questionnaires are reported in several tables.

Ingredients of diets fed to <i>Cuora amboinensis</i>

Cuora amboinensis is fed a variety of food items. All different food items fed can be found in Appendix VI.

The items most commonly fed to Cuora amboinensis are given in table 5.1. This table differentiates between the diets fed by zoos, and those fed by private keepers.

Table 5.1 Most commonly fed ingredients (Total >20%) in ex-situ feeding of
Cuora amboinensis, including the difference between zoos (n=4) and private keepers (n=6)

Table 5.1 shows no great differences between zoos and private keepers in terms of ingredients. It appears that private keepers feed a more varied diet, with more different ingredients (see also Appendix VI). Surprisingly this species, known as herbivorous, or largely so, is most commonly fed with animal matter (fish and beef meat). Although this data does not tell anything about the quantity of these food items fed it is remarkable that these are the most commonly fed items.

Ingredients of diets fed to <i>Heosemys spinosa</i>

The food items fed to Heosemys spinosa can be found in Appendix VII. The most commonly fed food items are given in table 5.2.

Table 5.2 Most commonly fed ingredients (Total >20%) in ex-situ feeding of
Heosemys spinosa, including the difference between zoos (n=6) and private keepers (n=1
This table clearly shows the animals are fed mostly herbivorous, although fish and mice are also included in the list of most fed items. Ten out of the sixteen most fed items is a fruit, other plant matter is only scarcely fed.

Supplements used

This paragraph describes the use of supplements in the diets fed to Cuora amboinensis and Heosemys spinosa by zoos and private keepers. All supplements used are shown in table 5.3.

Table 5.3 Supplements fed, differentiating between zoos (n=10) and private keepers (n=7).

In terms of supplementation the most commonly used practice appears to be to use none at all. Most commonly used are the supplements Carmix and Sporavit, these items especially are used by the private keepers.

Nutritional contents of diets fed

This paragraph will describe the nutritional values of the diets fed to Cuora amboinensis and Heosemys spinosa by zoos and private keepers. These values are calculated and progressed in excel (see Appendix IV). Some assumptions had to be made about the nutritional value of ingredients to make it possible to process more of the received data. The exact listing of all assumptions made is shown in Appendix VIII.

Diets fed to <i>Cuora amboinensis</i>

The results of the questionnaires as given in Appendix IV can be compared on the amount of nutrients present per MJ Gross Energy. A summarisation of this comparison is given in table 5.4.

Table 5.4 Nutritional compositions per MJ Gross Energy of diets of Cuora amboinensis as offered by zoos and private owners.

Table 5.4 shows large diversity between the different diets fed. Large fluctuations occur in some of the given values. Most striking is the difference in the amount of protein. This value differs by a factor 10 between the maximal and minimal value.

Table 5.5 shows the same nutritional values as given in table 5.4, here however the food that is said to be eaten is analysed

Table 5.5 Nutritional compositions per MJ Gross Energy of diets of Cuora amboinensis as estimated to be consumed at zoos and private owners.

The values in table 5.5 differ little from those given in table 5.4. This could indicate that what is fed is also consumed. However, as can be seen in Appendix IV some keepers do mention food being left over. The one value strikingly different in this table is that of b-carotene/MJ GE. This value is far higher (about twice as high) in the consumed diet. This is caused by the fact that animals from keeper 3 refuse the relatively energy rich cat food that they are offered (See Appendix IV). Without this food item energy will mostly come from vegetable matter. Vegetable matter is relatively high in levels of b-carotene

Diets fed to <i>Heosemys spinosa</i>

A comparison of nutrients per MJ Gross Energy is made from data in Appendix IV, a summarisation of this comparison is given in table 5.6.

Table 5.6 Nutritional compositions per MJ Gross Energy of diets of Heosemys spinosa as offered by zoos and private owners.

Nutritional values per MJ GE of the diets fed to Heosemys spinosa by zoos and private keepers are also rather scattered. Most striking, as with Cuora amboinensis, is the difference in protein levels.

Table 5.7 shows the nutrient values of the diets that are said to be consumed by Heosemys spinosa at zoos and private keepers.

Table 5.7 Nutritional composition per MJ Gross Energy of diets of Heosemys spinosa as estimated to be consumed at zoos and private owners.

The values in table 5.7 differ little from those given in table 5.6. This could indicate that what is fed is also consumed. However, as can be seen in Appendix IV some keepers do mention food being left over. The little difference with the levels of consumed food indicates that no specific selection takes place, as levels of nutrients stay roughly the same as in the diets fed.

Energy and food intake

This paragraph describes the average amount of food offered to one Cuora amboinensis or Heosemys spinosa weekly, compared with the average bodyweight of the animals kept by a specific keeper

Energy and food intake <i>Cuora amboinensis</i>

The average amount of dry matter and Gross Energy each zoo and private keeper feeds their Cuora amboinensis in relation to the average weight of the animals is described in table 5.8.

Table 5.8 Average amount of food offered to one individual of Cuora amboinensis weekly, comparing with the average bodyweight of animals kept by specified keeper

Large differences can be seen between the amount of food that is being fed to Cuora amboinensis at questioned zoos and private keepers. The amount fed per kg bodyweight differs from 31 to 227 grams per animal per week. If a correction is made by comparing diets on a dry matter basis, the difference becomes less dramatic but still remains remarkably large. Here the weight ranges from 6 grams DM to 53 grams DM weekly. Because animals basically eat to meet energy demands it can be expected that this difference is caused by a great fluctuation in energy density between the diets. If diets are compared on a GE/kg bodyweight basis differences are indeed somewhat flattened out. The lowest and the highest values still differ by a matter of 8 times, but these numbers are just what is being offered and only roughly indicate intake. Finally different levels of activity, physiological status and temperature also have influence on energy demand (see

The average amount of dry matter and gross energy each zoo and private keeper states is being eaten by their Cuora amboinensis, combined with the average weight of the animals kept is described in table 5.9.

Table 5.9 Average amount of food consumed by one individual of Cuora amboinensis weekly, comparing with the average bodyweight of animals kept by specified keeper.
Again, like in table 5.7, the amounts of food differ greatly between the different zoos and private keepers. If the energy intake is studied the scattered values in food amount show more resemblance. Apart from the highest values such as 0,635 and 0,471 all values are within a rather close range. If the very highest values are ignored it can be carefully said that the intake, and thus the requirement, of these animals lies somewhere about 0,25 MJ GE/week

Energy and food intake <i>Heosemys spinosa</i>

The average amount of dry matter and Gross Energy each zoo and private keeper feeds their Heosemys spinosa in relation to the average weight of the animals is described in table 5.10.

Table 5.10 Average amount of food offered to one individual of Heosemys spinosa weekly, comparing with the average bodyweight of animals kept by specified keeper.
Differences in the amount of food that is fed per kg bodyweight show little extremes. Only the diet fed to young kept by keeper 1 is a significant extreme being three times as high as the average of the other diets. However honest comparison can not be made in this matter since it obviously concerns very small juveniles that, for their growth, have totally different energy requirements as adults do. This theory as backed up by the fact that the diet second highest in energy is that fed by Zoo 5 (Moscow) where it also concerns juvenile animals, in this case, judging by weight, probably sub-adults.

The average amount of dry matter and gross energy each zoo and private keeper states is being eaten by their Cuora amboinensis, combined with the average weight of the animals kept is described in table 5.11.

Table 5.11 Average amount of food eaten by one individual of Heosemys spinosa weekly, comparing with the average bodyweight of animals kept by specified keeper

As in table 5.10, which described the amounts offered to Heosemys spinosa, table 5.11 also differs little in intake/kg bodyweight. The energy values given in table 5.11 still largely differ in terms of life stage. Still the adult animals (judging by weight) have significantly lower energy intakes than the younger animals kept by keeper 1, and Zoo 5 The energy intake, and thus roughly the requirement, of adult animals, based on the data above is somewhere in the line of 0,65 MJ GE/week.
Younger animals are likely to have a higher need of energy, according to data above this could be as high as 1,75 MJ GE/week, more than double that of adults.

Reproduction success

This paragraph will answer the sub-question:

  • Which diets are fed to Cuora amboinensis and Heosemys spinosa that have a good reproduction success?

Hardly any data on reproduction was gathered from zoos and private keepers. Only one zoo, Zoo 7, reported reproduction success. Cuora amboinensis is being bred regularly at this zoo. For Heosemys spinosa no data on successful reproduction was reported. The reproduction data of Cuora amboinensis at Zoo 7 is shown in table 5.12.

Table 5.12 Reproduction results of Cuora amboinensis at Zoo 7.

It can be clearly seen that both the number of eggs as the percentage of successful hatching increased over the years. In the questionnaire the zoo reported no changes in the diet over the last five years. The diet fed consists mainly of animal matter, the total amount of nutrients per MJ GE is given in table 5.13. This zoo reported that small amounts of plant matter are also fed occasionally. However no indications were given about the amounts concerned, therefore it has not been included in calculations. As a result values given in table 5.13 are likely to differ slightly from the actual situation. The complete composition of the diet is given in Appendix IV, Zoo7.

Table 5.13 Nutrients per MJ GE of the diet fed to
reproducing Cuora amboinensis at Zoo 7.

Diet related diseases and causes of death

This paragraph describes the nutrition-related diseases and deficiencies that occur with captive Cuora amboinensis and Heosemys spinosa. This paragraph will answer the sub-question:

  • · What nutrition related diseases and deficiencies occur amongst Cuora amboinensis and Heosemys spinosa in captivity?

  • Commonly reported diseases are pneumonia, shell rot, parasites and anorexia. Only pneumonia was mentioned amongst non-confiscated animals, these cases were reported by a single keeper. All reported diseases are shown in table 5.14.

    Table 5.14 Reported diseases, differentiating between non-confiscated,
    and confiscated animals.

    A lot of the confiscated animals suffered from some form of bad health. Several questionnaires mention single specimens to suffer from numerous disorders. The total number of reported cases therefore does not reflect a number of animals.
    Several animals also died after arrival at the zoos and keepers. Often several diseases were reported to trouble the animals before they died from bad general health. No indications were given on nutritional related diseases. Most nutrition related diseases take time to reveal themselves. Because most confiscated animals are adults, and have only been in captivity for a couple of months a deficiency, or overdose, of nutrients doesn’t show up even if it would be present. Long term captive animals were also not reported to suffer from any diseases related to their nutrition.


During this study several points of discussion have risen, both in the literature search and in the processing of the questionnaire results. In order to indicate the accuracy and foundation of found results this chapter discusses the topics found

General comments


As described in the general description of Cuora amboinensis three sub-species have been recognised. These subspecies are largely differentiated on the shape of their carapace, making them more, or less, domed. Highly domed specimens are likely to be less aquatic than those that have a more flattened carapace. The difference in lifestyle could also result in a difference in diets. Zoos often don’t know what subspecies they keep and therefore different subspecies are also mixed (Kerlen, pers. comm.). The animals from the impoundment most likely all belong to the subspecies Cuora amboinensis kamaroma (Kerlen, pers. comm.) This subspecies is the most domed of the three (Filella, 2000). If the assumption is made that a domed animal is indeed more terrestrial and slower in water these are likely to be the most herbivorous.

Diet frequency

In Appendix IV, and calculations based on data from Appendix IV, ingredients and nutrients values are presented in amounts per week. This data can easily be misinterpreted by those used to daily fed rations. The choice for amount per week, instead of amount per day as is regularly used was made because most zoos and private keepers proved to feed their animals less than seven times a week. Apart from this food amounts are very small, and the amounts of the different nutrients even smaller. Presenting the diets as weekly offered/eaten made both processing and interpreting of data easier and was therefore chosen as the standard for this study.


Because of the great difference in origin, the composition of ingredients of the diets of Cuora amboinensis and Heosemys spinosa were taken from several sources. Although there is no reason to doubt accuracy of the different sources used it does need to be mentioned. Different methods of analyses, renewed insights on nutrition and differences in significance of numbers influence results. Differences in sources also influence the advice given in chapter 8; recommendations. This is based on European, primarily Dutch, data on food composition. The composition of certain products can be significantly different in other parts of the world. (Huisman, pers. comm.). The given advice, when applied in for example the US might result in different nutrient levels then those that were aimed for.

Assumptions of food items

To process all the data that was gathered by the questionnaires several assumptions and calculations had to be made, those are given in Appendix VIII. Where the composition of food items was not available values of comparable food items were used. Of other food items some values were unavailable, the missing values were filled up with values of comparable food items. These assumptions had to be made, because filling in zero for a nutrient makes the results unreliable. With the solution of filling the missing values by values of comparable food items the reliability of the results increases in comparison to leaving these unfilled. However assumptions do influence the accuracy of data since the assumed values are never completely the same as actual values. Assumptions were made by comparing items to items that were reasoned to have the most similar composition possible. With this method the found results give a good indication on the actual truth.

Assumptions of supplementation

In some cases supplementation’s were reported that were of unknown composition. Despite several attempts to obtain the composition of these supplements from the institution using it, the manufacturer, or literature some of these compositions remained unknown. Because supplementation has a great influence on the composition of a diet (especially calcium, phosphorous and vitamin levels) assumptions had to be made to prevent extreme differences. Assuming that missing data is similar to the composition of the supplement ‘Gistocal’ made it possible to process diets with still a plausible composition. However because of the large influences of a supplement the difference in composition might have a large influence on the eventual values in the total diet. Because of the possible large influence of supplement assumptions, data that is based on such assumptions has been clearly marked in this report to emphasize these might in fact be significantly different. However the level of macronutrients is not likely to differ greatly because of these assumptions.

Accuracy of returned data

The questionnaires that were processed contained accurate numbers on amounts fed, presented in grams. Where keepers were asked to fill in how often the diets were actually weighed all reported amounts were never weighed. This data indicates the amounts noted in the questionnaire are almost always an estimate thus making data less accurate. Supplements on average were said to be more specifically measured. Often standard measuring spoons are said to prevent over- or under dosage. Supplements usually contain relatively high amounts of calcium, phosphorous and vitamins, outweighing levels in non-supplement food items by far. Because of this the significance of the levels of these nutrients is therefore more accurate than those in not measured non-supplement items.

Species information

Not much literature was found on the digestive system, ingredients and nutritional contents of the natural diet and the feeding behaviour of Cuora amboinensis and Heosemys spinosa. A comparison with similar species, or even turtles or reptiles in general, had to be made in order to complete missing data. In general not much literature is available on turtles, tortoises or terrapins in reference to the digestive system, ingredients and nutritional contents of the natural diet and their feeding. The data gathered by literature gives a trustworthy indication of the actual truth but might differ significantly. Cuora amboinensis and, to a lesser extent Heosemys spinosa, are bound to a somewhat aquatic environment, significantly different from the habitats inhabited by herbivorous tortoises living in dry regions.


Food intake and digestive turn over time is shown to be heavily correlated to temperature. (Parmenter & Avery, 1990). This correlation indicates the different need of energy at different temperatures. It is therefore hard to compare results of energy intake between individuals, because not only size and weight but also the enclosure temperature is of influence. Large differences between energy intakes can likely be described to differences in enclosure temperature. Temperature of the enclosures and water at individual keepers has not been included in results or comparisons. This choice has been made because actual body temperatures cannot be directly derived from the enclosure temperatures. Animals are usually able to thermoregulate because of a relative cool water temperature and a basking site with higher temperatures. What the actual body temperature of these animals is cannot be said with present data.


Zoos and private keepers were asked estimated the amount of food left over by their animals. Estimation is a personal view on a matter and can differ significantly from the actual truth. However it was chosen to be processed in addition to the composition of diets as offered to be able to compare. Values given for diets eaten should however be carefully interpreted.


<i>Cuora amboinensis</i>

There is a significant difference noticeable between diets that were reported. Most striking differences are seen in the macronutrients (Protein, Fats, Carbohydrates, Fibre and Ca /P). Differences in diets researched can best be seen when illustrated in graphs. Figures 6.1, 6.2 and 6.3 describe the macronutrients in diets of Cuora amboinensis in grams per MJ Gross Energy:

Figure 6.1 Macronutrients in diet of Cuora amboinensis in grams per MJ GE, averages of literature recommendations (derived from table 4.3).

Figure 6.2 Macronutrients in diet of Cuora amboinensis in grams per MJ GE, averages of zoos and private keepers (derived from table 5.4).

Figure 6.3 Macronutrients in diet of Cuora amboinensis in grams per MJ GE, advice as given by EZNC (derived from Appendix IX).

Very striking is the difference between average requirements as given in literature and the average diets that are actually being fed. Especially protein levels and carbohydrate levels differ greatly. This difference is the result of the fact that both largely carnivorous diets and largely herbivorous diets are fed (See Appendix IV, Zoo 4 and keeper 6). Levels of carbohydrates differ a lot because of the exact same difference in diets, the extremes are caused by keepers feeding high energy diets with little vegetable matter, and keepers feeding diets high in vegetable matter and low in energy density.

Herbivores fed with a diet rich in proteins are likely to develop serious health problems associated with growth deformities or even kidney failure. No such cases have been reported (also not amongst long-term keepers) Literature on ex-situ keeping and the reproduction success at Zoo 7 strongly indicate Cuora amboinensis might be more omnivorous than was thought at first. Comparison of literature values to the advice as given by EZNC at distribution of the animals shows the advice is more in line with the literature values, however this diet is extremely rich in fibre while it is contains less carbohydrates. Because both values are heavily associated with plant matter this difference is less striking than that between literature and actual practice.

The energy intake of Cuora amboinensis is significantly lower than expected. The lowest value mentioned is the need of inactive animals, ME = 0,063*(W ). For a 1 kg animal this would mean a weekly energy need of 0,441 MJ Metabolic Energy. The average energy content of diets offered to Cuora amboinensis is 0,367 MJ Gross Energy. If high levels for juveniles are ignored and the reported intake is chosen as an indicator apposed to the amounts offered the average intake reaches as low as 0,25 MJ GE. What part of that is utilised as Metabolic Energy is unknown, as is the reason for these low levels.

Table 6.1 shows all researched values per MJ Gross Energy in comparison, the carnivore diet as advised by EZNC is included for comparison and will not be discussed. The composition of this diet is given in Appendix IX.

Table 6.1 Nutritional qualities of Cuora amboinensis diets, comparing literature values, diets fed by questionnaire participants and the advice given by EZNC.
Diets that are already being fed are rather similar to the average literature values when looking at the different vitamins. The levels of vitamin A and D3 advised by EZNC (in the herbivore diet) however are very high in comparison to literature. This and the high levels of Calcium and Phosphorous are a direct result of high amounts of supplements used. Both vitamin D3 and vitamin A are known to be toxic in high levels, making the amounts advised by EZNC potentially dangerous. Also striking is the high level of vitamin E in both fed and EZNC advised diets, being a fat-soluble vitamin this will not be simply excreted and may form problems if build up occurs. The effects of excess vitamin E intake are not known and are potentially harmful, although definitely not as harmful as hypervitaminoses of vitamin A or D (Burger, 1995).

<i>Heosemys spinosa</i>

Macronutrients in the diets of Heosemys spinosa are given in figures 6.4, 6.5 and 6.6 where they are shown in grams per MJ Gross Energy:

Figure 6.4 Macronutrients in diet of Heosemys spinosa in grams per MJ Gross Energy, averages of literature recommendations (derived from table 4.4).

Figure 6.5 Macronutrients in diet of Heosemys spinosa in grams per MJ Gross Energy, averages of zoos and private keepers (derived from table 5.6).

Figure 6.6 Macronutrients in diet of Heosemys spinosain grams per MJ Gross Energy, advice as given by EZNC (derived from Appendix IX).

For Heosemys spinosa the actual diets that are being fed are strikingly similar to the literature requirements gathered. This similarity can be explained by the fact that Heosemys spinosa in general is fed a diet primarily herbivorous. Even though there are some exceptions overall the animals are being fed rather much like literature theory. The EZNC advice is significantly different on especially the levels of carbohydrates and crude fibre. Furthermore the advised diet contains large amounts of both Calcium and Phosphorous, although the ratio between the two is rather similar to that averagely fed by private keepers.
The estimated energy intake calculated from reported diets is more similar to literature values than those seen in Cuora amboinensis. Heosemys spinosa is fed averagely 0,65 MJ GE per kilogram bodyweight per week. Here too the minimum literature demand for a 1 kg animal is 0,441 MJ Metabolic Energy. This is in line with found Gross Energy values although it is not known what part of GE is utilised for ME.

All researched nutrients per MJ Gross Energy are given in comparison in table 6.2.

Table 6.2 Nutritional qualities of Heosemys spinosa diets, comparing literature values, diets fed by questionnaire participants and the advice given by EZNC.

As said the average diet of Heosemys spinosa is fairly close to advised literature values. Here too the most important and striking differences are found in vitamin levels. Again the levels of Retinol and vitamin D3 are extremely high in the advised diet. Vitamin E again is high in both fed and advised diets although the difference of literature to fed diets is not as big in this case. As with Cuora amboinensis it is likely that over usage of supplements is the base of these high levels.


All data put together results in the following conclusions in reflection of the research questions asked.

In situ data

In what kind of ecosystem do Cuora amboinensis and Heosemys spinosa live?
  • Both Cuora amboinensis and Heosemys spinosa live primarily in areas with water bodies such as rivers and rice paddocks. Cuora amboinensis is very much aquatic whereas Heosemys spinosa, being a poor swimmer, appears to live a more terrestrial life.

What is known about the digestive system of Cuora amboinensis and Heosemys spinosa?
  • Very little is known about the digestive system of turtles in general. Information available often refers to truly terrestrial tortoises or truly aquatic turtle species such as terrapins. The digestive systems of Cuora amboinensis and Heosemys spinosa as far as known have not been described.

What is known about the natural diet and feeding behaviour of Cuora amboinensis and Heosemys spinosa?
  • Very little is known about the composition of the natural diet of these turtles.
    Indications are made that both are largely herbivorous but contents are not clearly described in available publications.

  • Cuora amboinensis, being very much aquatic, is thought to rely heavily on aquatic food items. Reed and/or grass likely form some part of the natural diet as wild caught animals produced faeces containing fibrous matter of such vegetation. Animal matter is thought to be occasionally eaten..

  • Heosemys spinosa probably is bound very much too terrestrial vegetation, as it is a poor swimmer. Seed bearing plants are proven to be at least a part of the natural diet as wild caught animals produced faeces containing seeds of at least two different plant species.

Ex-situ data

What is the composition and nutritional value of the diets currently fed to Cuora amboinensis and Heosemys spinosa in captivity?
  • Cuora amboinensis is fed a largely omnivorous diet in captivity, Questionnaire results show an average of 52% of the weight of the diet as fed is animal matter. Also the most commonly fed food items are of animal origin.

  • Heosemys spinosa is fed mostly herbivorous in captivity, on average 5% of the weight of the diet as fed consists of animal matter. The overall diet of Heosemys spinosa in captivity consists mainly of fruits.

  • The average energy intake of Cuora amboinensis is 0,301 MJ GE /kg/week, ignoring extreme values indicates this being even lower, around 0,25 MJ GE/kg/week. According to questionnaire results energy intake of juveniles are significantly higher, this is about 1,75 MJ GE/kg/week.

  • Lots of different supplements are used in the nutrition of these species, composition of those supplements are often not findable.

  • Overall supplements are fairly easily used. In several diets, including the advice given by EZNC the levels of the potentially toxic vitamins as vitamin A, vitamin D3 and vitamin E are several times greater than advised. The same trend is found in Calcium and Phosphorous levels, also the result of too large amounts of supplements.

Which diets are fed at institutions that have a good reproduction success?
  • Reproduction in captivity proved to be rare, only one zoo breeds Cuora amboinensis. The diet fed to at this zoo is largely carnivorous.

  • No breeding results have been reported for Heosemys spinosa.

What nutrition related diseases and deficiencies occur amongst Cuora amboinensis and Heosemys spinosa in captivity?
  • No nutrition related diseases are reported to occur amongst Cuora amboinensis and Heosemys spinosa in captivity. It cannot be concluded that the diets fed to these two species must therefore meet requirements as some diets have only been fed since the institution using it received animals from the confiscation.

What diet composition in terms of nutrients and ingredients is best applicable in captive management of the species Cuora amboinensis and Heosemys spinosa?

Cuora amboinensis
    Captive Cuora amboinensis are omnivorous by choice; this can be caused by the high digestibility of aquatic vegetation that makes up at least a large part of their natural diet. The diet fed to captive Cuora amboinensis is likely to most successful when containing a certain part of animal matter as is partly proven by the single reproducing zoo feeding largely carnivorous.

Heosemys spinosa
    As Heosemys spinosa lives a largely terrestrial life, its natural diet most likely consists of terrestrial vegetation. A captive diet can be based largely on knowledge about tortoises although this species appears to prefer a diet consisting largely of fruits. This preference can reflect the natural diet, as seeds that have been found in faeces may very well be residues of consumed fruits. Furthermore fruits are likely to make up a large part of the food available in the forests this species is often found in.

In conclusion it can be said that overall data on Cuora amboinensis and Heosemys spinosa and similar species gives a good picture on the rough outlines of their nutrition, but the actual dietary requirements of the species cannot be exactly determined. The diets that are currently fed to Cuora amboinensis and Heosemys spinosa appear to be sufficient for maintenance, as no serious deficiencies have been reported. However, because a large portion of the diets has not been used for a long time (only since specific keeper received the species from the impoundment) it cannot be concluded that all diets actually meet the nutritional requirement. An important aspect in the nutrition of these animals is the use of supplements, although needed for the correction of levels of important minerals and vitamins it should not be used too lightly as over dosage can also have serious effects. Finally breeding of these species is still a rarity, both in literature and in questioned zoos and keepers. The information gathered in the previous chapters and the conclusions here have been used to revise the advice given by EZNC in January 2002 and to give more insight in the poorly studied nutrition of these turtles. In the next chapter recommendations are given for optimal maintenance of these species.


This chapter describes the recommendations for the nutritional composition of the ex-situ diets for Cuora amboinensis and Heosemys spinosa by answering the sub-question:
  • · What diet composition in terms of nutrients and ingredients is best applicable in captive management of the species Cuora amboinensis and Heosemys spinosa?

Feeding advice

Diet composition

Chapter 9 and 10 describe the nutritional requirements and diet composition for Cuora amboinensis and Heosemys spinosa. All demands have been taken into account. Diets are composed primarily of most commonly used food items, were needed somewhat less used products have been included to adjust the nutritional composition. Calculations are made for a one kilogram animal, which is close to the average adult weight for both species (Heosemys spinosa can exceed this greatly though). If bodyweight differs greatly the amounts given can be multiplied with the bodyweight (in kilograms).
The diet recommended for Cuora amboinensis is given in table 8.1, the composition per MJ GE is given in table 8.3. The total nutritional composition is given in Appendix X.

Table 8.1 Advised diet composition for Cuora amboinensis,
food items per week per kilogram animal.

The diet recommended for Heosemys spinosa is given in table 8.2, the composition per MJ GE is given in table 8.3. The total nutritional composition is given in Appendix XI.

Table 8.2 Advised diet composition for Heosemys spinosa,
food items per week per kilogram animal.

The total amount of nutrients per MJ GE of the recommended diets for Cuora amboinensis and Heosemys spinosa are given in table 8.3.

Table 8.3 Total amount of nutrients per MJ GE of the recommended diets for Cuora amboinensis and Heosemys spinosa.
The compositions of the advised diets are an interpretation of the gathered requirements for these animals. If for any reason (such as availability, price or food refusal) the composition of the advised diet needs to be changed, the nutrient levels as given in table 8.3 can be used as a guideline. Nutrient levels should approach values as mentioned in table 8.3. However it is also advisable to reflect any changes with the dietary requirements as mentioned in tables 4.2, 4.3 and 4.4 of this report as these are the original base of the dietary advice.

Feeding practice

Amounts given in the advice are per week. It is recommended to spread this amount over a couple of days throughout the week, according to a schedule that is convenient to a given organisation. Daily feeding has proven not to be necessary, however to ensure animals can take in enough to meet their requirements feeding at least 3-4 times a week is likely to give satisfying results.
In literature Heosemys spinosa has been reported to be a picky feeder sometimes. It is therefore recommended to feed the advised diets in finely copped pieces thoroughly mixed up to prevent selective feeding. If this is done the mixture can be used for group-feeding or the feeding of significantly larger individuals by multiplying all amounts by the same number (roughly the total weight of all animals to be fed). Feeding large pieces will enable animals to feed selectively, optimal intake of all nutrients is than no longer assured.
Because energy demand is estimated and as shown also differs according to temperature and physiological status the recommended total amount given above is likely to be significantly different if tried in practice. However, since the mixture will contain nutrient levels in the right proportion to energy content an animal (eating to meet its energy requirements) will take in right amounts of all nutrients.

Feeding can best be done on dry land. Heosemys spinosa is a very terrestrial animal making it unsure whether it would feed when only offered food in the water. Furthermore, the need for a thoroughly mixed, and chopped up meal makes aquatic feeding impossible since it would generate enormous pollution. It is advisable to check whether animals (especially Cuora amboinensis) take in food on dry land as some may be used to aquatic feeding only. Finally it is recommended to offer all meals in a large flat bowl e.g. on a flat rock or board. Meals should be easy to reach but simply tossing food in the enclosure might lead to intestinal blockage due to Geophagy or Litophagy of enclosure substrate.

Further research

This study was done to further explore the preliminary advice that was given by EZNC. The results of this study are still a basic advice a lot of research still is wishful to increase knowledge on this theme and insure an optimal captive maintenance

Successfulness of advised diet
The diets advised above are based on theory and experience. If the advice is followed the physiological status of the animals should be monitored. After a year another questionnaire can be sent to zoos and private keepers that received this advice. Health status, reproduction and refusal of food items should be included in order to judge the successfulness of this advice. The advised diet has to be adapted to the experiences of the zoos and private keepers.
Study on faeces and gut content
Useful in further understanding the nutrition of these and other turtles is a study on the faeces and gut contents of in-situ <>Cuora amboinensis,
and Heosemys spinosa. Both faeces and gut contents can be obtained by close cooperation with field workers, or even by research at the food markets dealing with mentioned species. Because of slow digestive turnover times at lower temperatures animals destined for trade are still likely to contain parts of the last consumed meals and thus are a readily accessible source of data.

Digestive tract
No dissection results have been available at time of this study. However questionnaires have shown a rather high mortality rate and dissection has taken place on several individuals. Post mortem research needs to be more focussed on the physiology of the digestive tract, something that has not been described before. Data from such post mortems can give more insight in the nutritional requirements of these turtles.

Energy intake
The energy intake of the two species is something still very disputable. Close monitoring studies of energy intake and excretion through faeces is recommended to establish the energy requirements of these animals. Gained knowledge could be used to correct amounts advised in the previous paragraph.

In-situ lifestyle
In situ monitoring of the species Cuora amboinensis and Heosemys spinosa would increase the limited knowledge of the in-situ lifestyle of both species and with that the feeding behaviour and natural diet of the animals.

Sub-species of Cuora amboinensis
More research is recommended on the sub-species of Cuora amboinensis in captivity. It does not appear to be common practice to differentiate between the three subspecies while this is important in terms of conservation as biological diversity will be lost if interbreeding occurs.


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CITES, 01-04-2002

CITES, 13-06-2002

EAZA, 28-03-2002

E. Colijn, (r) 20-04-2001

ESF, 13-06-2002

ISIS, 02-05-2002


<b>Appendix I</b>

Information and primary targets of European Zoo Nutrition Centre (EZNC)

European Zoo Nutrition Centre
Ing. J. Nijboer
Dr. Ir. W.L. Jansen

In order to stimulate and to improve the exchange of European Zoo Nutrition information the European Zoo Nutrition Centre (EZNC) has started officially on January 11th 2002.

EZNC is established in the EAZA office in Amsterdam. EZNC will be responsible for the implementation of the plans made by the European Zoo Nutrition Research Group (EZNRG). Suggested targets:
  • Co-ordinating zoo nutrition research projects all over Europe

  • Initiate zoo nutrition projects

  • Set up a zoo nutrition literature database

  • Formulate diets

  • Zoo nutrition education

  • roduct development

  • Feed purchase optimisation

  • Support zoo nutritionists

EZNC will co-operate with national and international organisations and institutes to achieve the targets. EZNC will provide communication between the different participants. Besides that it will also co-ordinate the input of information, relationships between resources of information and find financial support and personnel to achieve it. EZNC will be staffed by Dr. Ir. Walter Jansen (Jagran Zoological Research & Development) and ing. Joeke Nijboer (Rotterdam zoo). Students of the Van Hall Institute (Leeuwarden, the Netherlands) will be stimulated to work for the centre.
EZNC will be financial supported during the first year through EAZA, Marwell Presevation Trust, Jagran ZR&D and Rotterdam Zoo.
Soon a web-site will be set up to inform you about the European zoo nutrition subjects.
Distribution of information and collecting information will be done by the EZNRG Forum. If you want to subscribe, send an e-mail to

A number of persons from several countries have already offered their support to EZNC. We thank them for their confidence and enthusiasm and will certainly use the expertise of all those persons to achieve our goals!

Our address is:
European Zoo Nutrition Centre
C/O Artis
P.O. Box 20164
1000 HP Amsterdam
The Netherlands
Tel : +31-20 52 00 750
Fax : +31-20 52 00 752
E-mail :

Dr. Ir. Walter Jansen
Ing. Joeke Nijboer

<b>Appendix II</b>

Preliminary advice given by EZNC at distribution of confiscated turtles, narrowed down to information relevant for the species Cuora amboinensis and Heosemys spinosa

Heosemys spinosa
Southeast Asian Spiny Turtle (Cogwheel Turtle, Spiny Hill Turtle)

Spiny turtles are mostly herbivorous by nature, although they will sometimes eat meat in captivity. It is best to feed them salads consisting of fruits (especially tomatoes), vegetables, and collard greens two to three times a week. A healthy salad for this species might consist of red lettuce, dandelion, tomato, blueberry, and cantaloupe chopped up together and lightly sprinkled with a supplement such as Rep-Cal. Chopped skinned mice or mouse pinkies may be fed to adults biweekly, but refrain from feeding meat to neonates and juveniles. Most neonates and juveniles prefer tomatoes over any other food items and tomatoes may be the best choice for getting finicky eaters to feed regularly. Vitamin supplements are not usually necessary if a mixed salad is offered. A calcium/phosphate supplement may be given to neonates and juveniles and a good diet could include Turtle Brittleâ to provide Vitamin D3.

Some specimens remain entirely herbivorous while other accept occasional earthworm or slug.

Cuora amboinensis
Malayan Box Turtle:

In diet, at least, the Malayan is somewhat like other box turtles--omnivorous. However, aquatic plants provide the main food source for C. amboinensis in the wild. Provide a variety of greens 'n veggies, some fruits, mushrooms and an occasional waxworm or cricket. "Gut loading," or feeding nutritional plant matter to the worms or crickets before offering them to the turtle, improves the quality of this food source. Use a good supplement, formulated for turtles, to assure proper nutrition. (Supplements are not needed daily if the animal is feeding well and is provided with an excellent variety.) Malayans prefer to feed in the water, if the water is warm enough. Aquatic plants and greens can be provided in the pond or aquarium at all times. Feeding in a sink or plastic tub away from the aquarium will make cleaning easier. Healthy, well-nourished turtles do not require large feedings on a daily basis. One or two substantial feedings per week should keep your turtle happy and active without risking overfeeding. It is a good idea to keep cuttlebone, or some other high calcium food, available all the time.

Refusal to eat:
This species tends to eat eagerly, even with less than optimum care. If your C. amboinensis -is not eating, it may be very ill. The first thing to try would be aquatic plants. If that fails, seek veterinary help. Some sick "ambys" will eat only live foods. They may be craving the extra protein. But an unwillingness to eat aquatic plants would be evidence of illness.

Suggested diets

We send you these two diets (1 herbivore and 1 carnivore) as a suggestion how to feed your animals. If you received sick animals, please contact your veterinarian.

Suggested Herbivore diet(tabel)

Suggested carnivore diet(tabel)