Dietary Requirements of Asian turtles
Preface
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
Summary
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 animals requirements.
Acknowledgements
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
Bodyweight.
Ca
Calcium.
Ca:P
Calcium : Phosphorus ratio.
CITES
The Convention on International Trade in Endangered Species of wild flora and fauna.
DM
Dry matter.
EAZA
European Association of Zoos and Aquaria.
ESF
European Studbook Foundation.
EZNC
European Zoo Nutrition Centre.
GE
Gross Energy.
IUCN
The world conservation union.
MBD
Metabolic Bone Disease.
NSV
Nederlandse Schildpadden Vereniging (Dutch Turtle/Tortoise Society).
P
Phosphorus.
USD
Ulcerative Shell Disease. Most commonly referred to as shell disease.
Introduction
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?
- 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?
- 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 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
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
<i>Cuora amboinensis</i> Status
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
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
<i>Heosemys spinosa</i> Status
Methods
Subject
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.
Process
- 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?
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?
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?
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
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.
Calcium
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
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
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
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.
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.
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
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 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
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.
- Calculating phosphorous demand /MJ GE from known calcium/MJ demand and Ca/P ratio:
- Calculating vitamin demand/ MJ GE from known mg/kg level:
Vitamin B1 = 4,4 mg/kg x 0,09266/ 0,367 = 1,11
In-situ diet
- What is known about the natural diet and feeding behaviour of Cuora amboinensis and Heosemys spinosa?
<i>Cuora amboinensis</i> Digestive system
<i>Cuora amboinensis</i> Ingredients and nutritional contents of the natural diet
<i>Cuora amboinensis</i> Feeding behaviour
<i>Heosemys spinosa</i> Digestive system
<i>Heosemys spinosa</i> Ingredients and nutritional contents of the natural diet
<i>Heosemys spinosa</i> Feeding behaviour
Comparison 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 turtles diets.
Digestive system
Ingredients and nutritional contents of the natural diet
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 digestibilitys 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
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
Energy
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)
Nutrients
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.
Fats
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.
Carbohydrates
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.
Fibre
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
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).
Phosphorous
Calculating back from Calcium/ Phosphorous ratios 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
Protein
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).
Fats
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).
Litophagy
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
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
- 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>
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>
Diets fed by Zoos and Private keepers
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?
Ingredients
Ingredients of diets fed to <i>Cuora amboinensis</i>
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>
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
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
Diets fed to <i>Cuora amboinensis</i>
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>
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
Energy and food intake <i>Cuora amboinensis</i>
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 3.3.4.2).
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>
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
- 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
- · 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 doesnt 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.
Discussion
General comments
Sub-species
Diet frequency
Sources
Assumptions of food items
Assumptions of supplementation
Accuracy of returned data
Species information
Temperature
Estimations
Diets
<i>Cuora amboinensis</i>
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>
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.
Conclusions
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.
Recommendations
- · 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
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
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
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.
References
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Appendices
<b>Appendix I</b>
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 EZNRG_Forum-subscribe@yahoogroups.com
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 : EZNC@nvdzoos.nl
Dr. Ir. Walter Jansen
Ing. Joeke Nijboer
<b>Appendix II</b>
Heosemys spinosa
Southeast Asian Spiny Turtle (Cogwheel Turtle, Spiny Hill Turtle)
Feeding:
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:
Feeding
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)