Freshwater turtle nutrition - A review of scientific and practical knowledge

Abstract

Freshwater turtles are commonly kept in captivity as pets, bred in zoos for conservation programs, and commercially farmed for pet markets and human consumption, but their nutrition can be challenging. However, based on practical experience, two main strategies may be identified: the use of non-calculated raw diets and the use of balanced commercial feeds. Raw diets are based on fresh, frozen and dried components including invertebrates, fish, rodents and plant matter; they imitate the variety of foods that are accessible to turtles in the wild and are considered most useful when turtles are bred for reintroduction into their natural habitat as part of conservation programs. Granulated, pelleted or extruded commercial diets are frequently used for farmed and pet turtles; they contain animal- and plant-based materials supplemented with vitamin and mineral premixes and calculated to reach the nutrient levels assumed to be optimal for most species. Until more species-specific information on the nutritional requirements of freshwater turtles is available, the Chinese softshell turtle (Pelodiscus sinensis), a commonly commercially farmed species for human consumption, may be used as a reference for other species in terms of suggested nutrients levels. Based on experimental data, the most important nutrients and their levels that should be included in turtle diets are crude protein (39.0 - 46.5%), crude fat (8.8%), Ca (5.7%), P (3.0%), methionine (1.03%), and cysteine (0.25%). The diet composition for freshwater turtles should be based on scientific knowledge and practical experience, so this paper aimed to present and discuss the available data on the nutrient requirements of turtles and the characteristics of the feed materials used in their nutrition.

Full text

Ann. Anim. Sci., Vol. 18, No. 1 (2018) 17–37 DOI: 10.1515/aoas-2017-0025
FRESHWATER TURTLE NUTRITION – A REVIEW OF SCIENTIFIC
AND PRACTICAL KNOWLEDGE* *
Mateusz Rawski1,2♦, Christoph Mans3, Bartosz Kierończyk1
, Sylwester Świątkiewicz4, Aneta Barc1,
Damian Józeak1
1Department of Animal Nutrition and Feed Management, Poznań University of Life Sciences,
Wołyńska 33, 60-637 Poznań, Poland
2Division of Inland Fisheries and Aquaculture, Institute of Zoology,
Poznań University of Life Sciences, Wojska Polskiego 71C, 60-625 Poznań, Poland
3Department of Surgical Sciences, School of Veterinary Medicine, University of Wisconsin-Madison,
2015 Linden Drive, WI 53706, Madison, United States of America
4Department of Nutrition Physiology, National Research Institute of Animal Production,
Balice n. Kraków, Poland
♦Corresponding author: mrawski@up.poznan.pl
Abstract
Freshwater turtles are commonly kept in captivity as pets, bred in zoos for conservation programs,
and commercially farmed for pet markets and human consumption, but their nutrition can be
challenging. However, based on practical experience, two main strategies may be identied: the
use of non-calculated raw diets and the use of balanced commercial feeds. Raw diets are based on
fresh, frozen and dried components including invertebrates, sh, rodents and plant matter; they
imitate the variety of foods that are accessible to turtles in the wild and are considered most useful
when turtles are bred for reintroduction into their natural habitat as part of conservation pro-
grams. Granulated, pelleted or extruded commercial diets are frequently used for farmed and pet
turtles; they contain animal- and plant-based materials supplemented with vitamin and mineral
premixes and calculated to reach the nutrient levels assumed to be optimal for most species. Until
more species-specic information on the nutritional requirements of freshwater turtles is avail-
able, the Chinese softshell turtle (Pelodiscus sinensis), a commonly commercially farmed species
for human consumption, may be used as a reference for other species in terms of suggested nutri-
ent levels. Based on experimental data, the most important nutrients and their levels that should
be included in turtle diets are crude protein (39.0–46.5%), crude fat (8.8%), Ca (5.7%), P (3.0%),
methionine (1.03%), and cysteine (0.25%). The diet composition for freshwater turtles should be
based on scientic knowledge and practical experience, so this paper aimed to present and discuss
the available data on the nutrient requirements of turtles and the characteristics of the feed mate-
rials used in their nutrition.
Key words: freshwater turtles, turtle nutrition, nutrient requirements, metabolic diseases, Pelo-
discus sinensis
* The current study was supported by the grant NCN PRELUDIUM: UMO-2013/11/N/NZ9/04624,
nanced by National Science Centre (Poland).
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Freshwater turtles are widely distributed in almost all types of aquatic habitats
(Bonin et al., 2006), so their diets and feeding strategies in the wild vary substan-
tially. However, most are opportunistic carnivores or omnivores, consuming inver-
tebrates, small vertebrates, and aquatic vegetation (Bouchard and Bjorndal, 2006;
Gibbons, 1990; Luiselli et al., 2011; Ottonello et al., 2005; Rhodin et al., 2008;
Spencer et al., 1998). The wide spectrum of feeding strategies among freshwater
turtles and their slow metabolism may explain their high tolerance for unbalanced
diets, but their longevity and the energetic expense required for shell mineralization
make them vulnerable to nutritional deciencies in captivity (McWilliams, 2005).
Moreover, the nutrient requirements for most species, especially those not routinely
used in large-scale turtle farming, are poorly documented. It should be highlighted
that the nutritional needs of freshwater turtles are affected by numerous factors such
as the species, environmental conditions, digestion and assimilation efciency, sex,
age, health status and history of specimen (Figure 1), but diet composition should be
both species-specic and suitable for raising turtles in captivity. Therefore, diets used
in commercial turtle farming may not be adequate for non-commercial purposes in
terms of feed ingredients or physical form of the feed which are optimized in terms
of feed utilization and economic results. However, the available data on the nutri-
tional requirements of turtle species that are commonly raised commercially (i.e., the
Chinese softshell turtle (Pelodiscus sinensis) may be an important source of general
information for other turtle species kept as pets, in zoological institutions or as part
of conservation programs. This paper aimed to present and discuss the available sci-
entic data on the nutrient requirements of turtles and the characteristics of the feed
materials used in their nutrition.
Figure 1. Extrinsic and intrinsic factors and their interactions that affect the nutritional requirements of
turtles (Bouchard, 2004; Gibbons, 1990; Luiselli et al., 2011; McCauley and Bjorndal, 1999; Seebacher
et al., 2004; Spencer et al., 1998; Zhang et al., 2009)
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Freshwater turtle nutrition – a review 19
Gastrointestinal tract anatomy and physiology of freshwater turtles
Turtles are monogastric animals, and their gastrointestinal tract (GIT) begins with
an oral cavity that has no lips or teeth (Mitchell and Tully, 2009). Therefore, they
are unable to chew their food but instead swallow entire prey or large bites. In some
species, feed cutting and shredding is performed with the use of a beak-like keratin
layer on the upper and lower jaw (rhamphotheca) as well as the claws. The shape and
function of the rhamphotheca is very similar among omnivorous turtle species, such
as pond turtles (Emydidae), but in highly specialized turtles, the structure reects
their feeding habits. The rhamphotheca may be very well developed as in the alliga-
tor snapping turtle (Macrochelys temminckii), which has powerful jaws, or reduced
as in the matamata turtle (Chelus mbriata), which has a limited bite force (Lemell et
al., 2010). Due to the large feed intake by a turtle during a single meal, the pharynx,
esophagus and stomach are highly exible. In the stomach, the low pH and enzy-
matic activity starts the digestion process. The stomach is curved to the left, shorter
and wider than the esophagus, and its mucosal surface is divided into the proper gas-
tric and cardiac glandular mucosa regions (Stevens and Hume, 1998). There are two
kinds of gastric glands in the stomach, peptic cells and oxyntic cells, which indicates
that turtles are well adapted for omnivory (Rahman and Sharma, 2014).
The small intestine is the longest organ in the turtle GIT (Figure 2), but the duo-
denum, jejunum and ileum are not well distinguished and difcult to identify (Rah-
man and Sharma, 2014). The length and capacity of the intestines is diet-dependent
and may vary signicantly between species and different diets (Bouchard, 2004).
The mucosa of the small intestine is composed of a single columnar epithelium,
and the lining of the intestinal villi includes three types of cells: simple columnar
cells, goblet cells and endocrine cells (McArthur et al., 2008; Rahman and Sharma,
2014; Wurth and Musacchia, 1964). The large intestine seems to be a site for wa-
ter absorption, microbial fermentation and short-chain fatty acid (SCFA) produc-
tion (Bouchard, 2004); its proximal part is the caecal extension of the colonic wall
(Bouchard, 2004; McArthur et al., 2008). The colon is typically divided into three
parts: ascending, transverse and descending. The reptile GIT ends with the cloaca,
the site where the terminal parts of the GIT, urinary and reproductive tracts join,
which is subdivided into the coprodeum, urodeum and proctodeum (McArthur et al.,
2008; Mitchell and Tully, 2009). Turtle saliva does not contain digestive enzymes,
which are instead secreted by the stomach, pancreas and intestines. Chelonian stom-
achs secrete amylase, pepsin, trypsin, chitinase and chitobiase; the pancreas secretes
amylase, ribonuclease, trypsin, chymotrypsin, carboxypeptidase A and chitinase; and
the intestines secrete proteinase, invertase, amylase, maltase, chitobiase, trehalase,
isomaltase and sucrase (McArthur et al., 2008). Protease and amylase are considered
the two main digestive enzymes in the turtle GIT (Sun et al., 2007), and the opti-
mal conditions for their specic activities vary among GIT segments. In the pond
slider (Trachemys scripta), pancreatic protease shows the highest activity (36 U/mg
of protein), and in the stomach, maximal protease activity (24 U/mg of protein) was
recorded at pH 2.5 and 40°C. In contrast, amylase had the highest activity (12 U/mg
of protein) in the anterior intestine under neutral conditions (Sun et al., 2007). The
liver is, to some extent, divided into triangular lobes (Rahman and Sharma, 2014),
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M. Rawski et al.
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and it plays a key role in vitamin D3 synthesis and storage and the transformations of
lipids, proteins and glycogen. Another important GIT gland is the pancreas, which
is situated along the proximal segment of the duodenum (McArthur et al., 2008).
Because turtles are ectothermic, their metabolic rate and digestion mainly depends
on the temperature of the environment and external heat sources.
For most turtle species, feed intake and enzyme secretion and activity, as well
as the absorptive capacity of the intestinal mucosa, are highest and feed passage
is shortest in the preferred optimal temperature zone (POTZ), above which these
parameters decrease (Figure 3) (McArthur et al., 2008; Seebacher et al., 2004; Sun
et al., 2007). In most species, this zone is between 25 and 34°C (Table 1) (Gibbons,
1990; Mitchell and Tully, 2009), and turtles can even reach their POTZ in lower air
temperatures through basking behavior. However, there are exceptions, especially
in species that naturally inhabit cold mountain creeks such as the big-headed turtle
(Platysternon megacephalum), whose POTZ is 22–25°C (Jianwei et al., 2013; Zhang
et al., 2009). Due to the above-mentioned behavioral mechanism and the lack of
energetic expenses for heat production, the average reptile energy expenditure is
only 25–35% that of mammals (Mader, 2005). In reptiles, energy utilization mainly
depends on feeding strategy and diet composition. Carbohydrates are a source of
75% of the metabolizable energy for herbivorous and 50% for omnivorous reptilian
species. In carnivores, carbohydrates provide only 5% of the dietary matabolizable
energy, while protein provides 50% and fat 45% (Hand et al., 2000; Mader, 2005).
The function of the GIT microbiota has not been well studied in reptiles, but it seems
to play an important role in the secretion of bacterial enzymes and the immuno-
logical response. Similar to other animals, microbial homeostasis in reptiles may
improve gut health, while disturbances in composition may lead to depressed growth
and subclinical and clinical infections (Lei and Yaohong, 2010; Zhang et al., 2014;
Rawski et al., 2016). The microbial GIT symbionts in turtles signicantly support
plant matter digestion and produce SCFAs, which may be an important energy source
for omnivorous or herbivorous animals (Bouchard and Bjorndal, 2005). Based on its
SCFAs concentrations, the anterior large intestine should be considered the main site
of microbial fermentation of carbohydrates of plant origin in T. scripta. In the Florida
red-bellied cooter (Pseudemys nelsoni), microbial fermentation may also occur in the
small intestine (Bjorndal and Bolten, 1990; Bouchard and Bjorndal, 2005). It has been
suggested that the importance of SCFAs as energy source increases with an increase
in the amount of plant matter in the turtle diet, but it may also depend on fermentation
capacity (Bouchard, 2004; Bouchard and Bjorndal, 2005). The pattern of the relative
proportions of SCFAs in T. scripta was described as acetate > propionate > butyrate >
valerate (Bouchard and Bjorndal, 2005). During development, several species undergo
an ontogenetic diet shift from carnivorous hatchlings to omnivorous adults (Bouchard,
2004; Bouchard and Bjorndal, 2006; McCauley and Bjorndal, 1999); this occurs in
Emydidae and Chelidae as well as in other reptile species (Bouchard, 2004; Bouchard
and Bjorndal, 2005, 2006; Kennett and Tory, 1996). Both juvenile and adult turtles
digest animal and plant matter, but animal matter has a higher digestibility compared
to plant matter in juvenile T. scripta (97.2% vs. 89.4%) and results in greater growth
(0.2 vs. 0.6 g/week). In adults, plant matter is more digestible (Bouchard and Bjorndal,
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Freshwater turtle nutrition – a review 21
2006). However, in most cases, adult turtles do not become predominately herbivo-
rous; in T. scripta, the animal to plant matter ratio in the diet was recorded as 77:23
(Gibbons, 1990). This diet composition may by highly nutritive for GIT microbiota,
and the nutrients supplied from animal matter may support plant matter microbial
fermentation (Bjorndal, 1991). It is assumed that adult turtles can meet their meta-
bolic demands on a plant-based diet, which would be insufcient to meet juvenile
growth requirements due to the low concentration of protein and energy (Bouchard
and Bjorndal, 2006).
Figure 2. Gastrointestinal tract (GIT) segment proportions (% of the entire GIT length) in selected turtle
species. Data for Trachemys scripta (n=40, 1 year old non-sexed specimens), Sternotherus odoratus
(n=36, 1 year old non-sexed specimens) and Apalone ferox (n=40, 1 year old non-sexed specimens),
M. Rawski unpublished data. *Data for Pangshura tenoria (n=20, adult specimens, both sexes) based on
the literature (Rahman and Sharma, 2014)
*POTZ – preferred optimal temperature zone.
Figure 3. Dependence of turtle nutritional performance (including feed intake, digestion efciency,
enzyme secretion, digesta turnover) on environmental temperature (Seebacher et al., 2004; Zhang et al., 2009)
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Table 1. A summary of published reports on body temperature in free-ranging turtles and the
preferred body temperature
Species
Field
body temperature
(ºC)
Preferred
body temperature
(ºC)
References
Chelydra serpentina 22.7 (SD=2.8) 27–30 (hatchlings)
27–33 (yearlings)
Brown et al., 1990; Bury et
al., 2000
Macroclemys
temmincki
19.96 (12.21–27.76) NA*Fitzgerald and Nelson, 2011
Platysternon
megacephalum
19.3–22.2 25.3 (juveniles) Jianwei et al., 2013
Chrysemys picta 25–32
(basking temperature)
34 (juveniles) Grayson and Dorcas, 2004;
Tamplin and Cyr, 2011
Glyptemys insculpta 23.2 (SD=3.9)
5–30 (basking temperature)
30 (juveniles) Ernst, 1986; Tamplin, 2009
Pseudemys nelsoni NA*30 (hatchlings) Nebeker and Bury, 2000
Terrapene ornata 28.0 (15.3–35.3) 28.3 (fasted)
29.8 (recently fed)
Gatten Jr, 1974; Legler, 1960
Trachemys scripta 27.2–38.0 30 (hatchlings) Bury et al., 2000; Gibbons,
1990
Ocadia sinensis NA*25.4–29.2 (juveniles) Pan et al., 2002
Apalone spinifera NA*30 (juveniles) Feltz and Tamplin, 2007
Pelodiscus sinensis NA*30.3 (juveniles) Sun et al., 2002
Chelodina longicollis 20.2–24.4 NA*Seebacher et al., 2004
*NA – data not available.
Nutritional requirements
In contrast to domesticated animals, no standardized nutritional requirements are
available for most freshwater turtles, which makes the provisioning of a proper diet
in captivity challenging. There are general rules for feeding different age groups of
turtle species that inhabit a wide range of ecological niches, but it should be em-
phasized that in the case of highly specialized species, such as the matamata (Che-
lus mbriata), only species-specic diets that reect their feeding ecology in the
wild should be provided. Nutritional requirements are best known for commonly
farmed freshwater turtle species, and they may be used as a reference and by analogy
for other turtles until better information is published. The Chinese softshell turtle
(Pelodiscus sinensis) is the best-known species due to large-scale farming in Asia,
and many studies on its nutritional requirements have been published (the results
are summarized in Table 2). In the rst days after hatching, turtles may not con-
sume any food due to yolk sac absorption, which satises some of the nutritional
needs of hatchlings (Mitchell and Tully, 2009). The hatchlings of most freshwa-
ter turtle species are almost strictly carnivorous (Bouchard, 2004; Bouchard and
Bjorndal, 2006), so their growth performance is correlated with the concentration
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Freshwater turtle nutrition – a review 23
of crude protein (CP) in the diet (Gibbons, 1990). The optimal CP level for young
Pelodiscus sinensis is assumed to be as high as 39–46.5% (Jia et al., 2005; Nu-
angsaeng and Boonyaratapalin, 2001; Zhou et al., 2013) and is likely dependent on
the energy content of the diet (Nuangsaeng and Boonyaratapalin, 2001). A study of
P. sinensis suggests that the optimal CP to energy ratio of the diet should be at the
level of 32–36 mg/kJ–1 (Zhou et al., 2013). This ratio should be considered an impor-
tant factor in diet suitability; when the ratio is too low, it may not only limit growth
but feed intake as well. Crude protein characteristics, such as the quantity, ratios and
bioavailability of essential amino acids, are key factors in animal nutrition (Ei and
Kavas, 1996). Methionine and cysteine seem to be limiting amino acids in P. sinensis
with estimated optimal levels of 1.03% and 0.25% of the diet, respectively (Huang
and Lin, 2002). No experimental information is available for lysine. Exogenous tau-
rine also seems to be essential and should constitute 0.9% of the diet, especially
when CP of plant origin is used (Hou et al., 2013). The CP concentration in captive
turtle diets may be lowered when the animals reach sexual maturity and their growth
rate decreases, and plant matter should be provided to achieve this goal. A nutritional
experiment using the scorpion mud turtle (Kinosternon scorpioides) indicated that
slow-growing adults may be fed CP at a lower level than young turtles (26%), but
in the case of breeding stock females, diets containing 61–66% animal-derived CP
increased laying performance and egg quality compared to 26% dietary CP (da Costa
Araújo et al., 2013). Furthermore, in the case of slow-growing, non-breeding stock
adult males or females, the balance of protein and energy should be only slightly
above zero to avoid obesity (Rawski and Józeak, 2014).
Nutritional recommendations for P. sinensis diets are optimized to maintain high
growth performance, so when turtles are not maintained under commercial farming
conditions, energy and protein concentrations may be lowered to prevent too-rapid
growth and poor skeletal system development. Due to the low energetic expenses of
turtles and the high availability of feed in captivity, no additional source of dietary
fat is needed in most cases. However, in fast-growing P. sinensis, the optimal fat con-
tent in the diet is estimated to be 8.8%, and there is no apparent effect of fat source
on growth performance (Lin and Huang, 2007). Turtles probably have the highest
skeletal mass to body weight ratio among all vertebrates. Calcium and phosphorus
should be given at a ratio of approximately 2:1, i.e., 5.7% and 3.0% of the diet, re-
spectively, according to studies of P. sinensis (Huang et al., 2003); a lower Ca:P ratio
may cause shell malformations or lower growth rates. Other minerals such as Mg,
Fe, Zn and Cu also seem to be important for turtle metabolism and shell mineraliza-
tion (Chen et al., 2014; Chu et al., 2007; Huang et al., 2003; Huang et al., 2010; Wu
and Huang, 2008). Vitamins are a group of complex organic compounds that are
present in small amounts in plant and animal matter. Their ingestion is essential for
normal metabolism, and deciencies can lead to various diseases (McDowell, 1989).
Vitamin C has been shown to have an important role in the ability of turtles to with-
stand stress (Zhou et al., 2002). The diet of P. sinensis should contain 2500 mg/kg of
vitamin C and 88 IU/kg of vitamin E (Huang and Lin, 2004; Zhou et al., 2002). For
vitamin A, 2000–8000 IU/kg of the diet on a dry matter basis seems to be adequate
(Mader, 2005), but this vitamin may be synthesized by turtles using β-carotene, of
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M. Rawski et al.
24
which 50–90 mg/kg should be provided in the P. sinensis diet (Chen and Huang,
2011). In contrast, lutein and canthaxanthin may be equally or more effective forms
of provitamin A in reptiles, which may selectively absorb carotenoids (Raila et al.,
2002). Vitamin D3 synthesis occurs in reptilian skin and is stimulated by UVB radia-
tion; in carnivorous and omnivorous species, dietary sources of this vitamin seem
to play an important role (Hoby et al., 2010). However, despite being the key for
shell mineralization, the vitamin D3 requirements of turtles are still poorly known
(McArthur et al., 2008).
Table 2. Summary of the published reports on the nutritional requirements of young Chinese softshell
turtles (Pelodiscus sinensis)
Item Unit Optimal level References
Protein to energy ratio mg/kj–1 32–36 Zhou et al., 2013
Protein % 39.0–46.5 Jia et al., 2005; Nuangsaeng and
Boonyaratapalin, 2001; Xie et al.,
2012; Zhou et al., 2013
Fat % 8.8 Huang et al., 2005
Calcium % 5.7 Huang et al., 2003
Phosphorus % 3.0 Huang et al., 2003
Methionine % 1.03 Huang and Lin, 2002
Methionine % of protein 2.48 Huang and Lin, 2002
Cysteine % 0.25 Huang and Lin, 2002
Cysteine % of protein 0.60 Huang and Lin, 2002
Taurine % 0.90 Hou et al., 2013
Magnesium mg/kg 970–980
650–750
(phytic acid free diet)
Chen et al., 2014
Iron mg/kg 266–325 Chu et al., 2007
Zinc mg/kg 35–46 Huang et al., 2010
Copper mg/kg 4–5 Wu and Huang, 2008
β-carotene mg/kg 49–89 Chen and Huang, 2011
Vitamin C mg/kg 2500–5000 Zhou et al., 2002
Vitamin A mg/kg 2.58–3.84 Chen and Huang, 2014
Vitamin E IU/kg–1 40 Huang and Lin, 2004
Feeding strategies in captivity
Due to the practical experience of zoos and breeders, two main strategies may
be distinguished for providing adequate nutrition for turtles in captivity. The rst is
the use of non-calculated, raw diets based on unprocessed or minimally processed
components, such as live, fresh, dried or frozen food items; the main aim is to imitate
the natural diets of freshwater turtles with undetermined nutritional requirements
(examples of natural diet compositions are shown in Table 3). The second strategy
is based on commercial diets, which may be considered suitable for the most com-
monly kept turtle species (in the Emydidae and Pelomedusidae families). Another
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Freshwater turtle nutrition – a review 25
important issue is feeding frequency and quantity, which are restricted under natural
conditions by prey availability, season and predation success. These factors lead to
periodic starvation that results in the use of body energy reserves, which tends to
result in lower growth and breeding performance than would have been possible
based on the genetic potential of the animals. This is in contrast to the situation in
captivity, where regular access to an appropriate diet will lead to the fulllment of
the genetic potential. However, it should be emphasized that food restriction seems
to have health benets and promotes longevity in animals (Lawler et al., 2005). Ad-
ditionally, high nutrient and energy availability may result in accelerated growth and
poor bone mineralization in turtles, as observed in fast-growing poultry and other
animals (Julian, 1998), and it may also cause obesity in adult animals, including
turtles (Mader, 2005; Mitchell and Tully, 2009; Rawski and Józeak, 2014). Turtles
can achieve high feed intake; T. scripta elegans may consume up to 12% of its body
weight during one meal (Rawski, unpublished data). Under experimental conditions,
4% of body weight was reported to be an optimal meal size for suitable growth per-
formance in P. sinensis since higher feed intake may decrease nutrient digestibility
(Lei, 2006). In contrast, commercial feed producers frequently advise that turtles be
fed ad libitum or during restricted time periods, sometimes even more than once dai-
ly. However, in the opinion of this author, restricting the amount, not feeding time,
of commercial feeds containing a high amount of dry matter may be more effective
at preventing overfeeding, excessive growth and obesity.
Table 3. Diet composition of selected turtle species in nature
Species Diet composition Sampling method References
Trachemys
scripta
Animal matter: Gastropoda: Physidae,
Insecta: Coleoptera, Diptera, Hymenoptera,
Odonata: Anisoptera, Zygoptera,
Orthoptera: Locustidae
Fish, unknown claws and bones, craysh, shrimps
Plant matter: Algae, Bacopa caroliniana, Brasenia schre-
beri, Najas guadelupensis, Nymphaea odorata, Potamo-
geton spp., Sagitaria spp., Utricularia spp., Lemna spp.
stomach ushing Gibbons,
1990
Emys
orbicularis
Gastropoda: Bithyniidae, Lymnaeidae, Physidae, Pla-
norbidae,
Arachnida: Acarina, Araneae,
Crustacea: Conchostraca, Decapoda
Insecta: Coleoptera, Diptera, Heteroptera, Hymenop-
tera, Odonata Trichoptera
Vertebrata and plant matter
fecal samples Ottonello et
al., 2005
Emydura
macquarii
Arthropoda: Arachnida, Decapoda
Insecta: Hemiptera, Coleoptera, Diptera, Trichoptera
Hymenoptera
Vertebrates, lamentous algae, plant detritus
stomach content Spencer et
al., 1998
Pelomedusa
subrufa
Rodents, Birds, Lizards, Snakes, Tadpoles, Frogs, Fish,
Gastropoda, Bivalvia, Anellida, Arachnida, Chilo-
poa, Crustacea, Odonata larvae, Rhynochota, Coleop-
tera adult, Coleoptera larvae, plant matter, fungi
stomach ushing,
fecal samples
Luiselli et
al., 2011
Chelodina
mccordi
Fish, tadpoles, insects, freshwater gastropods, water
weeds
observations Rhodin et al.,
2008
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Table 4. Nutritional composition of a whole prey used in captive turtle diets
Prey species Notes DM*CP*EE*Ash Ca*P*References
% as feed % on a DM basis
Blood worm - 9.9 53 9.7 12 0.38 0.85 Bernard et al., 1997
Black soldier y Larvae 30 38–60 9–26 3–17 0.30–0.80 0.90–2.4 Józeak et al., 2016
American cockroach - 39 54 28 3.3 0.20 0.50 Bernard et al., 1997
American cockroach Nymph 37 54–73 18–26 4.6–5.4 0.02 0.06–0.07 Józeak et al., 2016
Domestic cricket Imago 27–38 40–68 14–44 2.7–5.7 0.14 0.99 Bernard et al., 1997; Mader, 2005
Domestic cricket Larvae 33 40–50 10 9.1 0.1–0.2 0.8 Mader, 2005
Domestic cricket Imago, high Ca diet 30 65 13 9.8 0.90 0.92 Bernard et al., 1997
Jamaican eld cricket Imago 31 56 24 6.4 0.80 0.99 Józeak et al., 2016
Earthworm - 20 62 18 5.0 1.7 0.90 Bernard et al., 1997; Mader, 2005
Night crawler Wild 15–26 31–81 6–13 9–46 0.97–1.5 0.79–0.96 Bernard et al., 1997; Mader, 2005
Night crawler Commercial 16–24 50–81 11–13 25 1.2 0.86 Mader, 2005
Mealworm Larvae 38–43 53 31–60 3.0–7.0 0.04–0.12 0.83–1.4 Bernard et al., 1997; Mader, 2005
Superworm Larvae 41–43 40–50 41–44 2.9–3.5 0.03–0.12 0.6–0.8 Mader, 2005
Tubifex worm - 12 46 15 6.9 0.19 0.73 Bernard et al., 1997
Wax moth Larvae 34 42 46 2.7 0.11 0.62 Bernard et al., 1997
Wax moth Larvae, high Ca diet 40 NA†NA†2.5 0.50 0.33 Bernard et al., 1997
Domestic mouse Neonatal, <3 g 19–26 51–64 17–34 8.0–9.7 1.2–3.5 1.6 Crissey et al., 1999; Dierenfeld et
al., 2002; Douglas et al., 1994
Domestic mouse Juvenile, 3–10 g 18–29 44–59 24–30 8.5–10 1.5–3.0 1.4 Crissey et al., 1999; Dierenfeld et
al., 2002; Douglas et al., 1994
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Freshwater turtle nutrition – a review 27
Domestic mouse Adult or > 10 g 33 56 24 11-12 2.6-3.0 1.7–1.9 Clum et al., 1996; Crissey et al.,
1999; Dierenfeld et al., 2002;
Douglas et al., 1994
Domestic rat Neonatal, <10 g 21 65 16 12 1.9 NA†Dierenfeld et al., 2002; Douglas et
al., 1994
Domestic rat Juvenile, 10–50 g 23–30 58–60 24–27 12–15 2.1 NA†Dierenfeld et al., 2002; Douglas et
al., 1994
Domestic rat Adult or > 50 g 34 56 12 9.8 2.6 1.72 Clum et al., 1996; Dierenfeld et al.,
2002; Douglas et al., 1994
Chicken One-day-old 26 65 22 6.4 1.7 1.2 Dierenfeld et al., 2002
European smelt Dried 91 47 34 11 NA†NA†Declared by producer (Katrinex,
Poland)
*Abbreviations: DM – dry matter, CP – crude protein, EE – ether extract (crude fat), Ca – calcium, P – phosphorus, NA – data not available.
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M. Rawski et al.
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Raw diets
Raw diets are considered most suitable for turtles designated for reintroduction
into the wild as well as for those used as breeding stocks in conservation programs.
The diets should be as similar as possible to the variety of food resources accessible
to specic turtle species in their natural environment, including live prey, and in most
cases, these diets are based on invertebrates, insects and their larvae, as well as small
vertebrates to maintain foraging and hunting abilities of animals at optimal level.
Many turtle breeders and zoos use gelatin-based diets (puddings) that fall some-
where between raw and commercial diets. These diets are multi-ingredient mixtures
solidied by gelatin and represent the easiest way to maintain a diverse diet based
on fresh and frozen ingredients. The main advantage of these diets is the possibility
for modifying recipes according to changes in scientic knowledge, experience and
the available components. All raw components should be used fresh or after a sin-
gle freezing; prolonged storage or refreezing may promote microbial contamination
and nutrient degradation, which can result in negative side effects for the animals.
Gelatin-based diets should be offered at a temperature similar to that of the turtles’
environment and not frozen. If raw diets are aimed at imitating natural ones, inverte-
brates, sh, rodents and aquatic plants should be used. The nutritional values of ma-
terials of animal origin that are commonly used in turtle nutrition are given in Tables
4 and 5. It should be suggested that even in the case of raw, nature imitating diets
use, their nutritive value should be calculated and at the diet composition optimized
according to current knowledge about nutritional requirements of turtles.
Table 5. Nutritional composition of commercial turtle feeds based on producers declarations
Nutrient (%)
Nonspecic feeds1Age specic feeds2
all
turtles hatchling growth
formula
adult
maintenance
Crude protein (min) 38 39 35 25
Fat (min) 7.4 10 5 5
Fiber (max) 3.4 358
Ca (min) 2.2 ND3ND3ND3
P (min) 1.2 1 1 1
1Based on average of declared nutritional values of 15 commercial feeds recommended by producers as for-
mulations for all turtles.
2 Based on declared nutritional values of feeds recommended by producer as age specic formulations.
3 ND – no declaration.
Invertebrates
Insects are a rich source of high-quality protein, essential amino acids and other
nutrients. Additionally, they have short life cycles and are easy to produce and handle
(Józeak et al., 2016; Ramos-Elorduy et al., 2002). Due to a high amount of inver-
tebrates in the natural diets of many turtle species (Table 3), insects are an important
dietary component in captivity, but the high fat content in insect larvae, e.g., meal
worms (Tenebrio molitor) or wax worms (Pyralidae), may lead to excessive energy
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Freshwater turtle nutrition – a review 29
intake. Chitin is the main component of insect exoskeletons, and it seems to be well
digested by chitinases and chitobiases produced by the stomach and pancreas in tur-
tles (McArthur et al., 2008). An important disadvantage of feeder insects is that their
Ca:P ratio is less than optimal (2:1), and most contain low amounts of vitamin A and
D3. Therefore, supplementation of additional Ca and vitamin A and D3 is required.
Feeding insects a vitamin-and-mineral-rich diet shortly before feeding them to tur-
tles, which is also known as “gut-loading,” will improve their nutritional content
(Finke, 2003). Earthworms and night crawlers are also suitable turtle feed; they have
high mineral contents because of the high volume of soil in their guts (Bernard et al.,
1997). Similarly, a variety of shellsh may also be used due to their high nutritive
value, but negative effects may result from the long-term use of shellsh-based diets
due to the high concentrations of environmental pollutants in shellsh, especially
heavy metals (Sivaperumal et al., 2007).
Fish
Fish are a natural and valuable component of captive turtle diets. They contain,
on average, 15–20% high-quality protein that is rich in essential amino acids, i.e.,
lysine, methionine and cysteine. Moreover, sh are a good source of vitamins A, B
complex and D3 as well as minerals, such as Ca, P, Fe, and S, and long-chain polyun-
saturated fatty acids (Tacon and Metian, 2013). Whole small sh should be fed fre-
quently to most freshwater turtles and should be the main diet component for Chelus
mbriata and other piscivorous species. The presence of live small sh (Poeciliidae
or Danio spp.) in the turtle tank may serve as a food source but also stimulate turtle
foraging behavior. However, when a sh-based diet is used, frequent use of sh in
the Cyprinidae family should be avoided due to their high amounts of thiaminase,
a B1 antivitamin (Mader, 2005).
Mammals and birds
For many years, the main component of captive turtle diets was animal matter
derived from commercially raised domestic mammals or birds, which do not account
for a signicant proportion of natural freshwater turtle diets. However, whole car-
casses (e.g., mice and rats or quails and chicks) are frequently used in captive turtle
feeding. The skeletons and GIT contents of vertebrates provide valuable vitamins and
minerals (Hand et al., 2000), and fur and feathers mechanically stimulate the GIT,
similar to the function of the ber in plant matter. Among the most commonly used
rodents, adult mice seem to be most suitable for freshwater turtles due to their high
mineral content and adequate Ca:P ratio (Mader, 2005). In contrast, lleted meat,
an excellent protein source, should not be fed as one of the main diet components
because of its low content of minerals and vitamins. If the abovementioned feeds,
such as insects, whole sh or rodents, are not available or they are refused by the
turtles, internal organs, particularly the liver and kidneys, are good alternatives due
to their high protein quality and high concentrations of fat-soluble vitamins (Acker
et al., 1959). However, care should be taken not to feed raw liver in large quanti-
ties since hypervitaminosis A, which is often fatal, can develop (Mans and Braun,
2014).
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M. Rawski et al.
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Plant matter
To simulate their natural diet, most adult freshwater turtles should be provided
with various amounts of plant matter. In captivity, aquatic plants such as duckweed
(Lemna spp.), pondweed (Elodea spp.), and hornwort (Ceratophyllum spp.) are fre-
quently used. Algae such as Spirulina spp. are also used in commercial sh and turtle
diets, and they are also available in a dried form and may be used as a separate feed
component. Aquatic plants may be permanently present in turtle tanks and be ingest-
ed between main meals. For some tropical and subtropical turtle species, fruits may
also be used, but in the case of T. scripta elegans, we observed digestive disturbances
after feeding fruits, such as bananas (Rawski, unpublished data).
Commercial diets
Most commercial diets are extruded or hot pelleted and are based on animal and
plant materials with dry matter contents close to 90%. The declared average nutri-
tional values of various commercial diets are presented in Table 6, and in many of
them, the Ca:P ratio is close to 2:1. However, the levels of these nutrients are low
relative to the optimal levels for P. sinensis, not exceeding 2.1% for Ca and 1.4% for
P. Frequently, the declared nutritional content is not described in detail or given just
as minimal or maximal levels, but based on research carried out on P. sinensis, the
chemical composition of commercial diets appears to meet the main requirements of
turtles in terms of the CP and fat contents. In contrast to fresh components, the vita-
min levels of commercial diets may be partially decreased relative to the declarations
of the producers due to improper storage as well as processing, i.e., extrusion. Prac-
tically, the use of commercial feeds supplemented with natural components seems
to be a good strategy for maintaining diet diversity in captivity (Mitchell and Tully,
2009), but from the nutritional point of view, this strategy leads to an unknown sup-
ply of energy and nutrients. In commercial diets, the main components are meals of
animal origin, cereals and soybean meal supplemented with vitamin and minerals,
and in the case of plant matter-based diets, the levels of essential amino acids may be
not sufcient for strict carnivores. Moreover, the phosphorus in plant matter, and in
cereals in particular, is bound in a phytate form, which is unavailable to monogastric
animals (Pen et al., 1993). When plant matter is used as an animal protein replace-
ment in diets for mainly carnivorous turtles, Ca, Mg and P supplementation or the
use of endogenous phytase may be needed, as was shown in P. sinensis (Chen et al.,
2014). If commercial diets are offered, the trends of lower CP requirements and on-
togenetic diet shifts during different life stages are often not considered, but several
commercial diets are now available that provide formulations for hatchlings, grow-
ing turtles and adults that contain approximately 40, 35 and 20% CP, respectively
(Table 5).
Consequences of improper nutritional practices
In the available literature we can nd frequent reports on diet related and meta-
bolic disorders in turtles. Most of them deal with nutritional metabolic bone disease
and hypovitaminosis A which are well discussed (Mader, 2005; Boyer, 2006; Dono-
ghue, 2006; Mans, 2013; Mans and Braun, 2014). However in the case of captive
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Freshwater turtle nutrition – a review 31
turtles issues which are not directly caused by inaccuracy of diet composition seem
to be neglected. They involve environmental factors, form and amount of feed as
well as feeding frequency which all together affect metabolism and feed acceptance.
Most of diet and environmental-related issues are caused by lack of knowledge. In
some cases turtle keepers are not able to identify whether the animal is turtle or tor-
toise and keep freshwater species with no or limited access to water which results in
dehydration and malnutrition (Köbölkuti et al., 2016).
Stress, improper environmental conditions and diet form
Captive reptiles are subjected to many stressors, however, this is frequently ig-
nored due to common opinion that they are less likely to be negatively affected by
them than higher vertebrates. The time to response after stressors including improper
environmental conditions vary from several minutes to even weeks after the factor
occurs (Silvestre, 2014). A very frequent stress-related issue in turtles is anorexia
which may be caused by hypothermia, diseases, injuries, chronic pain or harassment.
Particularly prone to anorexia are hatchlings, wild-caught individuals and animals in
short period after transfer between facilities. They frequently refuse to ingest food
for a long period of time due to poor acclimatization to captivity. Hatchlings may
not accept the food until full yolk sack resorption, in adults food refusal up to two
weeks after the transfer may be interpreted as normal. In their case, longer periods of
starving should be interpreted as a sign of illness or improper environmental condi-
tions. For young and wild-caught animals anorexia may be also caused by improper
form of the diet – they may not accept pelleted feeds, and prefer live prey. In adult
females 2–4 weeks of decreased feed intake coincidental with increased locomotory
activity may be a symptom of egg development and physically decreased capac-
ity of the gastrointestinal tract. In the above case egg binding occurrence should
be excluded. Authors’ observations suggest that in newly settled turtles presence of
the hiding areas, constant temperature in preferred optimal temperature zone, single
animal enclosures and 24/24h of light photoperiod supports acclimatization. In tur-
tle enclosure gradient temperature areas should be present to avoid hypothermia or
heat stress and allow the animal for selection of its preferred temperature – optimal
for metabolism in the moment. It should be underlined that too low temperatures
negatively affect energy and nutrient assimilation efciency, feed intake as well as
digestive turnover rates, as it is shown in Figure 1 (Kepenis and McManus, 1974;
Parmenter, 1981) Too high temperatures and heat stress when no possibility of cool-
ing is given may also cause anorexia. Long-term nutritional deciencies such as
insufcient energy, CP, minerals or vitamin intake may lead to cachexia. When it is
of nutritional origin, improper environmental conditions like low temperatures and
underlying disease also contribute to development of cachexia. Treatment of both
anorexia and cachexia should focus on an increase in diet energy content and opti-
mizing environmental conditions. The type of food offered should be re-considered
for cachexic wild-caught turtles which usually prefer live prey. Suboptimal environ-
mental conditions and protein deciency may not only reduce growth performance,
but may also lead to regression in shell development in hatchlings (Gibbons, 1990).
However, turtles have the ability of growth compensation, if dietary imbalances are
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M. Rawski et al.
32
corrected (Xie et al., 2012). To avoid hypophosphatemia and hypocalcaemia, re-
feeding of cachexic animals should not be too rapid, and energy level should be
increased by 10–50% only when the animal shows improvement during treatment
(Mader, 2005). All together, above-mentioned issues may cause growth depression
which is frequent, however, non-specic symptom of improper nutrition. It is present
in most cases of non-balanced diet in young turtles.
Stereotypic-like nutritional behavior
In many cases, reptile keepers use one or a few kinds of feed for many years
without diversifying the diet of captive turtles. It may be the reason not only for
development of metabolic disorders, but may also cause stereotypical-like behavior
when animals do not accept other kinds of components than those they were fed for
years. Turtles will imprint on food and prefer a diet that they are used to, instead
of newly introduced feeds (Burghardt and Hess, 1966). If new food items are not
accepted, then the most effective seems to be the use of live feeds – sh, shrimps,
bloodworms or other insects larvae, and small vertebrates – to enrich turtle diet and
stimulate feed intake.
Obesity
Another issue in the case of captive animals is positive energy balance – higher
intake than expenditures of metabolic energy may accelerate growth in young ani-
mals and have positive effects if there are no deciencies in the diet. However, it may
lead to obesity in adults, which is dened as an accumulation of excessive amounts
of adipose tissue in the body (Hand et al., 2000). More prone to obesity are species
that are sedentary “bottom walkers” like snapping turtles (Chelydra spp.) or musk
turtles (Sternotherus spp.) and African sidenecks (Pelomedusa spp. and Pelusios
spp.). The best method of obesity prevention is regular body condition score (BCS)
monitoring (Rawski and Józeak, 2014). In chelonians, BCS is assessed mainly on
the basis of comparison of straight carapace length and BW. However, additional
visual assessment should be performed, and conditions, which may mimic obesity
excluded (Jackson, 1980; Willemsen and Hailey; 2002; Rawski and Józeak, 2014).
Obese turtles store adipose tissue mainly in the coelom and internal organs, which
may severely impair their function (Divers and Cooper, 2000). According to screen-
ing in Pelomedusa spp. and Pelusios spp. up to 22% of captive turtles may be over-
weight and obese (Rawski and Józeak, 2014). Treatment of obesity should focus
on restriction of energy intake. It should be lowered progressively to no less than
60% of usual intake. The body weight loss in that case should not exceed 0.5 to
1% weekly (Mader, 2005). According to practical experience of the authors feed-
ing regime in terms of frequency of feeding may be one of the most effective in
obesity prevention. It may be suggested that hatchlings should receive feed 6 times
per week, animals between 6 months to 2 years of age 3-4 times per week and older
ones 1 or 2 times per week. Additionally, turtles should undergo seasonal environ-
mental stimulation for breeding; lipogenesis which occurs as a part of preparation
for folliculogenesis is an important obesity-preventing factor in reptiles (Divers and
Cooper, 2000).
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Freshwater turtle nutrition – a review 33
Conclusions
Despite the recent increase in our scientic knowledge of turtle nutrition, the
statement by Kollias and Gentz from 1996 that “reptile feeding is an art not a sci-
ence” may still be partially valid. Due to the lack of suitable nutritional guidelines
for most turtle species, observations of animal development as well as the experience
and knowledge of keepers are still the most important sources of information for
feeding freshwater turtles. Diet composition should be veried through long-term
experiments, including digestibility studies at each turtle life stage. However, the
basic rules for reptilian nutrition may be stated as follows:
1. The diversication of feed sources and their similarity to natural diet compo-
nents are key to achieving sustainable growth and shell mineralization.
2. Commercial diets, if properly used without overfeeding, provide appropriate
nutrition for turtles in captivity. However, in many cases, their formulation should be
more specically tailored to the needs of turtles with similar natural diets.
3. The exact nutritional requirements of turtles are still largely unknown, but
large-scale farming and scientic experiments provide an opportunity to gain impor-
tant knowledge that is applicable to this problem.
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Received: 30 V 2017
Accepted: 23 VIII 2017
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