Understanding Tortoise Nutrition: A Literature Review.

Heather A. Bjornebo, DVM, DABVP (Reptile/Amphibian Practice), CertAqV

Introduction

As exotic animal practitioners, we all recognize the important role proper husbandry plays in the health and wellbeing of our patients. Tortoises in general are considered herbivores and veterinarians often fall into a one size fits all trap when it comes to approaching nutrition in this truly diverse group of animals. We must remember that tortoises are as evolutionarily varied as herbivorous mammals. We would not recommend the same diet for a rabbit as we would for an elephant. Can we really recommend the same diet for a Sulcata as we do for a Russian or a Red-foot? So how do we better approach tortoise nutrition as practitioners? With any captive zoologic species this process starts with asking three basic questions: First, what do they eat in the wild? Second, does the captive environment influence their nutritional needs? And third, how do we simulate this in a captive setting?

What are these species consuming in the wild?

Tortoise foraging behavior has been fairly well studied in a number of species commonly kept in captivity.  One of the most extensively studied tortoises are the Sonoran desert tortoises of North America, Gopherus morafki. Desert tortoises are opportunistic herbivores foraging 0.5 meters or less off the ground. In general, these tortoises take to desert vines, mallows, grasses, forbs, herbs, and shrubs while occasionally consuming succulents and cacti.₁ Leopard tortoises (Geochelone pardalis) have demonstrated similar dietary interest in the wild. A study in Tanzania found that they consumed approximately 74.5% forbs, of which 51% were succulents and 13.5% were legumes. The remainder of their diet was comprised of monocots of which 16.8% were grasses.₂

A number of studies involving palearctic tortoises (Testudo sp.) are available within the literature. Fecal samples from 44 Greek tortoises (Testudo graeca) in Algeria were analyzed to evaluate their diet. Plant parts consumed consisted of leaves, stems, and flowers. Their diet consisted of over 70% dicots. Of dicots consumed, the most common were members of Fabaceae, Compositeae, Primulaceae, and Caryophyllaceae families. Monocots were consumed in low numbers and only 3 species were observed in samples: Cynodon dactylon, Hordeum murinum, and Carex remota. No fruit was consumed.₃ Two studies involving Hermann’s tortoises (Testudo hermanni) — one in Montenegro and Croatia and the other in Italy — found a preference for legume leaves and to a smaller extent grasses._4,5

While fecal analyses can tell us what is being eaten, they do not provide insight into what foods the tortoises avoided. Two studies have directly observed the animals’ foraging behaviors to answer both of these questions. The first, a study of Testudo graeca graeca in Morocco, found this species to be a rather specialist herbivorous tortoise which focuses its foraging effort under spiny shrubs. The five main plants eaten (70%) were Leontodon saxatilis, Malva parviflora, Astragalus cruciatus, Medicago hispida and Lotus arenarius — all forbs. Eryngium ilicifolium, Emex spinosus, and Spergula flaccida were universally avoided.₆ The second is a study of  Agrionemys horsfieldi, and while technically they are not considered a member of the Testudo genus, many practitioners still consider Russian tortoises a member of the palearctic group. This study again focused on observing tortoise foraging behavior in the wild and documented both plants eaten as well as those avoided. Their diet consisted of predominantly Ceratocephalus falcatus, Papaveraceae, Koelpinia and Brassicaceae. Grasses were completely avoided by this species despite being abundant.₇

Moving back to the Americas, we find another study focusing on Geochelone carbonaria and G. denticulata (red-foot and yellow-foot tortoises, respectively) in Northwestern Brazil. Fecal analysis was utilized to find these tortoises consumed a large variety of fruits, flowers, mushrooms, palm frond bases, unidentified grasses, live leaves, vine stems, roots, insects, and carrion. The ingestion of a large amount of fruits as well as animal matter in these species is in contrast to the species previously discussed. So while these species are still considered generalist herbivores, they do tend to stray to the more omnivorous side of things.₈ Another species group also known for their more omnivorous tendencies are the Hingeback tortoises. In a study of Kinixys spekii that focused on food selection in this species, it was noted that wild specimens ingest approximately 47% vascular plants, 41% fungi, and 12% invertebrates (mostly millipedes) in the wild.₉

Many other species have been studied, but for the sake of brevity and the fact that these species are less commonly kept in captivity and encountered these shall not be covered in this review. One might note a species that is extremely commonly kept, but studies appear completely absent here. That is Centrochelys sulcata. To date, no English language studies could be located documenting the diet of this species in the wild, which is quite strange given how well known its dietary needs are in the captive environment.

Does the captive environment influence their nutritional needs?

Before we can discuss simulating wild diets in a captive environment, we must acknowledge that being in captivity is different than being in the wild. The question is, how much does captivity impact a tortoise’s nutritional needs? First, let us look at a study on a group of captive Gopherus agassizi (desert tortoises) examining their growth rates over a period of three years. When compared to age matched wild counterparts, their growth rates were markedly accelerated with a one-, two- and three-year-old captive animals being similar in size to 11-, 17-, and 18-year-old wild specimens. This growth rate was attributed to not only skipped winter dormancy for the first two winters but having constant access for high quality nutrition.₁₀ A second desert tortoise study in published in 2018 compared the growth and body condition of tortoises raised outdoors, indoors, and those released directly into the wild. Indoor tortoises grew approximately 16 times faster than those released directly into the wild. Those raised outdoors but fed a captive diet grew 8 times faster than their wild released counterparts. Being raised indoors did have other significant impacts on their health: shell hardness was significantly impacted, and while indoor tortoises were the size of three- or– four-year-olds at only 7.5 months old, they weighed less than those similarly-sized tortoises. It should be noted that indoor raised tortoises were not provided UVB lighting in this study.₁₁ These studies highlight that supplemental feeding can significantly impact growth rates which needs to be a consideration with captive tortoises._10,11

A study in Testudo hermanni found similar results when it compared artificial housing and diets to outdoor housing and naturally growing vegetation. Using dual-energy x-ray absorptiometry, they evaluated bone density and the tortoises’ conformation. Tortoises raised indoors were provided UVB, and no deficits of bone density were noted. However, higher bone density was associated with pyramiding and was noted in both groups housed in artificial conditions.₁₂

Supplemental heating in captivity also needs to be considered. A study in 2002 investigated the effects of supplemental heat on captive Stigmochelys pardalis (leopard tortoises)and Centrochelys sulcata. It found that both growth rate and incidence of shell pyramiding increased with excess nocturnal heat.₁₃ Humidity can also impact growth in captive tortoises. A study in 2002 investigated the influence environmental humidity along with dietary protein impact has on carapacial conformation on Centrochelys sulcata. Drier environmental conditions produced more pyramiding than humid conditions, as did increased dietary protein.₁₄

How do we simulate natural diets in a captive setting?

Although we would ideally feed natural diets to captive chelonians, many diets provided in captivity are based on more readily available grocery store greens, which can also impact tortoise health. There are few studies investigating diet and dietary components in captive tortoises, some including actual feeding trials. One interesting study in Testudo graeca terrestris in Israel investigated diets with the goal to increase growth in a model breeding farm. Vegetarian diets consisting of horticulturally available greens resulted in soft shell syndrome and high mortality in hatchlings. Increasing the protein levels alleviated the soft shell syndrome but resulted in gout and again high mortality. The high protein diet consisted of cat food and corn flour, used to dilute the cat food in an attempt to prevent gout. This diet resulted in sexually mature females by 230 weeks of age and mature males at 170 weeks. However, this study did not discuss any impact on conformation or negative consequences of this rapid growth.₁₅ While this study is definitely informative of the impact protein has on growth rate, the high protein diet is definitely not one we should encourage for appropriate tortoise nutrition in captivity.

In 2005, a study looked into the influence dietary calcium levels have on leopard tortoises. Tortoises where split into four groups. The first group received no calcium supplementation. The second received calcium supplementation based on recommendations by the manufacturer. Groups 3 and 4 received three times and nine times the manufacturer’s recommended doses of calcium. Not surprisingly, tortoises that were not supplemented ended up with depleted calcium levels throughout their bodies by the end of the study. Those receiving the manufacturer’s recommended doses also did not calcify to normal levels. Those with three times the manufacturer’s recommended doses had high growth rate and were thriving; however, both groups 3 and 4 had metastatic calcifications observed postmortem.₁₆

Mineral levels were also the subject of a study on Testudo hermanni. The digestibility of calcium, magnesium, and phosphorus was investigated. Higher calcium concentrations in the feed led to a higher digestibility of not only calcium but magnesium as well. ₁₇

Lickel also investigated diets in leopard tortoises looking at the digestibility of a complete, extruded feed. This commercially available feed was fed to a group of juvenile tortoises for three or seven days per week as part of their diet. Weight, digesta transit time, rate of passage, and indigestible fill were evaluated. Tortoises receiving the diet daily grew more in plastron width and carapace height, but not carapace length. The researcher did not discuss whether this increased carapace height was the result of pyramiding, but her assessment was that those tortoises fed daily did not grow ideally conformationally.₁₈

So… Where does this leave us on understanding the nutritional needs of captive tortoises?

We have come a long way in understanding the dietary needs of these animals. Back in 2005, Innis published recommendations focusing around store bought items such as dandelion greens, cabbage, endive, etc.₁₉ Ten years later we look at recommendations published by Pellet who noted “a fruit, salad and vegetable diet is not ideal for most species.” She recommended Testudo spp. receive various plants and flowers and be provided an edible weed and plant garden. For larger, grass-eating species, she recommended grass grazing and only supplementing them with edible plants and weeds.₂₀ While we still have a long way to go to fully understand the nutritional needs of these fascinating animals, it is important to not lose sight of their wild diets. Horticultural greens fall short in providing for the nutritional needs of these species and the answer to feeding may not be found in the grocery store but instead in the garden center.

References:

1. Van Devender, TR. 2002. The Sonoran Desert Tortoise: Natural History, Biology, and Conservation. The University of Arizona Press and The Arizona-Sonora Desert Museum; Tucson, Arizona.
2. Kabigumila, J. 2001. Sighting frequency and food habits of the leopard tortoise, Geochelone pardalis, in Northern Tanzania. African Journal of Ecology; 39:276-285.
3. Rouag, R.. et al. 2010. Food choice of an Algerian population of the spur‐thighed tortoise, Testudo graeca. African Journal of Herpetology. 57(2), 103-113.
4. Meek, R. 2010. Nutritional selection in Hermann’s tortoise, Testudo hermanni, in Montenegro and Croatia. B.C.G. Testudo. 7(2):88-95.
5. Vecchio, et. al. 2011. Seasonal Changes in the Diet of Testudo hermanni hermanni in Central Italy. Herpetologica, 67(3):236-249.
6. El Mouden, EH et al. 2006. Testudo graeca graeca feeding ecology in an arid and overgrazed zone of Morocco. Journal of Arid Environments; 64:422-435.
7. Largarde, F., et. al. 2003. Foraging behaviour and diet of an ectothermic herbivore: Testudo horsfieldi. Ecography. 26:236-242.
8. Moskovits, DK. & KA. Bjorndal. 1990. Diet and Food Preferneces of the Tortoises Geochelone carbonaria and G. denticulate in Northwestern Brazil. Herpetologica. 46(2). 207-218.
9. Hingeback
10. Jackson, CG., et. al. 1976. Accelerated Growth Rate and Early Maturity in Gopherus agassizi. Herpetologica. 32:139-145.
11. Daly, JA., et. al. 2018. Comparing Growth and Body Condition of Indoor-reared, Outdoor-reared, and Direct-released Juvenile Mojave Desert Tortoises. Herpetological Conservation and Biology. 13(3):633-633.
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13. Heinrich, ML., et. al. 2016. Effect of Supplemental Heat in Captive African Leopard Tortoises (Stigmochelys pardalis) and Spurred Tortoises (Centrochelys sulcata) on Growth Rate and Carapacial Scute Pyramiding. Journal of Exotic Pet Medicine. 25(1):18-25.
14. Wiesner CS. And C Iben. 2003. Influence of Environmental Humidity and Dietary Protein on Pyramidal Growth of Carapaces in African Spurred Tortoises (Geochelone sulcate). J Anim Physiol a Anim Nutr. (87):66-74.
15. Lapid, RH. et. al. 2005. Growth and body composition in captive Testudo graeca terrestris fed with a high-energy diet. Applied Herpetology. 2(2):201-209.
16. Fledelius, B. et.al. 2005. Influence of calcium content of the diet offered to leopard tortoises (Geochelone pardalis). The Veterinary Record.
17. Liesengang, A. et. al. 2007. Influence of different dietary calcium levels on the digestibility of Ca, Mg, and P in Hermann’s tortoises (Testudo hermanni). Journal of Animal Physiology and Animal Nutrition. 91:459-464.
18. Lickel, LE. 2010. Intake, apparently digestibility, and digesta passage in leopard tortoises (Geochelone pardalis) fed a complete, extruded feed. A Thesis Presented to the Faculty of California Polytechnic State University San Luis Obispo, CA, USA.
19. Innis, C. 2005. Considerations in Formulating Captive Tortoise Diets. ARAV. 4(1):8-12.
20. Pellet, S. et. al. 2015. Tortoise feeding and nutritional requirements. Companion Animal. 21(4):240-245.