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tonnes of meat and more than 1 billion eggs in 2012, that has become the most indispensable ... Various animals, such as goats, camels, yak, and water buffalo,.
The role of traditional and non-traditional meat animals in feeding a growing and evolving world Donna-Mareè Cawthorn* and Louwrens C. Hoffman*† *

Department of Animal Sciences, University of Stellenbosch, Private Bag X1, Matieland 7600, South Africa



 outh African Research Chair in Meat Science, hosted by the University of Stellenbosch in partnership with the University of Fort Hare and funded S by the Department of Science and Technology and administered by the National Research Foundation

Implications • Although our hunter-gatherer ancestors relied on an enormous array of animal species to fulfil their protein requirements, only a handful of these were subsequently domesticated, and cattle, sheep, pigs, and chickens currently represent the main animals used for global meat production. • In spite of various attempts to improve the productivity of these traditional livestock species, this sector is facing immense pressure to meet the increasing demand for animal protein from a growing human population, and the future situation will likely only be aggravated by global warming, water shortages, and land restrictions for livestock production. • Various animals, such as goats, camels, yak, and water buffalo, have accompanied man for centuries, surviving in the harshest conditions and on sparse feed resources. Due to their outstanding adaptability, these species could become crucial for future food supply, as well as for socio–economic and environmental stability. •  While subsistence hunting undoubtedly threatens wildlife populations throughout the world, there are many wild animals that are abundant and even considered as pests that could play a pivotal role in improving food security. Larger prolific species that could be further exploited for meat production include kangaroo, wild pigs, and deer while “mini-livestock” species (e.g., rabbits and rodents) hold particular promise for becoming valuable commercial commodities for food use. Keywords: animal protein, food security, indigenous animals, mini-livestock, wildlife

Meat and Man: The Origins Archeological evidence, including stone tools and butchery marks on fossilized bones, suggests that early hominins adapted to an omnivorous diet more than 2.6 million years ago, supplementing their plant-based diets of fruits, seeds, and tubers with the meat and marrow from various wild animals

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(Pobiner, 2013). This dietary modification appears to be linked with the evolution of the large human brain, which to function, requires a relatively greater proportion of the total energy budget than in other primates, therefore necessitating the addition of energy- and nutrient-rich meat sources (Leonard et al., 2007). These meat sources are believed to have originally been scavenged from the kills of more efficient predators, until such time as hunting skills developed around 500,000 years ago. One of the most momentous evolutionary steps for humankind came many years later through the domestication of livestock animals, beginning with sheep and goats, then progressing to pigs, cattle, horses, donkeys, water buffalo, camelids, and later chickens (Magee et al., 2014; Mignon-Grasteau et al., 2005). The subsequent establishment of animal husbandry techniques enabled man to generate ample and reliable sources of meat, reducing the number of species from which this was derived, but simultaneously facilitating the acceleration of human population growth that has continued unabated ever since (Diamond, 2002). Compared with the estimated 10 million people on earth at the time of agriculture development ca. 10,000 years ago, the world population today far exceeds 7 billion people. The current demand for meat is at an all-time high, driven predominantly by the developing world, where increasing populations, urbanization, and greater incomes have promoted the increased inclusion of animal proteins in the diet (Thornton, 2010). Meat production has consequently been forced to follow suit in almost every part of the globe (Figure 1), more than quadrupling over the last 50 years to reach 302 million tonnes in 2012 (FAOSTAT, 2014). As of 2012, there were more than 1.485 billion cattle in the world, 1.169 billion sheep, and at least 21 billion chickens. Cattle produced 63 million tonnes of meat in 2012, sheep 8.5 million tonnes, and goats 5.3 million tonnes, but these species were far outranked by pigs (109 million tonnes) and poultry (105 million tonnes; FAOSTAT, 2014). The demand for beef and mutton has largely declined over the last few decades, mainly due to their high prices, the perceived health concerns surrounding red meat consumption, and the associated food safety concerns (e.g., bovine spongiform encephalopathy in cattle; Kearney, 2010; Kanerva, 2013). While pig production has continued to increase, the production of poultry has shown the greatest and most rapid growth among the traditional livestock species, increasing almost 12-fold from 9 million tonnes in 1961 (Figure 2). Birds contributing to the current world poultry production include turkeys (5 million tonnes), ducks (4 million tonnes), and guinea fowls and geese (ca. 2.8 million tonnes), but it has been the chicken, producing more than 92 million tonnes of meat and more than 1 billion eggs in 2012, that has become the most indispensable to commercial meat production. As with pigs, chick-

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Figure 1. The contribution of individual countries to global meat production from selected traditional livestock species (Kalverkamp et al., 2014; reproduced under a Creative Commons License).

ens have good feed conversion rates, fast growth rates, and minimal space requirements, meaning that they have been heavily utilized to supply the global demand for cheap protein (Sherman, 2002). Industrialization and specialization have undoubtedly facilitated these enormous meat outputs, with the objectives of some in the U.S., for example, being to modernize farming and to “make every farm a factory” (Fitzgerald, 2003). Biotechnologies such as genetic modification (GM) have been applied to improve the yields of certain crops used to feed both humans and animals (Herrera-Estrella, 2000). Yields within the traditionally farmed livestock sector have been increased through selective breeding for desired production traits (e.g., larger sizes, faster growth rates, and hardiness). Selective breeding, as well as specialized rearing techniques, have also been applied to enhance meat quality and palatability attributes. Such interventions have often generated animals with greater fat contents than their wild progenitors but favored by certain groups of contemporary consumers, such as the modern varieties of intensely marbled Japanese Wagyu beef, which is produced from placid cattle kept in confinement, fed beer, and regularly massaged (Bingen and Bush, 2006). Livestock productivity has been additionally encouraged through advances in science, including the administration of hormones to stimulate growth and antibi-

otics to combat disease. However, as with the application of GM technologies, there has been growing consumer resistance relating to the aforementioned interventions and the notion of intensive farming as a whole, with concerns extending from animal welfare to the pollution, carbon footprints, and water footprints associated with such systems (Napolitano et al., 2010; Hoffman and Cawthorn, 2013). Thus, while technological elaborations have made farmers immensely productive and have indeed transformed the face of agriculture, modern agrarian systems have concurrently disrupted finely balanced systems, contributed to environmental changes, and ultimately transformed the face of the earth. The fact further remains that, in spite of the very best efforts, more than 1 billion (>13%) people in the world still experience famine, hunger, and malnourishment on a daily basis, and this number is only growing (Ingram et al., 2010).

Meat and Man: Future Outlooks Most food producers are likely well aware that the global human population is forecast to surpass 9 billion by 2050, necessitating more than a 50% increase in food productivity to meet these growing needs (Ingram et al., 2010). Livestock systems, however, currently occupy approximately 30% of

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mutus), for instance, which inhabit the mountainous regions and plateaus of central Asia, are the only large mammals able to graze at altitudes of 6,000 m above sea level, at temperatures as low as –40°C, surviving on scantly supplies of mountain feed, yet still remaining productive. The 13.3 million yaks found in Chinese territories produce around 226,000 tonnes of meat and more than 1.4 million tonnes of milk per annum while the 600,000 yaks in land-locked Mongolia provide up to one-half of the meat, milk, and butter of the country (Wiener et al., 2003; Gregory, 2007). The one-humped dromedary camels (Camelus dromedarius), on the other hand, exhibit a number of remarkable anatomical and physiological features that enable them to live, work, reproduce, and yield meat and milk in the blistering hot deserts of northern Africa and eastern Asia. For one, these large herbivores far surpass any other large animals (Kadim et al., 2014) in terms of their adaption to heat and water deprivation (Bornstein, 1990). Further, their ability to store Figure 2. The quantity of meat produced globally from pigs, chickens, cattle, sheep, and goats between 1961 and 2011 large fat deposits in their humps provides them (FAOSTAT, 2014), superimposed with the human population growth (UNDESA, 2013) over the same time period. with crucial energy in times of feed scarcity, as well as insulation from solar radiation. In spite of the ice-free terrestrial surface area of the planet, and much of the best farm- the highly nutritious meat of the camel (Hoffman, 2008) and their symbiland has long been under cultivation. Urbanization and biofuel production are otic relationship with man for thousands of years, camels have been largely reducing this land rapidly, and apart from additional forest clearing, which neglected as economically productive animals with great potential for food will lead to further habitat degradation and biodiversity loss, there is very production. A lack of effort in enhancing camel productivity has been one of little room for further expansion (Steinfeld et al., 2006). In addition to land the primary constraints in developing marketable camel meat products for restrictions for grazing and forage production, the future supply of meat from worldwide supply (Kadim et al., 2013). Nonetheless, in the face of growing conventional livestock species will likely be additionally impacted by climate food insecurity, coupled with climate change and desertification, there is an change, water shortages, carbon emission constraints, high feed prices, and urgent need to better utilize marginal and sub-marginal lands while improvenvironmental and welfare legislation (FAO, 2010; Thornton, 2010). All of ing and stocking such species that thrive under severe environmental condithese factors compound to present one of the biggest threats to food security tions (Lambrecht, 1983; Hoffman, 2008; Webb, 2014). and sustainable resource use that the human race has ever faced. The goat (Capra aegagrus hircus), one of man’s most enduring sources In the pursuit to circumvent this impending food crisis, the scientific com- of high-quality meat and milk, holds many advantages for poorer farmers munity has increasingly begun to focus on the role of “new” or non-traditional and households in the developing world: they are small and cheap to keep, animals in supplying high quality protein for human consumption (Cooper, are amendable to a range of climatic conditions, and their efficient feed 1995). Potential meat producers have no boundaries of size or species: wild, utilization and disease tolerance allows them to flourish on many natural resemi-domesticated, or domesticated animals that can be used for meat con- sources left untouched by other domestic ruminants (Peters, 1987; Alexansumption belong to every mammalian family and also encompass thousands dre and Mandonnet, 2005). Although goats have been criticized for causing of avian, reptilian, and amphibian species (Smil, 2002). Many of these species environmental degradation through overgrazing, when carefully controlled, have long been used by indigenous people in diverse regions of the world they not only control bush encroachment, but these small ruminants also for food (Figure 3), as well as agricultural products and for work purposes, produce meat that is lean, nutritious, and acceptable under most religious with some being well suited to commercial utilization in terms of their sizes, convictions (Hoffman et al., 2002). Goat meat is highly prized and well constitutions, and husbandry requirements (Hoffman and Cawthorn, 2012). accepted in many rural communities (particularly at ceremonial and festive occasions); however, factors that hinder its universal distribution and global Overlooked indigenous species acceptance include the problems of inconsistent supply and quality, the lack On much of the earth's surface that is too steep, too dry, too cold, or too of an organized meat industry and marketing structures, as well as social hot for crop production, pastoralists have for centuries herded large num- stigmas surrounding the meat. Certain consumers inevitably link goats with bers of goats, camels, yak, reindeer, llamas, and alpaca (Figure 3); using poverty, see the meat as inferior, and associate it with lower-income classes, their animals to strategically and sustainably convert the most inhospitable issues that need to be addressed in the marketing of this commodity (Mahscrub into food and energy (Blench, 2001). Developed through the ages, goub et al., 2012). Even so, the world goat population has increased much these animals have become exceptionally well adapted to sparse vegetation, more rapidly (>100%) over the last 3 decades than those of cattle (19%) and harsh terrains, and extreme climatic conditions. Yaks (Bos grunniens and B. sheep (3%) to reach more than 996 million in 2012 (FAOSTAT, 2014), re-

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Figure 3. Examples of ruminant production, by countries and main species (adapted from Kalverkamp et al., 2014; reproduced under a Creative Commons License).

flecting the emergence of goats as crucial livestock species. More than 90% of these animals are concentrated in Africa and Asia while only small numbers are kept as specialty or exotic livestock in developed countries. While global goat meat production was officially reported at 5.3 million tonnes in 2012 (1.1 million, 85% of which are red deer, Cervus elaphus) and dominates the global supply of farmed venison, exporting ca. 15,000 tonnes of the meat in 2011 with a value of NZ$ 211 million (DINZ, 2011). Some wild suid species, including the wild boar (Sus scrofa) found predominantly across Eurasia and the warthog (Phacochoerus africanus) of sub-Saharan Africa, have long been valued for food and recreational hunting, but these animals have come to be regarded as nuisances to agricultural systems and threats to ecosystems in some regions. Nonetheless, given their rapid reproductive rates, outstanding adaptability, and highly nutritious meat, interest has been raised on the potential of these animals as farmed species (Zomborszky et al., 1996; Hoffman and Sales, 2007). The farming of wild boar has thus developed since the 1970s in Europe, Japan, and the USA, while the meat from warthogs is still exclusively obtained from wild populations (Roth and Günter, 1996).

Small animals with big potential While the sustainability and future of the entire bushmeat trade is dubious, the farming or backyard production of smaller wild animals and pests can help to alleviate this uncertainty and contribute to improving food security, especially in developing countries (Hardouin et al., 2003; Hoffman and Cawthorn, 2012, 2013; Assan, 2013). The meat of lagomorphs (i.e., rabbits, hares, and pikas) and rodents (Dalle Zotte, 2014) in particular, has long played a vital role in subsistence societies throughout the world where it is considered tasty, nutritious, and often superior to that from conventional livestock (Roth and Günter, 1996). Both groups of animals show great promise as meat producers due to their legendary reproductive capacities (short gestation periods, large litter sizes, and early sexual maturity), as well as their ability to survive on diverse diets and to reutilize their own digesta through coprophagy (Vietmeyer, 1991; Hirakawa, 2001). The breeding of rabbits (Oryctolagus cuniculus) is already a thriving industry that produces more than 1.8 million tonnes of meat per annum, with China being the main producer (Poławska et al., 2013; FAOSTAT, 2014). Other candidate species for “mini-livestock” production have been reviewed (Vietmeyer, 1991; Hardouin, 1995; Hardouin et al., 2003; Assan, 2013) and comprise the cane rat (Thryonomys spp.), giant rat (Cricetomys gambianus), and the brush-tailed porcupine (Atherurus

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africanus) in Africa, as well as the tenrec (Setifer setosus) in the Mascarene Islands. The rodents that have been identified as having production potential in Latin America include the capybara (Hydrochoerus hydrochaeris), paca (Cuniculus spp.), agouti (Dasyprocta spp.), guinea pig (Cavia porcellus), and coypu (Myocastor coypus; FAO, 1996; Hardouin et al., 2003). Reptiles, frogs, giant snails, and caterpillars have also been recognized as having potential for mini-livestock production.

Conclusions A rising wave of food insecurity threatens mankind as it becomes apparent that our ever-increasing demand for animal protein may well be at odds with the capacity of the planet to supply it. While meat eating is inevitability here to stay, the uncertainty lies in whether just a handful of species will be capable of feeding the growing human population and securing its income in the long term. The need to realize the potential of alternative meat producers is thus substantial. This was foreseen more than 50 years ago by Fraser Darling (1960) who stated that “...to exchange the wide spectrum of animals living in delicate adjustment to their habitat, for the narrowed spectrum of 3 ungulates exotic to Africa—cattle, sheep, and goats—is to throw away a bountiful resource and a marvelous ordering of nature.” A large number of prospective non-traditional meat producers have been introduced in this paper, and while it is not anticipated that these will solve the global food shortages in their entirety, they may well aid in decreasing the extent of current and future food shortages. Although a positive shift towards rearing non-traditional animal species has recently occurred among meat producers worldwide, there is still a gross under-valuation of their meat. This is partly due to old prejudices and the erroneous perception that this meat is of an inferior quality or nutritive value than that of traditional meat species. Indeed, the time for altering these misconceptions is ripe. The conditions for increasing the contribution of non-traditional species to global meat supply could be met, but such progress will likely only become possible with increased emphasis, research, and development of these sectors, with increased productivity, with a supply of meat products that are of a consistent quality and safety, with an efficient market and marketing channels, and with better communication on the quality and nutritive properties of the meat.

Acknowledgements This work is based on the research supported by the South African Research Chairs Initiative of the Department of Science and Technology (DST) and National Research Foundation (NRF) of South Africa. Any opinion, finding, and conclusion or recommendation expressed in this material is that of the authors, and the NRF does not accept any liability in this regard.

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About the Authors Louw Hoffman was born on a cattle and pig ranch in Zimbabwe. He studied animal sciences at Stellenbosch University. After completing his M.Sc. degree on pig meat quality attributes, he was employed as a researcher in aquaculture at Limpopo University. While there, he completed his Ph.D. on the meat quality of the catfish. Thereafter, he was employed as an academic and researcher at Stellenbosch University in the meat science discipline. Dr. Hoffman has published more than 160 scientific peer-reviewed research articles in national and international journals, and 65 M.Sc. and 11 Ph.D. students have already completed their scientific investigations under his supervision. His special research interest is in exotic meat (game and ostrich). Last year (2013), his research on game meat and its contribution to International knowledge was recognized internationally when the American Meat Science Association awarded him its International Lectureship Award. Hoffman is the incumbent of the highly competitive SARChI (South African Research Chair Initiative) Chair in Meat Science: Genomics to Nutriomics. This Chair allows him to focus primarily on research, and presently, he has 44 postgraduate students under his mentorship. He describes himself as a frustrated farmer who has no farm and is therefore an academic and researcher. Correspondence: [email protected] Donna Cawthorn obtained her B.SC. and M.Sc. degrees in food science (cum laude) at Stellenbosch University in South Africa in 2005 and 2007, respectively, where after she completed a Ph.D. degree in food science, focused on the establishment of molecular methods for the identification of South African fish species. Her interest in meat science led her to join the Department of Animal Sciences (Stellenbosch University) as a post-doctoral fellow in 2012, where she still works. Her current foci are on animal forensics and DNAbased species authentication. She has a particular passion for conservation and sustainability issues, and thus much of the latter work is directed towards the fisheries and the illegal bushmeat trade. Dr. Cawthorn has published more than 20 papers in peer-reviewed journals and has presented more than 50 oral presentations on her work. She was also the recipient of the IUFoST Young Scientist Award in 2012 and has received numerous awards for academics and for her oral presentation skills.

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