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Invited review: Ruminant ecology and evolution: Perspectives useful to ruminant livestock research and production

      Abstract

      The article reviews ruminant ecology and evolution and shows insights they offer into livestock research. The first ruminants evolved about 50 million years ago and were small (<5 kg) forest-dwelling omnivores. Today there are almost 200 living ruminant species in 6 families. Wild ruminants number about 75 million, range from about 2 to more than 800 kg, and generally prefer at least some browse in their diets. Nine species have been domesticated within the last 10,000 yr. Their combined population currently numbers 3.6 billion. In contrast to wild ruminants, domestic species naturally prefer at least some grass in their diets, are of large body weight (BW; roughly from 35 to 800 kg), and, excepting reindeer, belong to one family (Bovidae). Wild ruminants thus have a comparatively rich ecological diversity and long evolutionary history. Studying them gives a broad perspective that can augment and challenge the status quo of ruminant research and production. Allometric equations, often used in ecology, relate BW to physiological measurements from several species (typically both wild and domestic). They are chiefly used to predict or explain values of physiological parameters from BW alone. Results of one such equation suggest that artificial selection has increased peak milk energy yield by 250% over its natural level. Voluntary feed intake is proportional to BW0.9 across wild and domestic ruminant species. This proportionality suggests that physical and metabolic factors regulate intake simultaneously, not mutually exclusively as often presumed. Studying the omasum in wild species suggests it functions primarily in particle separation and retention and only secondarily in absorption and other roles. Studies on the African Serengeti show that multiple species, when grazed together, feed such that they use grasslands more completely. They support the use of mixed-species grazing systems in production agriculture. When under metabolic stress, wild species will not rebreed, but rather will extend lactation (to nourish their current offspring). This bolsters the suggestion that lactation length be extended in dairy operations. Cooperation between animal scientists and ecologists could generate more valuable insight.

      Key words

      Introduction

      As an applied field, animal science borrows variously from classical physiology, endocrinology, biochemistry, genetics, and nutrition, among other disciplines. It draws less often from ecological and evolutionary research. For ruminant livestock research, several excellent publications exist on these 2 overlooked subjects, including classic works such as those by
      • Hofmann R.R.
      The Ruminant Stomach: Stomach Structure and Feeding Habits of East African Game Ruminants.
      ,
      • Clutton-Brock T.H.
      • Guinness F.E.
      • Albon S.D.
      Red Deer: The Behaviour and Ecology of Two Sexes.
      ,

      Foose, T. J. 1982. Trophic strategies of ruminant versus nonruminant ungulates. PhD Diss. Univ. Chicago, Chicago, IL.

      , and
      • Owen-Smith N.
      Megaherbivores: The Influence of Very Large Body Size on Ecology.
      and more recent material compilations such as those by
      and
      • Prothero D.R.
      • Foss S.E.
      The Evolution of the Artiodactyls.
      .
      In his general ruminant nutrition text,
      • Van Soest P.J.
      Nutritional Ecology of the Ruminant.
      presents a brief overview of ruminant ecology and evolution. As a brief overview, it necessarily lacks detail and synthesizes few explicit connections between ruminant ecology and evolution and applied livestock research. Some individual manuscripts (e.g.,
      • Walker J.W.
      Multispecies grazing: The ecological advantage.
      ;
      • Knight C.H.
      Lactation and gestation in dairy cows: Flexibility avoids nutritional extremes.
      ) have drawn more detailed and direct connections. Although valuable in their own right, these manuscripts do not include a thorough introduction to ruminant ecology and evolution.
      The aim of this review is to 1) summarize key points of ruminant ecology and evolution, and then 2) show where these points offer insight into livestock research and production, drawing on our original ideas and some isolated ones presented previously. The focus on nutrition and physiology in this review reflects our own expertise, not a lack of importance of other fields (e.g., reproduction, behavior, genetics).

      Ecology and Evolutionary History of Wild Ruminants

      For the purpose of this review, a ruminant includes any artiodactyl (member of the mammalian order Artiodactyla) possessing a rumen, reticulum, omasum, or isthmus homologous to the omasum, and abomasum. Ruminants also possess certain skeletal features—such as loss of upper incisors, the presence of incisiform lower canines, and fusion of the cubiod and navicular bones in the tarsus—that are useful in fossil identification (e.g.,
      • Gentry A.W.
      The ruminant radiation.
      ) but that are not of primary consideration here.

      Ruminant Families

      The 6 extant (i.e., nonextinct) ruminant families include the Tragulidae, Moschidae, Bovidae, Giraffidae, Antilocapridae, and Cervidae. Table 1 provides a description of these families, including the number of species and genera (from
      • Nowak R.M.
      ).
      Table 1Description of extant ruminant families, including number of genera and species and example species
      Data from Nowak (1999).
      FamilyGenera, no.Species, no.Example species
      Antilocapridae11Pronghorn
      Bovidae49140Cattle, sheep, goats, antelope
      Cervidae1741Red deer, caribou, moose
      Giraffidae22Giraffe, okapi
      Moschidae15Muskdeer
      Tragulidae34Chevrotains
      Total73193
      1 Data from
      • Nowak R.M.
      .
      The Tragulidae (chevrotains; 4 species) are small, reclusive, forest-dwelling, deer-like ruminants (Figure 1). They are the most primitive of all living families and have changed little morphologically over evolutionary history; this has led them to being called “living fossils” (
      • Janis C.M.
      Tragulids as living fossils.
      ). Their primitiveness is demonstrated by their 1) very simple social behavior, 2) retention of a gallbladder and appendix (
      • Janis C.M.
      Tragulids as living fossils.
      ), 3) lack of a true omasum (
      • Langer P.
      The Mammalian Herbivore Stomach: Comparative Anatomy, Function and Evolution.
      ), and 4) possession of many skeletal characters (e.g., short, unfused metapodials) considered ancestral (
      • Webb S.D.
      • Taylor B.E.
      The phylogeny of hornless ruminants and a description of the cranium of Archaeomeryx.
      ). Although still considered ruminants, the Tragulidae are not included in the same infraorder (Pecora) as other ruminant families (Moschidae, Bovidae, Giraffidae, Antilocapridae, Cervidae) because of these ancestral features.
      Figure thumbnail gr1
      Figure 1A greater Malay chevrotain (Tragulus napu), a member of the family Tragulidae and one of the most primitive ruminants. Note the small size (approximately 3 kg), short limbs, and absence of horns, all of which are characteristic of early ruminants. Enlarged upper canines are absent because this specimen is a female. Photo courtesy of Ellen S. Dierenfeld (Novus International Inc., St. Charles, MO).
      The Moschidae (musk deer; 5 species) are small, Asiatic forest deer whose males possess a musk gland anterior to the genitals. Like tragulids, the moschids are hornless (other families possess horns or antlers), and the males have large upper canines instead. The remaining families, the Bovidae (e.g., cattle, sheep, goats, antelope; 140 species), Giraffidae (giraffe and okapi), Cervidae (true deer; e.g., white-tailed deer, red deer elk, caribou, moose; 41 species), and Antilocapridae (pronghorn), include species familiar to most readers. Standard mammalogy textbooks (e.g.,
      • Feldhamer G.A.
      • Drickamer L.C.
      • Vessey S.H.
      • Merrit J.F.
      • Krajewski C.
      Mammalogy: Adaptation, Diversity, Ecology.
      ) and encyclopedias (e.g.,
      • Nowak R.M.
      ) provide additional information for all these families.
      Five additional extinct families are generally recognized (
      • Carroll R.L.
      Vertebrate Paleontology and Evolution.
      ): the Hypertragulidae, Leptomerycidae, Gelocidae, Palaeomerycidae, and Dromomerycidae. The Hypertragulidae, Leptomerycidae, and Gelocidae were small, hornless ruminants that probably most closely resembled moschids or tragulids (
      • Webb S.D.
      • Taylor B.E.
      The phylogeny of hornless ruminants and a description of the cranium of Archaeomeryx.
      ;
      • Webb S.D.
      Hornless ruminants.
      ). The Palaeomerycidae and Dromomerycidae were medium to large sized, with giraffe-like horns but deer-like limb proportions (
      • Janis C.M.
      • Scott K.M.
      The interrelationships of higher ruminant families with special emphasis on the members of the Cervoidea.
      ). Their ecological niche probably resembled that of a subtropical deer (
      • Janis C.M.
      • Manning E.
      Dromomerycidae.
      ).

      Phylogeny and Evolution

      The phylogeny of these families is not well resolved, but one possible scenario (a simplified and updated version presented by
      • Gentry A.W.
      The ruminant radiation.
      ) is shown in Figure 2. The Hypertragulidae are the most primitive and were thus probably the first to appear (
      • Webb S.D.
      • Taylor B.E.
      The phylogeny of hornless ruminants and a description of the cranium of Archaeomeryx.
      ), around 50 million years ago (Ma; Early Eocene) in Southeast Asia (
      • Hernández Fernández M.H.
      • Vrba E.S.
      A complete estimate of the phylogenetic relationships in Ruminantia: A dated species-level supertree of the extant ruminants.
      ;
      • Métais G.
      • Vislobokova I.
      Basal ruminants.
      ). The Tragulidae and Leptomerycidae (or close ancestors thereof) arose shortly thereafter, again in Asia (
      • Colbert E.H.
      The osteology and relationships of Archaeomeryx, an ancestral ruminant.
      ;
      • Métais G.
      • Chaimanee Y.
      • Jaeger J.J.
      • Ducrocq S.
      New remains of primitive ruminants from Thailand: Evidence of the early evolution of the Ruminantia in Asia.
      ), but quickly dispersed to North America (
      • Webb S.D.
      Hornless ruminants.
      ). During this time, tropical, closed-canopy forests were widespread (
      • Janis C.M.
      Tertiary mammal evolution in the context of changing climates, vegetation, and tectonic events.
      ) and temperatures were very warm (near their highest point in the last 65 million years;
      • Zachos J.
      • Pagani M.
      • Sloan L.
      • Thomas E.
      • Billups K.
      Trends, rhythms, and aberrations in global climate 65 Ma to present.
      ). The Gelocidae appeared at approximately 40 Ma (Middle Eocene), when the climate had already cooled (about 5°C relative to 50 Ma;
      • Zachos J.
      • Pagani M.
      • Sloan L.
      • Thomas E.
      • Billups K.
      Trends, rhythms, and aberrations in global climate 65 Ma to present.
      ) and temperate woodlands appeared (
      • Janis C.M.
      Tertiary mammal evolution in the context of changing climates, vegetation, and tectonic events.
      ).
      Figure thumbnail gr2
      Figure 2A phylogeny of ruminant families. Families included are the Hypertragulidae, Tragulidae, Leptomerycidae, Gelocidae, Moschidae, Dromomerycidae, Palaeomerycidae, Antilocapridae, Giraffidae, Cervidae, and Bovidae—that is, those recognized by
      • Carroll R.L.
      Vertebrate Paleontology and Evolution.
      . Solid lines indicate age ranges documented in the fossil record [adapted from
      • Métais G.
      • Chaimanee Y.
      • Jaeger J.J.
      • Ducrocq S.
      New remains of primitive ruminants from Thailand: Evidence of the early evolution of the Ruminantia in Asia.
      for Tragulidae;
      • Webb S.D.
      Hornless ruminants.
      and
      • Gentry A.W.
      The ruminant radiation.
      for Gelocidae; and
      • Gentry A.W.
      The ruminant radiation.
      for all other families, assuming Archaeomeryx belongs to Leptomerycidae (
      • Webb S.D.
      • Taylor B.E.
      The phylogeny of hornless ruminants and a description of the cranium of Archaeomeryx.
      )]; stippled lines indicate inferred age ranges and family relationships (adapted from
      • Gentry A.W.
      The ruminant radiation.
      ).
      When these first ruminant groups emerged, they were rabbit-sized (<5 kg;
      • Métais G.
      • Vislobokova I.
      Basal ruminants.
      ). Their skull and dental morphology (low-crowned teeth, small incisors, long and narrow skulls) were optimal for consuming fruits, shoots, and insects (
      • Webb S.D.
      Hornless ruminants.
      ). This evidence, in addition to the observed habitat and diet of living tragulid and moschid species (which are taken as rough analogs for these first groups), suggests that the first ruminants were small, reclusive, forest-dwelling omnivores (
      • Webb S.D.
      Hornless ruminants.
      ). The first ruminants did not ruminate or have a functional rumen flora (viz., for fiber fermentation) until about 40 Ma, as indicated by dental morphology (
      • Janis C.M.
      The evolutionary strategy of the Equidae and the origins of rumen and cecal digestion.
      ) and molecular techniques (
      • Jermann T.M.
      • Opitz J.G.
      • Stackhouse J.
      • Benner S.A.
      Reconstructing the evolutionary history of the artiodactyl ribonuclease superfamily.
      ).
      The remaining families evolved about 18 to 23 Ma (Early Miocene) during a second radiation (
      • Janis C.M.
      Evolution of horns in ungulates: Ecology and paleoecology.
      ) in Eurasia (Antilocapridae, Cervidae, Moschidae, Dromomerycidae, Bovidae, Palaeomerycidae) and Africa (Giraffidae;
      • Gentry A.W.
      The ruminant radiation.
      ). Many of these families (Moschidae, Dromomerycidae, Antilocapridae) dispersed to North America shortly after their emergence (
      • Janis C.M.
      • Manning E.
      Antilocapridae.
      ,
      • Janis C.M.
      • Manning E.
      Dromomerycidae.
      ;
      • Webb S.D.
      Hornless ruminants.
      ). By this time, the climate was drier (
      • Janis C.M.
      Tertiary mammal evolution in the context of changing climates, vegetation, and tectonic events.
      ) and had cooled substantially (the first Antarctic ice sheets had formed;
      • Zachos J.
      • Pagani M.
      • Sloan L.
      • Thomas E.
      • Billups K.
      Trends, rhythms, and aberrations in global climate 65 Ma to present.
      ) and open, temperate woodlands were the dominant flora (
      • Janis C.M.
      Evolution of horns in ungulates: Ecology and paleoecology.
      ,
      • Janis C.M.
      Tertiary mammal evolution in the context of changing climates, vegetation, and tectonic events.
      ). Dental wear patterns and craniodental morphology suggest these groups ate primarily leaves (
      • Janis C.M.
      Evolution of horns in ungulates: Ecology and paleoecology.
      ;
      • Solounias N.
      • Moelleken S.M.C.
      Tooth microwear analysis of Eotragus sansaniensis (Mammalia: Ruminantia), one of the oldest known bovids.
      ) or grass and leaves (
      • Solounias N.
      • McGraw W.S.
      • Hayek L.-A.C.
      • Werdelin L.
      The paleodiet of the Giraffidae.
      ;
      • Semprebon G.
      • Janis C.M.
      • Solounias N.
      The diets of the Dromomerycidae (Mammalia: Artiodactyla) and their response to Miocene vegetational change.
      ;
      • Semprebon G.M.
      • Rivals F.
      Was grass more prevalent in the pronghorn past? An assessment of the dietary adaptations of Miocene to recent Antilocapridae (Mammalia: Artiodactyla).
      ;
      • DeMiguel D.
      • Fortelius M.
      • Azanza B.
      • Morales J.
      Ancestral feeding state of ruminants reconsidered: Earliest grazing adaptation claims a mixed condition for Cervidae.
      ). The body mass of these groups was initially about 20 to 40 kg (
      • Janis C.M.
      Evolution of horns in ungulates: Ecology and paleoecology.
      ).
      By about 5 to 11 Ma (Late Miocene), grasslands had expanded (
      • Jacobs B.F.
      • Kingston J.D.
      • Jacobs L.J.
      The origin of grass-dominated ecosystems.
      ), and some species began including more grass in their diets, again as suggested by dental wear patterns and craniodental morphology (
      • Semprebon G.
      • Janis C.M.
      • Solounias N.
      The diets of the Dromomerycidae (Mammalia: Artiodactyla) and their response to Miocene vegetational change.
      ;
      • Semprebon G.M.
      • Rivals F.
      Was grass more prevalent in the pronghorn past? An assessment of the dietary adaptations of Miocene to recent Antilocapridae (Mammalia: Artiodactyla).
      ). At the end of this period (5 Ma), bovids and cervids migrated to North America (
      • Webb S.D.
      Cervidae and bovidae.
      ,
      • Webb S.D.
      Evolutionary history of new world Cervidae.
      ). Later (2 Ma; Latest Pliocene), deer would migrate to South America (
      • Webb S.D.
      Evolutionary history of new world Cervidae.
      ).

      Distribution, Abundance, BW, and Dietary Preferences of Living Ruminants

      Today, nearly 200 wild ruminant species exist (
      • Nowak R.M.
      ), most of which are Bovidae and Cervidae (Table 1). A conservative estimate places the world population of wild ruminants at 75.3 million, with 0.28 million tragulids, 0.28 million moschids, 44.6 million cervids, 29.1 million bovids, 0.15 million giraffids, and 0.88 million antilocaprids (Supplemental Table 1, http://www.journalofdairyscience.org/; Appendix). The majority of wild ruminants, in terms of species and population numbers, are thus bovids and cervids.
      Following their distribution in the fossil record, living ruminants are natively found on all continents except Antarctica and Australia, although most species are found in Africa and Eurasia (Table 2, constructed from data in

      van Wieren, S. E. 1996. Digestive strategies in ruminants and nonruminants. PhD Diss. Wageningen Univ., Wageningen, the Netherlands.

      ). The Bovidae and Cervidae both enjoy an almost worldwide distribution, whereas the range of the remaining families is much more restricted (Table 2). Only the Cervidae are found in South America (Table 2).
      Table 2Native distribution of species (% of total within family) across continents and habitat and climate types
      Data from van Wieren (1996).
      FamilyContinent
      EA=Eurasia; AF=Africa; NA=North America; SA=South America.
      ,
      Percentages for each continent may not sum to 100 within family because some species may be located on multiple continents.
      HabitatClimate
      EAAFNASAForestEcotoneOpenWarmTemperateCold
      Antilocapridae0010000010001000
      Bovidae28.467.64.9025.432.442.274.516.78.8
      Cervidae63.30
      Does not include species that have a limited range in Africa.
      13.330.050.030.020.046.746.76.7
      Giraffidae01000050.050.0010000
      Moschidae1000000100000100
      Tragulidae75.025.0001000010000
      Total37.651.17.16.432.631.935.568.822.09.2
      1 Data from

      van Wieren, S. E. 1996. Digestive strategies in ruminants and nonruminants. PhD Diss. Wageningen Univ., Wageningen, the Netherlands.

      .
      2 EA = Eurasia; AF = Africa; NA = North America; SA = South America.
      3 Percentages for each continent may not sum to 100 within family because some species may be located on multiple continents.
      4 Does not include species that have a limited range in Africa.
      Ruminants not only have a wide geographic distribution, but are also found across many climates and habitats. Although the classification system of habitats and climates used in this review (adopted from

      van Wieren, S. E. 1996. Digestive strategies in ruminants and nonruminants. PhD Diss. Wageningen Univ., Wageningen, the Netherlands.

      ) is admittedly crude, it still gives a general sense of this distribution. As a whole, ruminant species are evenly spread across open, ecotone, and forested habitats, but they prefer warm to other types of climates (Table 2). The distribution of the Bovidae and Cervidae is generally representative of this overall pattern, whereas other families individually inhabit a more restricted range of habitats and climates (Table 2).
      As reported in Table 3 (data from

      van Wieren, S. E. 1996. Digestive strategies in ruminants and nonruminants. PhD Diss. Wageningen Univ., Wageningen, the Netherlands.

      ), the median BW of modern ruminants is 45 kg. Body mass ranges greatly, from approximately 2 kg [Salt's dik-dik (Madoqua saltiana), royal antelope (Neotragus pygmaeus), lesser Malay mouse deer (Tragulus javanicus)] to 800 kg [American bison (Bison bison), wisent (Bison bonasus), gaur (Bos gaurus), Asian water buffalo (Bubalus bubalis), kouprey (Bos sauveli);

      van Wieren, S. E. 1996. Digestive strategies in ruminants and nonruminants. PhD Diss. Wageningen Univ., Wageningen, the Netherlands.

      ]. Although not shown in Table 3, some individuals from the largest species achieve BW ≥1,000 kg, with the maximum size of a male reticulated giraffe (Giraffa camelopardalis) reaching 1,400 kg (
      • Clauss M.
      • Frey R.
      • Kiefer B.
      • Lechner-Doll M.
      • Loehlein W.
      • Polster C.
      • Rössner G.E.
      • Streich W.J.
      The maximum attainable body size of herbivorous mammals: Morphophysiological constraints on foregut, and adaptations of hindgut fermenters.
      ). By family, the Giraffidae are the largest; Antilocapridae, Bovidae, Cervidae are intermediate; and Moschidae and Tragulidae are the smallest (Table 3). The Bovidae and Cervidae have species at or near these BW extremes, whereas the other families display a much more restricted range in BW (Table 3).
      Table 3Body mass of wild ruminant species by family
      Values computed from species averages reported by van Wieren (1996).
      FamilyBody mass, kg
      MedianMinimumMaximum
      Antilocapridae404040
      Bovidae52.52800
      Cervidae47.56550
      Giraffidae475250700
      Moschidae11.51112
      Tragulidae228
      Total452800
      1 Values computed from species averages reported by

      van Wieren, S. E. 1996. Digestive strategies in ruminants and nonruminants. PhD Diss. Wageningen Univ., Wageningen, the Netherlands.

      .
      Ruminant species display innate dietary preferences, and these differ greatly across species. A concise way of classifying these preferences is with the feeding class system (first proposed by
      • Hofmann R.R.
      • Stewart D.R.M.
      Grazer or browser: A classification based on the stomach-structure and feeding habits of East African ruminants.
      ), which categorizes species as 1) browsers, which innately prefer browse such as fruits, shoots, and leaves (typically from shrubs, forbs, and trees); 2) grazers, which innately prefer grasses; or 3) intermediate feeders, which switch between browse and grass, usually depending on their seasonal availability. For most of their evolutionary history, ruminant species were predominately or exclusively browsers. Today, a plurality of ruminant species are still classified as browsers (Table 4), and only about a quarter are grazers. The Bovidae and Cervidae have species represented in all 3 feeding classes; the other families are exclusively browsers.
      Table 4Dietary preferences of species (% of total species within family), according to their assignment as browsers (BR), intermediate feeders (IM), or grazers (GR)
      Data from van Wieren (1996).
      FamilyFeeding class
      BRIMGR
      Antilocapridae10000
      Bovidae35.326.539.2
      Cervidae46.736.716.7
      Giraffidae10000
      Moschidae10000
      Tragulidae10000
      Total41.131.927.0
      1 Data from

      van Wieren, S. E. 1996. Digestive strategies in ruminants and nonruminants. PhD Diss. Wageningen Univ., Wageningen, the Netherlands.

      .

      Domestication of Ruminant Species

      Details of Domestication

      The first livestock species to be domesticated (ruminant or nonruminant) was the goat, at approximately 8,000 BC in the Fertile Crescent of the Near East (
      • Zeder M.A.
      • Hesse B.
      The initial domestication of goats (Capra hircus) in the Zagros Mountains 10,000 years ago.
      ). The goat was initially domesticated to supply meat to burgeoning, congested human populations whose hunting had depleted large prey populations in the wild (
      • Clutton-Brock J.
      A Natural History of Domesticated Mammals.
      ;
      • Diamond J.
      Evolution, consequences and future of plant and animal domestication.
      ). Most of the other 8 domesticated ruminant species (sheep, European and Zebu cattle, water buffaloes, mithans, reindeer, yaks, Bali cattle) were brought under human control by 2,500 BC in either the Near East or southern Asia (
      • Clutton-Brock J.
      A Natural History of Domesticated Mammals.
      ). Some of these species, such as the goat, were initially domesticated for meat, but reasons for domestication varied greatly, including for milk, draft, transportation, sacrifice, and barter (
      • Clutton-Brock J.
      A Natural History of Domesticated Mammals.
      ).
      Molecular approaches (
      • Bruford M.W.
      • Bradley D.G.
      • Luikart G.
      DNA markers reveal the complexity of livestock domestication.
      ) have determined that each domestic species is probably derived from several wild species; at least 12 species can claim ancestry to the 9 domesticated species. Of the multitude of available wild species, these 12 were chosen for domestication because they were gregarious, submissive to human captors, unexcitable, and easy to breed (
      • Clutton-Brock J.
      A Natural History of Domesticated Mammals.
      ;
      • Diamond J.
      Evolution, consequences and future of plant and animal domestication.
      ).

      Characteristics of Domestic Species

      Points in the discussion below are summarized in Table 5. The total population size of domestic species is 3.57 billion, nearly 50-fold larger than that of wild ruminants. As might be anticipated, cattle, sheep, and goats constitute most (about 95%) of the domestic ruminant population. All but reindeer belong to the family Bovidae.
      Table 5Characteristics of domestic species, including population size, mean BW, and feeding class
      SpeciesPopulation size,
      Data for goats, sheep, cattle, and water buffaloes from the Food and Agriculture Organization of the United Nations (2008a); for reindeer from Ulvevadet and Klokov (2004); for yaks from Wiener et al. (2003); and for Bali cattle from the Food and Agriculture Organization of the United Nations (2008b).
      millions
      BW
      Data for sheep, cattle, and goats are from typical literature studies (those summarized in Tables 5 and 6 of Hummel et al., 2005); for water buffaloes from Popenoe (1981); for yaks from Wiener et al. (2003); and for all other species from van Wieren (1996), taking BW of wild ancestors.
      Feeding class
      IM=intermediate feeder; GR=grazer.
      ,
      Data for goats, cattle, and water buffaloes from Hofmann (1989); for sheep from Hofmann (1989) and Pfister and Malechek (1986); and for all other species from van Wieren (1996), taking feeding class of wild ancestors.
      Goat (Capra hircus)85035IM
      Sheep (Ovis aries)1,11350IM/GR
      European and Zebu cattle (Bos taurus, Bos indicus)
      Values for European and Zebu cattle are presented together because separate data are generally not available for these species.
      1,390600GR
      Water buffalo (Bubalus bubalis)202400GR
      Mithan (Bos frontalis)NA800GR
      Reindeer (Rangifer tarandus)2140IM
      Yak (Bos mutus)14700GR
      Bali cattle (Bos javanicus)4700GR
      Total3,574
      1 Data for goats, sheep, cattle, and water buffaloes from the

      Food and Agriculture Organization of the United Nations. 2008a. Domestic Animal Diversity Information System. Food Agric. Org. United Nations, Rome, Italy. http://lprdad.fao.org/ Accessed Sep. 9, 2008.

      ; for reindeer from
      ; for yaks from
      • Wiener G.
      • Jianlin H.
      • Ruijun L.
      The Yak.
      ; and for Bali cattle from the

      Food and Agriculture Organization of the United Nations. 2008b. FAO Statistical Databases. Food Agric. Org. United Nations, Rome, Italy. http://faostat.fao.org/ Accessed Sep. 9, 2008.

      .
      2 Data for sheep, cattle, and goats are from typical literature studies (those summarized in Tables 5 and 6 of
      • Hummel J.
      • Clauss M.
      • Zimmerman W.
      • Johanson K.
      • Nørgaard C.
      • Pfeffer E.
      Fluid and particle retention in captive okapi (Okapia johnstoni).
      ); for water buffaloes from
      • Popenoe H.
      The Water Buffalo: New Prospects for an Underutilized Animal.
      ; for yaks from
      • Wiener G.
      • Jianlin H.
      • Ruijun L.
      The Yak.
      ; and for all other species from

      van Wieren, S. E. 1996. Digestive strategies in ruminants and nonruminants. PhD Diss. Wageningen Univ., Wageningen, the Netherlands.

      , taking BW of wild ancestors.
      3 IM = intermediate feeder; GR = grazer.
      4 Data for goats, cattle, and water buffaloes from
      • Hofmann R.R.
      Evolutionary steps of ecophysiological adaptation and diversification of ruminants: A comparative view of their digestive system.
      ; for sheep from
      • Hofmann R.R.
      Evolutionary steps of ecophysiological adaptation and diversification of ruminants: A comparative view of their digestive system.
      and
      • Pfister J.A.
      • Malechek J.C.
      Dietary selection by goats and sheep in deciduous woodland of northeastern Brazil.
      ; and for all other species from

      van Wieren, S. E. 1996. Digestive strategies in ruminants and nonruminants. PhD Diss. Wageningen Univ., Wageningen, the Netherlands.

      , taking feeding class of wild ancestors.
      5 Values for European and Zebu cattle are presented together because separate data are generally not available for these species.
      Most species are grazers, with goats and reindeer the notable exceptions. Sheep were classified by
      • Hofmann R.R.
      Evolutionary steps of ecophysiological adaptation and diversification of ruminants: A comparative view of their digestive system.
      as grazers, although others (e.g.,
      • Pfister J.A.
      • Malechek J.C.
      Dietary selection by goats and sheep in deciduous woodland of northeastern Brazil.
      ) have argued that they are instead intermediate feeders.
      Although BW varies greatly by sex and across breeds, the rough averages in Table 5 demonstrate that the BW of domestic ruminants are large in comparison with many wild ruminants. The smallest species (sheep, goats) are near the median BW of wild ruminants (45 kg) and many species (cattle, mithans, Bali cattle) approach the maximum observed in the wild (800 kg; Table 3).

      Perspectives Relevant to Modern Production Systems

      Wild ruminants, past and present, prove much more diverse (in terms of phylogeny, behavior, diet, and otherwise) than domestic ruminants. Further, the 50-million-year evolutionary history of the ruminant extends far before domestication. Studying ruminant ecology and evolution gives a broad perspective of what ruminants are and how they came to be—much broader than achieved through studying domestic species alone. This broad perspective can augment or even challenge the status quo of livestock research and management, which has been established by using a much narrower perspective. The following discussion presents some examples of how principles in ruminant ecology and evolution can offer insight into livestock research and production.

      Predicting Values of Physiological Parameters from BW

      Body mass has a clear influence on the value of many physiological parameters. For example, the greater feed intake of a cow relative to a goat, intuitively, is largely attributable to the greater BW of the cow. The exact, quantitative relationship between a physiological parameter and BW is often less obvious, however.
      Allometric equations (
      • Peters R.H.
      The Ecological Implications of Body Size.
      ;
      • Calder III, W.A.
      Size, Function, and Life History.
      ;
      • Schmidt-Nielsen K.
      Scaling: Why is animal size so important?.
      ) quantitatively express these relationships with the formula
      y=aBWb,


      where y is the value of a physiological parameter, a is the allometric intercept (value of y at BW = 1), and b is the scaling parameter. Values of a and b are found empirically by regressing BW against y for several species (Figure 3). By using observations from multiple ruminant species (including wild ones), one is provided a widely applicable equation that gives a benchmark prediction for a physiological parameter from BW alone. Some uses of these predictions for livestock research include 1) serving as a first approximation for a physiological value for a species when one has not been measured directly and 2) explaining to what extent observed differences between livestock species are attributable to BW (i.e., act as a control for BW in comparisons).
      Figure thumbnail gr3
      Figure 3Graph of the allometric relationship between BW (kg) and wet mass of reticulorumen tissue (kg), illustrating the general principles of allometric equations. Tissue mass observations of individual ruminant species are shown with symbols (♦), with observations of sheep and cattle labeled. The solid line indicates the best-fit allometric equation, with the allometric intercept a and scaling parameter b defined graphically. Note that the plot is semilogarithmic. Data are for 18 wild and domestic species from 10 studies (listed in Table 6.1 of

      Hackmann, T. J. 2008. Studies of ruminant digestion, ecology, and evolution. MS Thesis. Univ. Missouri, Columbia.

      ).
      The allometric equation for metabolic rate (e.g.,
      • Blaxter K.L.
      Energy Metabolism in Animals and Man.
      ) is widely known and applied, but many others are much less so. Examples of allometric equations are given in Table 6, including those for predicting anatomical, ingestive and digestive, energetic, reproductive, and other physiological parameters. For illustration, expected values of these parameters for 2 different BW (50 and 500 kg) are shown. Note that many equations have a very high R2 (>0.95) and thus can be expected to be precise; others have much lower R2 values (as low as 0.18) and should be applied more cautiously.
      Table 6Some allometric equations useful for predicting physiological parameter values from BW
      Equations are of the form Y=a·BWb.
      ,
      Unit, logarithmic, and other conversions have been applied to equations in original sources to standardize their units and form.
      CategoryPhysiological parameterEquation parameterR2Predicted value
      abBW of 50 kgBW of 500 kgSource
      The phrase “data from” preceding a source, where present, indicates that we performed the allometric regression using ruminant data (averaged by species) originally reported by that source.
      AnatomicalReticulorumen volume, L0.2410.9250.9408.9975.61

      van Wieren, S. E. 1996. Digestive strategies in ruminants and nonruminants. PhD Diss. Wageningen Univ., Wageningen, the Netherlands.

      Skull length, cm6.180.3370.96023.150.2
      • Janis C.M.
      Correlation of body weight in ungulates with cranio-dental variables.
      Ingestive and digestiveVoluntary feed intake at maintenance, kg of DM/d0.0437
      a and predicted values reported in this table are for the 58% NDF, 19% CP mature alfalfa hay of van Wieren (1996); in the original equation, a is adjusted by a fixed-effect term for diet, which allows intake to be predicted for other diet types, but this term was omitted here for simplicity.
      0.8750.9671.3410.05See text
      Maximum intake rate, g of wet matter/min0.7380.6210.7548.3734.96Data from
      • Shipley L.A.
      • Gross J.E.
      • Spalinger D.E.
      • Hobbs N.T.
      • Wunder B.A.
      The scaling of intake rate in mammalian herbivores.
      Chewing rate during rumination, no./s2.53−0.1410.6601.461.05Data from
      • Langer P.
      The Mammalian Herbivore Stomach: Comparative Anatomy, Function and Evolution.
      Reticulorumen DM contents, kg0.00911.150.9720.8211.56
      • Illius A.W.
      • Gordon I.J.
      Prediction of intake and digestion in ruminants by a model of rumen kinetics integrating animal size and plant characteristics.
      EnergeticBasal metabolic rate,
      Equation applies to artiodactyls.
      Mcal/d
      0.06840.75NA
      NA=not available.
      1.297.23
      • Blaxter K.L.
      Energy Metabolism in Animals and Man.
      Peak milk energy yield,
      Equation applies to ungulates with single offspring.
      Mcal/d
      0.0880.710.891.417.26
      • Robbins C.T.
      Wildlife Feeding and Nutrition.
      ReproductiveAge at sexual maturity, mo8.860.1560.25016.323.4

      van Wieren, S. E. 1996. Digestive strategies in ruminants and nonruminants. PhD Diss. Wageningen Univ., Wageningen, the Netherlands.

      Reproductive output, young/yr2.54−0.1670.1801.320.90

      van Wieren, S. E. 1996. Digestive strategies in ruminants and nonruminants. PhD Diss. Wageningen Univ., Wageningen, the Netherlands.

      Gestation length, d1290.1250.556210280Data from
      • Peréz-Barbería F.J.
      • Gordon I.J.
      Gregariousness increases brain size in ungulates.
      1 Equations are of the form Y = a·BWb.
      2 Unit, logarithmic, and other conversions have been applied to equations in original sources to standardize their units and form.
      3 The phrase “data from” preceding a source, where present, indicates that we performed the allometric regression using ruminant data (averaged by species) originally reported by that source.
      4 a and predicted values reported in this table are for the 58% NDF, 19% CP mature alfalfa hay of

      van Wieren, S. E. 1996. Digestive strategies in ruminants and nonruminants. PhD Diss. Wageningen Univ., Wageningen, the Netherlands.

      ; in the original equation, a is adjusted by a fixed-effect term for diet, which allows intake to be predicted for other diet types, but this term was omitted here for simplicity.
      5 Equation applies to artiodactyls.
      6 NA = not available.
      7 Equation applies to ungulates with single offspring.
      The equations listed in Table 6 represent a broad survey of the many available in the literature. For more allometric equations, the reader should refer to the sources referenced in the table, as well as
      • Scott K.M.
      Postcranial dimensions of ungulates as predictors of body mass.
      for equations predicting postcranial skeletal dimensions;
      • Clauss M.
      • Hofmann R.R.
      • Streich W.J.
      • Fickel J.
      • Hummel J.
      Higher masseter muscle mass in grazing than in browsing ruminants.
      for masseter muscle mass;
      • Hofmann R.R.
      • Streich W.J.
      • Fickel J.
      • Hummel J.
      • Clauss M.
      Convergent evolution in feeding types: Salivary gland mass differences in wild ruminant species.
      for salivary gland mass;
      • Robbins C.T.
      • Spalinger D.E.
      • van Hoven W.
      Adaptation of ruminants to browse and grass diets: Are anatomical-based browser-grazer interpretations valid?.
      for parotid salivary gland mass and digestive parameters;
      • Illius A.W.
      • Gordon I.J.
      Prediction of intake and digestion in ruminants by a model of rumen kinetics integrating animal size and plant characteristics.
      and
      • Gordon I.J.
      • Illius A.W.
      The functional significance of the browser-grazer dichotomy in African ruminants.
      for mean retention time, particle breakdown rate, and other digestive parameters;
      • Illius A.W.
      • Gordon I.J.
      Physiological ecology of mammalian herbivory.
      for ingestive parameters related to foraging;
      • Clauss M.
      • Lechner-Doll M.
      • Striech W.J.
      Faecal particle size distribution in captive wild ruminants: An approach to the browser/grazer dichotomy from the other end.
      for fecal particle size; and
      • Mystrud A.
      The relative roles of body size and feeding type on activity time of temperate ruminants.
      for activity time.
      The equations given in Table 6 have been derived using both wild and domestic ruminant species. Note that one can parameterize allometric equations using other approaches. Domestic species alone can be used because only 2 species observations are technically required to estimate the 2 parameters (3 if error is to be estimated). However, with so few species observations, an outlier from any one species can unduly affect parameter estimates. Wild species should thus be included to increase the number of observations and the robustness of parameter estimates. At the opposite end, nonruminant species (wild or domestic) can be included in addition to ruminants. In this case, phylogenetic differences across the wide range of species, if not controlled for statistically, may make the resultant equation very general, but also very imprecise and potentially biased. For example, adding marsupials to the allometric equation for metabolic rate would make the equation more widely applicable (viz., for marsupials) but would skew the regression because marsupials have characteristically low metabolic rates (
      • Dawson T.J.
      • Hulbert A.J.
      Standard metabolism, body temperature, and surface area of Australian marsupials.
      ). A good balance between precision, generality, and robustness is thus found by including domestic and wild ruminant species and these alone.
      One must be careful in using allometric equations when a physiological parameter is affected by artificial selection. In such cases, allometric equations often predict poorly—namely, for domestic breeds for which the parameter has been targeted by artificial selection. For example, the equation for peak milk energy yield in Table 6—formulated with wild species and meat-producing domestic breeds fed predominantly forage—predicts a yield of 7.76 Mcal/d for a 550-kg cow. By contrast, observed peak yields for Holstein cows, for which milk production has been intensively selected, are approximately 20 Mcal/d on a similar (predominantly forage) diet (
      • Kolver E.S.
      • Roche J.R.
      • Burke C.R.
      • Kay J.K.
      • Aspin P.W.
      Extending lactation in pasture-based dairy cows: 1. Genotype and diet effect on milk and reproduction.
      , applying milk energy equations of
      NRC
      Nutrient Requirements of Dairy Cattle.
      ). Although allometric equations have little direct predictive ability in such cases, another valuable purpose emerges: to estimate the impact of artificial selection on a parameter. For peak milk energy yield, assuming that the higher-than-expected yield of the cow is primarily caused by artificial selection, we can infer that artificial selection has increased peak yield in the dairy cow by about 250% (20 Mcal/d observed vs. 7.76 Mcal/d expected).

      Role of Physical and Metabolic Factors in Regulating Feed Intake

      In addition to the 2 general uses of allometric equations explained above, some allometric equations can be applied to draw deeper, more complex inferences. For example, the allometric equation for voluntary feed intake (VFI) demonstrates that forage intake is regulated by physical and metabolic factors simultaneously.
      Physiological regulation of feed intake is important to livestock production systems because feed intake affects animal performance and operation costs. Of the many proposed regulation mechanisms (
      • Forbes J.M.
      Voluntary Food Intake and Diet Selection in Farm Animals.
      ), physical (
      • Allen M.S.
      Physical constraints on voluntary intake of forages by ruminants.
      ) and metabolic regulation (
      • Illius A.W.
      • Jessop N.S.
      Metabolic constraints on voluntary intake in ruminants.
      ) are often suggested to predominate. Generally, these 2 regulation mechanisms (physical, metabolic) are considered to operate on a mutually exclusive basis, with intake of low-energy, bulky diets (usually forages) regulated only physically and high-energy, highly degradable diets regulated only metabolically (
      • Conrad H.R.
      • Pratt A.D.
      • Hibbs J.W.
      Regulation of feed intake in dairy cows. I. Change in importance of physical and physiological factors with increasing digestibility.
      ;
      • Baumgardt B.R.
      Regulation of feed intake and energy balance.
      ).
      Theoretical arguments have suggested that these 2 or more regulation mechanisms operate simultaneously (
      • Fisher D.S.
      • Burns J.C.
      • Pond K.R.
      Modeling ad libitum dry matter intake by ruminants as regulated by distension and chemostatic feedbacks.
      ), as do experiments in which VFA is infused and a physical ballast is placed in the rumen simultaneously (
      • Forbes J.M.
      Integration of regulatory signals controlling forage intake in ruminants.
      ). An allometric examination of VFI of wild and domestic ruminants considerably strengthens the case for simultaneous regulation. Because reticulorumen digesta contents and volume are nearly proportional to BW1 (i.e., proportionally do not change with BW; Table 6), one would also expect VFI to be proportional to BW1, if physical regulation only were operating. On other hand, because metabolic rate is proportional to BW0.75 (Table 6), one would also expect VFI to be proportional to BW0.75, if metabolic regulation acted alone. To test which proportionality is observed (if either), we derived an allometric equation for forage intake by using data on 19 wild and domestic species from 5 studies (listed in Table 6.1 of

      Hackmann, T. J. 2008. Studies of ruminant digestion, ecology, and evolution. MS Thesis. Univ. Missouri, Columbia.

      ). We performed a regression similar to that shown in Figure 3, except we included an additional, fixed-effect term that adjusts the allometric intercept (a) by diet. The equation we derived (Table 6) indicates that forage intake is proportional to BW0.875±0.032, with lower and upper 95% confidence limits of BW0.810 and BW0.941. This agrees with the finding that, for livestock species (cattle, sheep, goats), forage intake scales with BW0.9 (
      • Minson D.J.
      Forage in Ruminant Nutrition.
      ;
      • Reid R.L.
      • Jung G.A.
      • Cox-Ganser J.M.
      • Rybeck B.F.
      • Townsend E.C.
      Comparative utilization of warm-and cool-season forages by cattle, sheep and goats.
      ).
      The mean value of the scaling parameter (0.9) and its 95% confidence limits fall in between values expected if intake were regulated only physically (1) and metabolically (0.75). Intuitively, this suggests that physical and metabolic regulation operate simultaneously for forage diets, contrary to the classical suggestion that physical regulation alone should occur; the mechanistic modeling described in

      Hackmann, T. J. 2008. Studies of ruminant digestion, ecology, and evolution. MS Thesis. Univ. Missouri, Columbia.

      confirmed this suggestion. Although a lack of controlled data disallows a similar examination with diets that are not all forage, the wide range in quality of the forage diets (predicted NEM ranged from 0.71 to 1.77 Mcal/kg of DM;
      NRC
      Nutrient Requirements of Dairy Cattle.
      ) suggests the results are not simply constrained to a narrow range of forages. Because this simultaneous regulation is apparent across wild and domestic species alike, it can be inferred that it is highly conserved evolutionarily and is deeply seated.
      • Conrad H.R.
      • Pratt A.D.
      • Hibbs J.W.
      Regulation of feed intake in dairy cows. I. Change in importance of physical and physiological factors with increasing digestibility.
      , who originally proposed that metabolic and physical regulation are mutually exclusive, also used allometry to support their arguments. They concluded that for high-producing dairy cows, VFI scaled with BW1 for low digestibility (<66.7 digestible DM) and with BW0.73 for high-digestibility (>66.7% digestible DM) diets, consistent with mutually exclusive regulation. However, for high-digestibility diets, scaling parameter values were approximately 0.73 for only 2 of their 5 regressions; all others were lower (≤0.62). The upper 95% confidence limits of these 2 favorable regressions (0.962 and 1.03) do not rule out VFI scaling with BW0.9 or possibly even BW1. This fact, and considering that VFI was only poorly related to BW (R2 = 0.074 or lower), indicates that this data set is poor for discriminating intake scaling patterns. Detailed results are not presented for low-digestibility diets, but the above discussion suggests one should remain skeptical of their conclusion that VFI scales with BW1 for these diets. Although intriguing for their time, the allometric analysis of
      • Conrad H.R.
      • Pratt A.D.
      • Hibbs J.W.
      Regulation of feed intake in dairy cows. I. Change in importance of physical and physiological factors with increasing digestibility.
      and conclusions based thereon must be rejected in favor of our more discriminating analysis.

      Primary Function of the Omasum

      Whereas functions of the rumen, reticulum, and abomasum are well delineated, the chief function of the omasum remains somewhat a mystery. It may help retain and separate particles because 1) large particles tend to become trapped between the omasal laminae, whereas small particles and liquids pass through quickly (
      • Bost J.
      Omasal physiology.
      ;
      • Langer P.
      The Mammalian Herbivore Stomach: Comparative Anatomy, Function and Evolution.
      ), and 2) large particles can be ejected from the omasum back into the reticulum (via the reticuloomasal orifice;

      Ehrlein, H. J. 1980. Forestomach motility in ruminants. Publikationen zu Wissenschagtlichen Filmen, Sektion Medizin, Serie 5, Film No 9/C 1328. IWF, Goettingen, Germany.

      ). It may more generally serve as a suction pump that regulates the flow of digesta (both liquid and particles) from the reticulum to the abomasum (
      • Stevens C.E.
      • Sellers A.F.
      • Spurrell F.A.
      Function of the bovine omasum in ingesta transfer.
      ), although some have questioned this purported ability (
      • Bost J.
      Omasal physiology.
      ;
      • Langer P.
      The Mammalian Herbivore Stomach: Comparative Anatomy, Function and Evolution.
      ). It may also be an absorptive organ; the omasum absorbs approximately 12.5, 50, 35, 25, 10, and 50% of water, VFA, ammonia, sodium, potassium, and carbon dioxide that enter (
      • Engelhardt W.V.
      • Hauffe R.
      Role of the omasum in absorption and secretion of water and electrolytes in sheep and goats.
      ). Some fiber digestion (7 to 9% of total tract;
      • Ahvenjärvi S.
      • Vanhatalo A.
      • Huhtanen P.
      • Varvikko T.
      Determination of reticulo-rumen and whole-stomach digestion in lactating cows by omasal canal or duodenal sampling.
      ,
      • Ahvenjärvi S.
      • Skiba B.
      • Huhtanen P.
      Effect of heterogeneous digesta chemical composition on the accuracy of measurements of fiber flow in dairy cows.
      ) also occurs in the omasum. Finally, some claim the omasum reduces particle size (via purported grinding of digesta between laminae), although evidence for this function is at best circumstantial (
      • Bost J.
      Omasal physiology.
      ).
      To establish the primary function of the omasum, we review the omasal form and function of several wild species and suggest how and why the omasum evolved. In tragulids, a true omasum is not present at all; where it should be found, only an isthmus exists instead (
      • Langer P.
      The Mammalian Herbivore Stomach: Comparative Anatomy, Function and Evolution.
      ). This isthmus (also called a transition zone) is short, narrow, and with only small, subtle longitudinal folds (
      • Agungpriyono S.
      • Yamamoto Y.
      • Kitamura N.
      • Yamada J.
      • Sigit K.
      • Yamashita T.
      Morphological study on the stomach of the lesser mouse deer (Tragulus javanicus) with special reference to the internal surface.
      ). Although it does not form a distinct compartment like a true omasum, it is still histologically distinct from the reticulum and abomasum (
      • Agungpriyono S.
      • Yamada J.
      • Kitamura N.
      • Sigit K.
      • Yamamoto Y.
      • Winarto A.
      • Yamashita T.
      Light microscopic studies of the stomach of the lesser mouse deer (Tragulus javanicus).
      ). Considering this evidence and that the Tragulidae are otherwise primitive (Figure 2), this isthmus probably resembles a very early form of omasum, as concluded by other authors (see
      • Langer P.
      The Mammalian Herbivore Stomach: Comparative Anatomy, Function and Evolution.
      ). Because the isthmus lacks structures to retain digesta within it, its contribution to absorption, fiber fermentation, absorption, and particle size reduction must be minimal. Its poor structural development also precludes it from acting as a suction pump to regulate digesta flow. However, the isthmus likely helps retain particles because its small aperture should allow only fine particles to pass into the abomasum and subsequently through the rest of the tract (
      • Langer P.
      The Mammalian Herbivore Stomach: Comparative Anatomy, Function and Evolution.
      ).
      In small, browsing Pecoran species, which are more advanced than the tragulids, the omasum forms a distinct compartment, but it still tends to be small and has few laminae (
      • Hofmann R.R.
      The Ruminant Stomach: Stomach Structure and Feeding Habits of East African Game Ruminants.
      ,
      • Hofmann R.R.
      Evolutionary steps of ecophysiological adaptation and diversification of ruminants: A comparative view of their digestive system.
      ;
      • Langer P.
      The Mammalian Herbivore Stomach: Comparative Anatomy, Function and Evolution.
      ,

      van Wieren, S. E. 1996. Digestive strategies in ruminants and nonruminants. PhD Diss. Wageningen Univ., Wageningen, the Netherlands.

      ).
      • Hofmann R.R.
      Evolutionary steps of ecophysiological adaptation and diversification of ruminants: A comparative view of their digestive system.
      concluded that its simple structure permits it to serve as little more than a “sieving screen” that prevents large particles from entering the abomasum. In large, grazing ruminants, the omasum is large and with many laminae (
      • Hofmann R.R.
      The Ruminant Stomach: Stomach Structure and Feeding Habits of East African Game Ruminants.
      ,
      • Hofmann R.R.
      Evolutionary steps of ecophysiological adaptation and diversification of ruminants: A comparative view of their digestive system.
      ;
      • Langer P.
      The Mammalian Herbivore Stomach: Comparative Anatomy, Function and Evolution.
      ;

      van Wieren, S. E. 1996. Digestive strategies in ruminants and nonruminants. PhD Diss. Wageningen Univ., Wageningen, the Netherlands.

      ). Whereas the omasum in these species still helps retain particles (
      • Langer P.
      The Mammalian Herbivore Stomach: Comparative Anatomy, Function and Evolution.
      ), its large surface area may additionally contribute to absorption (
      • Hofmann R.R.
      The Ruminant Stomach: Stomach Structure and Feeding Habits of East African Game Ruminants.
      ,
      • Hofmann R.R.
      Evolutionary steps of ecophysiological adaptation and diversification of ruminants: A comparative view of their digestive system.
      ) and presumably other more advanced functions (e.g., fiber fermentation).
      We thus find a progression in omasal form and function from the tragulids to browsing and then grazing Pecoran ruminants. This progression suggests the omasum originally evolved as a simple isthmus that acted as a “floodgate” (
      • Bost J.
      Omasal physiology.
      ) to retain particles. Compartmentalization, well-developed laminae, and complex motor activity subsequently evolved to support absorption, fiber fermentation, and suction-based digesta flow control. These more derived functions indeed have some adaptive benefit, particularly for grazers, for which they may help process large amounts of refractory fiber (
      • Hofmann R.R.
      The Ruminant Stomach: Stomach Structure and Feeding Habits of East African Game Ruminants.
      ,
      • Hofmann R.R.
      Evolutionary steps of ecophysiological adaptation and diversification of ruminants: A comparative view of their digestive system.
      ;
      • Van Soest P.J.
      Nutritional Ecology of the Ruminant.
      ). Nevertheless, considering that the particle retention function is pervasive across all species and is the impetus for the evolution of the omasum, this function would seem to be of primary importance.

      Dietary Niche Separation and Mixed-Species Grazing

      Certain elements of this argument have also been presented by
      • Walker J.W.
      Multispecies grazing: The ecological advantage.
      . Studies on the African Serengeti support the use of mixed-species grazing systems—that is, systems in which pastures are stocked with more than one livestock species simultaneously. In their seminal studies,
      • Gwynne M.D.
      • Bell R.H.V.
      Selection of vegetation components by grazing ungulates in the Serengeti National Park.
      and
      • Bell R.H.V.
      The use of the herb layer by grazing ungulates in the Serengeti.
      ,
      • Bell R.H.V.
      A grazing ecosystem in the Serengeti.
      showed that when an occupied area of the Serengeti plains becomes overgrazed, African buffalo and zebra are the first to migrate into ungrazed regions of long, poor-quality grass. As they remove the top herbage layer (stems and leaves of mature grasses), they expose lower, high-quality layers (stems, leaves, and fruits of immature grass and browse), which wildebeest, topi, and Thompson's gazelle then graze as they move in succession. By occupying different dietary niches, these ruminants and zebras together not only successfully occupy the same habitat, but also use grasslands more efficiently and completely.
      Two primary reasons explain why these species occupy different dietary niches and thus can exist sympatrically (i.e., in the same geographic area). First, these species exhibit innately different dietary selectivities (i.e., feeding classes) that would immediately suggest the observed dietary niches; the buffalo and zebra are strict grazers, the wildebeest and topi are more selective grazers, and the Thompson's gazelle is an intermediate feeder (
      • Gwynne M.D.
      • Bell R.H.V.
      Selection of vegetation components by grazing ungulates in the Serengeti National Park.
      ;
      • Bell R.H.V.
      The use of the herb layer by grazing ungulates in the Serengeti.
      ,
      • Bell R.H.V.
      A grazing ecosystem in the Serengeti.
      ;
      • Hofmann R.R.
      The Ruminant Stomach: Stomach Structure and Feeding Habits of East African Game Ruminants.
      ,
      • Hofmann R.R.
      Evolutionary steps of ecophysiological adaptation and diversification of ruminants: A comparative view of their digestive system.
      ). Second, these species range greatly in BW; the Thompson's gazelle and buffalo, the smallest and largest of the species, weigh 16 and 447 kg (
      • Gwynne M.D.
      • Bell R.H.V.
      Selection of vegetation components by grazing ungulates in the Serengeti National Park.
      ;
      • Bell R.H.V.
      The use of the herb layer by grazing ungulates in the Serengeti.
      ,
      • Bell R.H.V.
      A grazing ecosystem in the Serengeti.
      ). Because VFI scales with BW0.9 whereas metabolic requirements scale only with BW0.75 (Table 6), nutrient intake increases relative to metabolic requirements with increasing BW. Consequently, large species can adapt to poor-quality material because they can consume relatively large amounts to meet their metabolic requirements, whereas smaller species are constrained to higher quality material because they can eat relatively little (
      • Bell R.H.V.
      The use of the herb layer by grazing ungulates in the Serengeti.
      ,
      • Bell R.H.V.
      A grazing ecosystem in the Serengeti.
      ;
      • Jarman P.J.
      The social organization of antelope in relation to their ecology.
      ;

      Hackmann, T. J. 2008. Studies of ruminant digestion, ecology, and evolution. MS Thesis. Univ. Missouri, Columbia.

      ). This principle (the Bell-Jarman principle;

      Geist, V. 1974. On the relationship of ecology and behavior in the evolution of ungulates: Theoretical considerations. Pages 235–246 in The Behavior of Ungulates and Its Relation to Management. V. Geist and F. R. Walther, ed. New Series No. 24. IUCN Publications, Morges, Switzerland.

      ) further reinforces innate selectivity differences to establish different dietary niches.
      Significantly, major livestock species (goat, sheep, cattle) differ greatly in feeding class, BW, or both (Table 5). Probably as a combination of these factors, species choose diets that overlap incompletely: as goats choose more browse, cattle choose more grass, and sheep are intermediate (Figure 4). Diets should be even less similar than Figure 4 might suggest because 1) Figure 4 shows ranges that apply to single-species grazing, and cattle shift to poorer quality diets in their range when grazing with sheep (
      • Walker J.W.
      Multispecies grazing: The ecological advantage.
      ); 2) sheep eat plant biomass soiled by cattle feces, which cattle themselves avoid (
      • Nolan T.
      • Connolly J.
      Mixed versus mono grazing of steers and sheep.
      ); and 3) the rough expression of botanical composition shown in Figure 4 ignores other ways diets can differ (e.g., by plant species or part). Livestock species thus have ample opportunity to separate their dietary niches when grazed concurrently.
      Figure thumbnail gr4
      Figure 4Botanical composition (% of grass and browse) of diets chosen by goats (n = 13), sheep (n = 105), and cattle (n = 121) on pasture. Bars delineate mean ± SD. Data are from
      • Van Dyne G.M.
      • Brockington N.R.
      • Szocs Z.
      • Duek J.
      • Ribic C.A.
      Large herbivore subsystem.
      .
      Given this probable dietary niche separation, one might expect mixed-grazing systems to lead to more complete utilization of pasture and a higher combined level of animal productivity (because more pasture is transformed into animal tissue). In support,
      • Vallentine J.F.
      Grazing Management.
      observed that the extent of pasture use can be increased by 25% by using multi- vs. single-species grazing, and
      • Walker J.W.
      Multispecies grazing: The ecological advantage.
      found that multispecies grazing increased animal BW gain by 9 and 24% per unit area compared with sheep- and cattle-only systems, respectively.
      Some legitimate, practical limitations to mixed-species grazing exist, such as elevated facility costs and predation risk of sheep and goats (
      • Vallentine J.F.
      Grazing Management.
      ). However, most barriers are social, based on tradition and prejudice toward species (
      • Walker J.W.
      Multispecies grazing: The ecological advantage.
      ). However, the enhanced production and efficiency of the systems compared with conventional ones—as expected from the archetypal mixed-grazing system on the Serengeti—challenge these barriers.

      Extended Lactation

      Elements of this discussion are derived from
      • Knight C.H.
      Lactation and gestation in dairy cows: Flexibility avoids nutritional extremes.
      . The aim of many dairy cow operations is a 305-d lactation with a 12- to 14-mo calving interval. This requires cattle to be rebred by 100 d after parturition, soon after peak lactation, when they experience a negative energy balance (
      • Bauman D.E.
      • Currie W.B.
      Partitioning of nutrients during pregnancy and lactation: A review of mechanisms involving homeostasis and homeorhesis.
      ) and other metabolic stresses that severely reduce fertility (
      • Chagas L.M.
      • Bass J.J.
      • Blache D.
      • Burke C.R.
      • Kay J.K.
      • Lindsay D.R.
      • Lucy M.C.
      • Martin G.B.
      • Meier S.
      • Rhodes F.M.
      • Roche J.R.
      • Thatcher W.W.
      • Webb R.
      New perspectives on the roles of nutrition and metabolic priorities in the subfertility of high-producing dairy cows.
      ). With pregnancy rates of US breeds averaging about 25% (

      Animal Improvement Programs Laboratory. 2008. Cow genetic trends. USDA, Beltsville, MD. http://aipl.arsusda.gov/eval/summary/trend.cfm Accessed Oct. 13, 2008.

      ), this management strategy is largely untenable.
      One alternative management approach, forwarded by
      • Knight C.H.
      Mammary growth and development: Strategies of animals and investigators.
      and others, is to purposely extend lactation as long as possible and thus avoid early rebreeding. This approach, compared with current practice, indeed appears to be better supported by ecological observations. When in severe metabolic stress (poor body condition or nutritional plane) during lactation, many wild species [muskoxen (
      • Adamczewski J.Z.
      • Fargey P.J.
      • Laarveld B.
      • Gunn A.
      • Flood P.F.
      The influence of fatness on the likelihood of early-winter pregnancy in muskoxen (Ovibos moschatus).
      ), red deer (
      • Loudon A.S.I.
      • McNeilly A.S.
      • Milne J.A.
      Nutrition and lactational control of fertility in red deer.
      ;
      • Albon S.D.
      • Mitchell B.
      • Huby B.J.
      • Brown D.
      Fertility in female red deer (Cervus elaphus): The effects of body composition, age and reproductive status.
      ), caribou (
      • Gerhart K.L.
      • Russell D.E.
      • van de Wetering D.
      • White R.G.
      • Cameron R.D.
      Pregnancy of adult caribou (Rangifer tarandus): Evidence for lactational infertility.
      )] will not rebreed or do so only at low rates. Instead of rebreeding, they may extend lactation and thus invest in their current young [caribou (
      • White R.G.
      • Luick J.R.
      Plasticity and constraints in the lactational strategy of reindeer and caribou.
      ); muskoxen (
      • Knight C.H.
      Lactation and gestation in dairy cows: Flexibility avoids nutritional extremes.
      )]. In muskoxen, this extended lactation can exceed 1 yr (
      • Adamczewski J.Z.
      • Flood P.F.
      • Gunn A.
      Seasonal patterns in body composition and reproduction of female muskoxen (Ovibos moschatus).
      ). As explained by
      • Knight C.H.
      Lactation and gestation in dairy cows: Flexibility avoids nutritional extremes.
      , extending lactation is presumably a maternal strategy to maximize fitness (the most important biological drive of organisms); investing in current offspring by extending lactation is safer and, in the long term, more profitable than producing new offspring when necessary nutritional resources are inadequate.
      These observations of wild species suggest that when under metabolic stress, the ruminant animal is evolutionarily entrained to continue lactation rather than rebreed. Attempting to rebreed the high-producing dairy cow soon (60 d) after parturition is a direct fight against this entrained response. If producing replacement heifers is not a major production goal, it might make more sense to rebreed less frequently and exploit the physiological capacity and drive for extended lactation shown in wild ruminants.
      Although this argument for extended lactation is largely conceptual, growing experimental evidence suggests practicing extended lactation is viable and profitable. Lactation has been maintained naturally in goats for 4 yr (
      • Linzell J.L.
      Innate seasonal oscillations in the rate of milk secretion in goats.
      ) and in cattle for nearly 2 yr (
      • Auldist M.J.
      • O’Brien G.
      • Cole D.
      • Macmillan K.L.
      • Grainger C.
      Effects of varying lactation length on milk production capacity of cows in pasture-based dairying systems.
      ); with bST supplementation, it has been maintained for more than 2 yr in cattle (
      • van Amburgh M.E.
      • Galton D.M.
      • Bauman D.E.
      • Everett R.W.
      Management and economics of extended calving intervals with use of bovine somatotropin.
      ). Milk production far into an extended lactation is less than around peak, but it is more than with production of a rebred animal during late pregnancy and its dry period (Figure 5). All predesigned experiments have demonstrated that, over the long term, extending lactation up to 16 mo (and sometimes longer) does not decrease daily production (
      • van Amburgh M.E.
      • Galton D.M.
      • Bauman D.E.
      • Everett R.W.
      Management and economics of extended calving intervals with use of bovine somatotropin.
      ;
      • Rehn H.
      • Berglund B.
      • Emanuelson U.
      • Tengroth G.
      • Philipsson J.
      Milk production in Swedish dairy cows managed for calving intervals of 12 and 15 months.
      ;
      • Arbel R.
      • Bigun Y.
      • Ezra E.
      • Sturman H.
      • Hojman D.
      The effect of extended calving intervals in high lactating cows on milk production and profitability.
      ;
      • Österman S.
      • Bertilsson J.
      Extended calving interval in combination with milking two or three times per day: Effects on milk production and milk composition.
      ;
      • Salama A.A.K.
      • Caja G.
      • Such X.
      • Casals R.
      • Albanell E.
      Effect of pregnancy and extended lactation on milk production in dairy goats milked once daily.
      ;
      • Auldist M.J.
      • O’Brien G.
      • Cole D.
      • Macmillan K.L.
      • Grainger C.
      Effects of varying lactation length on milk production capacity of cows in pasture-based dairying systems.
      ). In some cases, extending lactation has increased either total milk (second lactation of primiparous cows;
      • Arbel R.
      • Bigun Y.
      • Ezra E.
      • Sturman H.
      • Hojman D.
      The effect of extended calving intervals in high lactating cows on milk production and profitability.
      ) or component (protein and fat of goats;
      • Salama A.A.K.
      • Caja G.
      • Such X.
      • Casals R.
      • Albanell E.
      Effect of pregnancy and extended lactation on milk production in dairy goats milked once daily.
      ) yields. The economic advantage of extended lactation ranged from $0.12 to 0.21/(d of calving interval) among treatment groups in
      • Arbel R.
      • Bigun Y.
      • Ezra E.
      • Sturman H.
      • Hojman D.
      The effect of extended calving intervals in high lactating cows on milk production and profitability.
      and $0.75/(d of productive life) in
      • van Amburgh M.E.
      • Galton D.M.
      • Bauman D.E.
      • Everett R.W.
      Management and economics of extended calving intervals with use of bovine somatotropin.
      . [Note that earlier studies claiming no positive economic response (e.g.,
      • Holmann F.J.
      • Shumway C.R.
      • Blake R.W.
      • Schwart R.B.
      • Sudweeks E.M.
      Economic value of days open for Holstein cows of alternative milk yields with varying calving intervals.
      ) were observational or theoretical, not experimental.] Although more research is clearly needed, these preliminary results suggest that the biological principles of extended lactation, as elucidated by wild ruminants, may be of great service to livestock production systems.
      Figure thumbnail gr5
      Figure 5Milk production of extended versus conventional lactations of multiparous Muriciano-Granadina goats milked once daily. Open (○) and closed (●) symbols represent production of goats managed for kidding intervals of 12 mo (K12) and 24 mo (K24), respectively. Arrows labeled a and b highlight where milk production of an extended lactation is greater (during pregnancy and the dry period of K12 goats) and less (during peak lactation of K12 goats) than conventional lactation. The first and second asterisks near the x-axis indicate times that K12 and all goats were rebred, respectively. Figure modified from
      • Salama A.A.K.
      • Caja G.
      • Such X.
      • Casals R.
      • Albanell E.
      Effect of pregnancy and extended lactation on milk production in dairy goats milked once daily.
      .

      Conclusions

      By offering a comparative vantage point, ruminant ecological and evolutionary research can offer valuable insight into livestock research. This research can reinforce and augment some conventional livestock practices, and if we allow, can challenge and help revise others. With further dialogue and cooperation between animal scientists and ecologists, the insights that ruminant ecology and evolution have to offer should grow in number and usefulness.

      Acknowledgments

      We acknowledge Benjamin Nielson (University of Missouri–Columbia) for laboratory support. Financial support is from the Missouri Agricultural Experiment Station (Columbia). Additional financial support for T. J. H. was provided by the C. W. Turner Graduate Scholarship (University of Missouri–Columbia).

      Appendix.

      Global population estimates of wild ruminants were compiled from several sources (
      • Whitehead G.K.
      Deer of the World.
      ;
      • Ohtaishi N.
      • Gao Y.
      A review of the distribution of all species of deer (Tragulidae, Moschidae and Cervidae) in China.
      ;

      East, R. 1999. African Antelope Database 1998. International Union for Conservation of Nature/Species Survival Commission Antelope Specialist Group, Gland, Switzerland.

      ;
      • Nowak R.M.
      ;
      • Wiener G.
      • Jianlin H.
      • Ruijun L.
      The Yak.
      ;
      ;
      • Zhou Y.
      • Meng X.
      • Feng J.
      • Yang Q.
      • Feng Z.
      • Xia L.
      • Bartos L.
      Review of the distribution, status and conservation of musk deer in China.
      ;

      International Union for Conservation of Nature. 2008. European Mammal Assessment. http://iucnredlist.org/search Accessed Sep. 9, 2008.

      ), many of which are compilations themselves. We excluded from our estimates domesticated, feral, captive, and nonnatively introduced populations or species. We also excluded species for which estimates were judged very fragmentary (that included only a few isolated or subspecies populations) and were unlikely to approach anything of a global estimate.
      In all, we obtained estimates for 150 species (78% of total). This includes 1 species from Antilocapridae (100% of family total), 116 from Bovidae (83% of total), 26 from Cervidae (63% of total), 2 from Giraffidae (100% of total), 4 from Moschidae (80% of total), and 1 from Tragulidae (25% of total). Poor or nonexistent census data account for missing species. In addition, note that estimates for many Asian species include numbers only in China, again because of poor census data.
      The population sizes reported here are clear underestimates. In total, they are still more comprehensive and up-to-date than the last apparent global census (
      • McDowell R.E.
      Ruminant Products: More Than Meat and Milk.
      ), which estimated population numbers for only 11 species (excluding feral and currently unrecognized species) in 2 families (Bovidae, Cervidae), for a total of 27 million ruminants overall.

      Supplementary data

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