- Email: [email protected]
Chewing behaviour in the domestic donkey (Equus asinus) fed fibrous forage
Applied Animal Behaviour Science 60 Ž1998. 241–251
Short communication
Chewing behaviour in the domestic donkey žEquus asinus / fed fibrous forage P.J. Mueller a b
a,)
, P. Protos b, K.A. Houpt b, P.J. Van Soest
a
Department of Animal Science, Cornell UniÕersity, Ithaca, NY 14853, USA College of Veterinary Medicine, Cornell UniÕersity, Ithaca, NY 14853, USA
Abstract A study was conducted to investigate chewing activity in domestic donkeys eating long-stem, high-fiber forage. Five donkeys Žbody weight 198 " 15 kg. were fed 2 types of forage containing equal amounts of fiber Ž65% neutral detergent fiber: NDF. at two levels of crude protein ŽCP.. Forage consumed was either a mixed legumerorchard grass hay ŽCP 13.7%. or a grass hay ŽCP 6.5%.. Chewing rate Žchewsrmin. and rate of feed consumption Žminrkg of dry matter ŽDM. or of NDF. were determined by direct observation. The study was designed as a two-period cross-over design with 3 sets of observations per animal per diet. There was no significant effect of protein level or forage type on average chewing rate Ž53 " 2 chewsrmin., time to consume 1 kg of DM Ž120 " 12 min. or 1 kg of NDF Ž184 " 18 min.. Chewing rate was no different at the start vs. end of a 1-h meal for animals eating mixed legumergrass hay, but was significantly Ž P - 0.05. slower later in the meal for donkeys eating grass hay. Each gram of NDF was chewed approximately 10 times. Donkeys consumed fiber at a faster rate than has been reported for equal or greater-sized ruminants, even though they did not chew at a faster speed. This behaviour could be due to a more efficient tooth and jaw apparatus, the swallowing of larger feed particles, or a combination of factors, and supports the postulated high intake feeding strategy of the donkey. Some donkeys may be prone to consume food, even forage, especially fast, without sufficient chewing, and may therefore be liable to esophageal obstruction. q 1998 Elsevier Science B.V. All rights reserved. Keywords: Chewing rate; Mastication; Intake; NDF; Equids
)
Corresponding author. Department of Physiology, UCLA School of Medicine, 10833 Le Conte Ave., Los Angeles, CA 90095-1751, USA. Tel.: q1-310-825-6076; fax: q1-310-206-5661. 0168-1591r98r$ - see front matter q 1998 Elsevier Science B.V. All rights reserved. PII: S 0 1 6 8 - 1 5 9 1 Ž 9 8 . 0 0 1 7 1 - 3
242
P.J. Mueller et al.r Applied Animal BehaÕiour Science 60 (1998) 241–251
1. Introduction Chewing activity is an important aspect of feeding behaviour in donkeys Ž Equus asinus .. All herbivorous mammals, especially those that derive energy from microbial fermentation of fiber, must chew their food in order prepare it for digestion. Chewing fragments plant cells, reduces the size of feed particles, promotes salivary secretion and allows wetting of feed. Ruminants chew upon initial ingestion Žmastication. and again during rumination. Non-ruminant herbivores, including donkeys, have only one opportunity, during mastication, to complete the physical processing of feed. The amount of time an individual herbivore spends chewing a given amount of food is affected by a variety of factors, including the animal’s species, body size, physiologic state, level of intake, amount of fiber in the diet, physical form of the feed, and the size of the feed particles. Numerous studies of chewing activity have been conducted with cattle, especially dairy cattle, as well as with sheep and goats ŽFujihara, 1980; Hooper and Welch, 1982; Woodford and Murphy, 1988; Luginbuhl et al., 1989a; Beauchemin, 1991a; Campbell et al., 1992; Beauchemin et al., 1994a; Dado and Allen, 1994; Warly et al., 1994.. In contrast, there is little available information on horses ŽGallagher and Hintz, 1988; Scott and Potter, 1989; Constable et al., 1994. and none for donkeys. In the semi-arid regions where the donkey evolved and is most commonly found today, food resources are often limited and of poor quality. Animals must be efficient consumers and processors of these limited resources in order to survive and compete with other species. Donkeys appear able to maintain body condition better than cattle during the dry season, when food is in particularly short supply Žpers. obs... This ability to conserve body reserves may be due to decreased metabolic requirements, increased selectivity for highly nutritious plant parts, tolerance of undesirable foods, or increased consumption and passage of fibrous foods. Probably some combination of strategies is employed. Several authors ŽJanis, 1976; Duncan et al., 1990. have proposed that the equids use a strategy of high intake, rapid transit and low nutrient extraction per unit of feed to compete with ruminants in high fiber environments. In the ruminant, feed particles must be reduced to a size small enough to pass out of the rumen, whereas equids are not similarly constrained. In order to achieve a high rate of intake, one feeding strategy might involve rapid chewing. We hypothesized that the donkey, a small equid, might chew faster and therefore consume feed faster than a ruminant. In this study, we investigated the rate at which donkeys chew forages, and the rate at which feed is ingested, to determine baseline data for this species. Forages are the above-ground portion of herbaceous plants ŽNational Research Council, 1989., characterized as coarse, bulky and containing more than 22% acid detergent fiber. We fed only forages, not grains, since grass, hay, browse and crop residues are the usual feeds of both feral and domestic donkeys in the arid tropical locations where the species evolved and thrives. Recent reports have suggested that, although body size and dietary fiber intake have the greatest effect on chewing activity, fiber source or type ŽWoodford and Murphy, 1988; Campbell et al., 1992. and amount of dietary protein ŽWarly et al., 1994. can also affect chewing. Although determination of the chewing response to different levels of dietary fiber is of interest, we held fiber
P.J. Mueller et al.r Applied Animal BehaÕiour Science 60 (1998) 241–251
243
constant in order to investigate the effects of fiber source and protein content by feeding two forages containing different amounts of protein but equal levels of neutral detergent fiber ŽNDF. from different plant sources.
2. Materials and methods 2.1. Animals and diets Five domestic donkeys Žthree male, two female, mean body weight 198 " 15 kg. were housed in individual box stalls with daily turn-out in a dry lot. Animals were fed one of two forages Žmixed hay or grass hay: see Table 1. ad libitum twice daily except when feed was removed for 8 h preceding a chewing observation. Salt and water were provided free choice; no food other than the assigned forage was allowed. All animals received both diets in a two-period cross-over design. Following seven days of adaptation to the diet, daily food intake was recorded for 21 days, after which chewing observations were made. Forages fed were Ž1. a mixed legumerorchard grass hay and Ž2. a grass hay. Both forages were highly fibrous, as measured by neutral detergent fiber ŽNDF. content. The nutrient composition is shown in Table 1. The two forages were very similar in all nutritive components compared except crude protein ŽCP., which was more than twice as high in the hay containing legume Ž13.7 vs. 6.5%.. Selected bales were identified for each animal so that an animal always ate from the same bale when being observed. Hay samples were analyzed from each bale used during observational studies so that NDF intake could be accurately assessed; average values appear in Table 1. Fiber varied up to 2% among bales. Pooled samples of all hay fed over the adaptation and intake phase were found to be identical in nutrient composition to the individual bales fed during chewing observations. 2.2. Chewing obserÕations Chewing data were collected by visual observation of donkeys eating. Two animals required adaptation to the presence of the observer Žaccomplished through three half-hour
Table 1 Fiber and protein concentrations of forages
Dry matter Ž%. Crude protein Ž% of DM. Neutral detergent Fiber Ž% of DM. Acid detergent fiber Ž% of DM. Ash Ž% of DM. H 2 SO4 lignin Ž% of DM.
Mixed hay
Grass hay
91.5 13.7 64.6 44.9 5.3 8.1
91.8 6.5 65.8 43.8 4.2 7.3
244
P.J. Mueller et al.r Applied Animal BehaÕiour Science 60 (1998) 241–251
Table 2 Chewing activity of donkeys fed forages Ž ns 5., presented as means"S.E. Mixed hay
Grass hay
120"10 183"17
121"18 185"26
Chewing rate (no.r min) Early-meal Late-meal Average
54"4 59"2 a 53"4
52"4 48"1b 54"1
Chewsr g of DM of NDF
6.2"0.3 9.5"0.5
6.5"0.8 9.9"1.2
Time to eat (min. per kg DM per kg NDF
a,b
Means in the same row with unlike letters differ significantly Ž P - 0.05..
sessions. before they would eat under scrutiny. The other three animals ate readily at all times. Since one person could not make all observations required for the experiment, to minimize intra-animal variation one individual was assigned to each donkey; inter-observer variation, however, was not assessed. Observations were made at the same time of day for each animal. The observer sat in plain view and watched the animal, which stood untethered in its customary box stall. To ensure that donkeys would eat, food was removed for 8 h preceding an observation period. Two types of observations were conducted: Ž1. measurement of time to consume feed, and Ž2. determination of chewing rate. For the former, animals were offered a weighed amount of hay and monitored for one hour to determine both the amount of food eaten in 1 h and the minutes spent chewing Žby recording activity each minute.. Chewing rate Žchewsrmin. was determined both at the start Žtermed ‘early-meal’. and at the finish Žtermed ‘late-meal’. of the 1-h eating bout, as follows: animals were offered a known amount of forage and observed. The observer counted chews during a 2- to 5-min bout of continuous chewing. Counting of jaw movement stopped when chewing ceased for more than 5 s, or after 5 min of continuous chewing, whichever came first. Three such bouts were observed and averaged to give early-meal chewing rate on a given day. This was followed by 1 h of
Table 3 Intake of forages by donkeys Ž ns 5., presented as means"S.E.
Dry matter ŽDM. Žkgrday. NDF Žkgrday. Water Žlrday. DM Žkgr100 kg of BW. NDF Žkgr100 kg of BW. BW Žkg.
Mixed hay
Grass hay
3.9"0.5 2.4"0.7 8.7"1.6 1.9"0.4 1.2"0.2 200"15
3.5"0.4 2.2"0.6 8.7"1.4 1.8"0.3 1.1"0.2 197"15
P.J. Mueller et al.r Applied Animal BehaÕiour Science 60 (1998) 241–251
245
food consumption with observation, as described above. The 1-h eating period was termed a meal. Therefore, after 1 h of eating, the chewing rate observations were repeated to determine late-meal chewing rate. Each complete set of observations was repeated three times per animal, on separate days, after which diets were reversed and the experiment repeated. 2.3. Laboratory and statistical analyses Forage samples were ground to pass through a 1-mm screen, dried at 608C and analyzed for nutritional constituents according to Van Soest et al. Ž1991.. Reported values are means " S.E. Diet effects were compared using paired t-tests.
3. Results Chewing activity for donkeys eating the two forages is shown in Table 2. There were no significant Ž P ) 0.05. differences due to forage type in any of the studied variables, with one exception. Only in the animals eating grass hay did chewing rate slow Ž P - 0.05. after one hour’s access to feed. Because of the lack of significant differences between forage types, data were pooled across the two diets. Donkeys consumed an average of 9.0 " 0.7 g of dry matter ŽDM. per minute, chewing 53 " 2 timesrmin. They required 120 " 12 min to eat one kg of DM, and 184 " 18 min to eat 1 kg of NDF. During the 3-week measurement period, there was no significant difference in intake between the two forages ŽTable 3.. Animals were able to maintain their body weight on either forage fed alone, despite the low CP content of the grass hay.
4. Discussion 4.1. Allometry of chewing efficiency Chewing efficiency is a measure of the amount of chewing time required for the physical processing of a unit of food. For clarity, in ruminants, initial chewing upon ingestion will be referred to as eating or mastication, while the term chewing itself is used to describe the combined total of eating plus rumination chews. Total chewing time is the most relevant measure to use when comparing the ruminant to the non-ruminant, for whom chewing consists only of eating. In this study, prehension was not distinguished from mastication, as the donkeys tended to continue chewing previously prehended feed when taking new bites. Chewing efficiency is positively correlated with body size in ruminants, both within ŽBae and Gilman, 1983. and across species ŽWelch, 1982.. Larger animals need less time and fewer chews per unit of feed than do small animals. In a comparative study ŽWelch, 1982., mature cows Ž560 kg. ruminated 1 kg of NDF for 100 min, while sheep Ž82 kg. ruminated 1180 min and goats Ž39 kg. ruminated 1300 min. Such differences in chewing efficiency may be related to mouth size and hence bite size, tooth area and jaw strength.
246
P.J. Mueller et al.r Applied Animal BehaÕiour Science 60 (1998) 241–251
Minutes of total chewing per kg DM ingested has been used as a measure of chewing efficiency but is highly variable. The literature contains values for cattle ranging from 25–35 min ŽJaster and Murphy, 1983; Woodford and Murphy, 1988; Beauchemin, 1991a; Colenbrander et al., 1991; Beauchemin et al., 1994b; Constable et al., 1994; Dado and Allen, 1994. to as high as 130 min per kg DM ŽBeauchemin and Iwassa, 1993., while sheep vary from 400 ŽCammell and Osbourn, 1972; Weston, 1988. to over 1000 min per kg DM ŽFujihara, 1980; Inoue´ et al., 1994; Warly et al., 1994.. Horses apparently can eat 1 kg of grain in 6 to 13 min ŽHintz et al., 1989; Scott and Potter, 1989. and 1 kg of hay in 25–50 min ŽGallagher and Hintz, 1988; Constable et al., 1994.. Donkeys in the present study spent 120 min chewing 1 kg of forage DM; therefore, their behaviour most closely resembled published data for cattle rather than that for horses or sheep. A better criterion for comparison of chewing efficiency is chewing time per unit of NDF, since fiber content is a principal determinant of requisite chewing time. When fed mixtures of concentrate and forage, dairy cattle required 30–60 min to eat a kg of NDF and an additional 50–100 min of rumination to complete the physical processing of the feed ŽWoodford and Murphy, 1988; Beauchemin and Buchanan-Smith, 1989; Beauchemin, 1991b; Colenbrander et al., 1991; Beauchemin et al., 1994a; Dado and Allen, 1994.. Limited studies in which cattle were fed forage-only diets show different results: 100 min for mastication of 1 kg of NDF plus 100–150 of rumination, for a total chewing time per kg NDF of 200–250 min ŽWelch, 1982; Luginbuhl et al., 1989a; Beauchemin and Iwassa, 1993.. Small ruminants such as sheep and goats are much less efficient fiber processors, requiring from 700 to over 1000 min to chew 1 kg of NDF when fed forage-only diets ŽCammell and Osbourn, 1972; Chai et al., 1985; Warly et al., 1994.. The donkeys in the present study accomplished the physical processing of forage NDF at a rate of 184 min per kg fiber. This is only slightly slower than has been reported in cows. If data are adjusted for body weight or metabolic body size, the donkey would appear capable of consuming forage NDF two to three times faster than previously reported in cattle, although the type of fiber fed and animal satiety state could also have contributed to these apparent interspecific differences. Bae and Gilman Ž1983. developed a regression equation, using cattle from 260 to 860 kg BW, to describe chewing efficiency based on body size. Their equation would predict that the donkey should require 261 min to chew 1 kg of fiber; in fact the donkeys in this study required only 184 min. Bae and Gilman used a medium quality Ž65% NDF. long-stem grass hay, a diet very similar to that fed to the donkeys in the present study. This suggests that the donkey can chew long fiber as efficiently or more efficiently than a much larger ruminant, although differences in experimental design between Bae and Gilman and the present study preclude definitive comparison. Is the allometry of chewing conserved, although at a different calibration, within the equids: do horses chew more efficiently than donkeys? Preliminary data from Constable et al. Ž1994., wherein three horses required only 60 to 80 min of chewing per kg of NDF when fed various types of hay, with the smallest horse chewing longest, would suggest that the allometry holds. Similarly, Hintz et al. Ž1989. found that horses consumed grain nearly twice as fast as ponies that were much smaller.
P.J. Mueller et al.r Applied Animal BehaÕiour Science 60 (1998) 241–251
247
Why, and how, does the donkey consume fiber rapidly? Fast eaters must either chew fast, swallow large particles or be highly efficient at reducing particle size on each chew. Speed of chewing does not seem to differ among similar-sized species Žsee below.. If the donkey can consume forage faster than the ruminant, even ruminants of much larger size, then the donkey must either chew the food less Žresulting in larger digesta particles., or must achieve greater mastication efficiency in fewer chews. Possibly some combination of these strategies is used. The hindgut presents less impediment to digesta passage than does the rumen; hence, there is less necessity for the donkey to reduce feed particle size. However, the ingestion of larger particles may compromise digestion, including the digestion and absorption of soluble carbohydrates and protein in the small intestine where residence time may be short if intake is high. Although there is no information on fecal particle size in donkeys, fiber particles found in the feces of ponies are twice as large as those from cattle ŽVan Soest, 1994.. Rapid consumption of fiber implies that the donkey’s feeding behaviour also includes large intakes and minimal particle size reduction through mastication. Cattle have been observed to chew 14–20 times for each gram of hay NDF ingested ŽLuginbuhl et al., 1989a; Beauchemin and Iwassa, 1993; Beauchemin et al., 1994a,b., while sheep chew 70–100 times per gram of NDF ŽChai et al., 1985.. Horses fed hay chewed 4–6 times per gram of hay NDF ŽConstable et al., 1994.. The donkeys, however, chewed 9 times per gram of hay NDF. This indicates one way that the donkey, despite its smaller mouth, might process food at approximately the same rate as larger cattle: fewer chews per gram of food. A stronger jaw and larger molar surface may help the donkey chew each mouthful more effectively. Equids in general have a larger tooth surface area than similarly-sized ruminants, because all premolars are molariform ŽJanis, 1979., and there is greater masticatory musculature ŽTurnbull, 1970.. Whether the donkey has absolutely more tooth surface than the cow is unknown. 4.2. Speed of chewing Although it may vary with type of feed, the chewing rate of similarly-sized adult herbivores eating dried forage is relatively constant. Literature values for chewing speed of ponies, horses, dairy cattle and immature steers fed hay all lie between 49 and 72 chewsrmin ŽTable 4.. Sheep and goats may chew faster because the smaller size of their eating apparatus both allows and requires speed. Bae and Gilman Ž1983., however, found no difference in chewing speed across a 4-fold difference in body size in cattle. Donkeys in the present study chewed on average 54 times per min, similar to many published values for other species ŽTable 4.. The chewing rate observed varied from a low of 43 to as high as 62 chewsrmin, with a tendency for the smaller donkeys to chew more slowly than the larger. Donkeys appeared to process feed more slowly than has been reported for horses ŽGallagher and Hintz, 1988; Constable et al., 1994., which could be the result of a slightly slower chewing rate, or could reflect differences in particle size diminution. The latter could be a factor contributing to observed differences in fiber digestibility between horses and donkeys ŽPearson and Merritt, 1991.. However, the data for both horses and donkeys are from very small samples and have not been obtained within the same study, and thus one can only speculate until further information is obtained.
248
P.J. Mueller et al.r Applied Animal BehaÕiour Science 60 (1998) 241–251
Table 4 Rate of chewing a in selected ungulates Species
Feed
Chew Rate Žchewsrmin.
Reference
Donkey Pony Horse Horse Horse Dairy cow Dairy cow Dairy cow Dairy cow Steer Steer Sheep Sheep Sheep Goat
Hay Hay Hay Grain Fresh grass Hay Hay Hay Total mixed ration Hay Hay Rice Straw Hay Fresh grass Hay
54 49 72 55 35–50 77 40–53 74 62 71 59–65 70 71 120–150 87
This study Sarna, pers. comm. Constable et al., 1994 Scott and Potter, 1989 Mayes and Duncan, 1994 Constable et al., 1994 Brouk and Belyea, 1993 Gill et al., 1966 Dado and Allen, 1994 Luginbuhl et al., 1989b Luginbuhl et al., 1989a Warly et al., 1994 Fujihara, 1980 Inoue´ et al., 1994 Hooper and Welch, 1982
a
In ruminants, average of mastication and rumination rates, where these differ.
Cattle are sometimes seen to chew faster at the start of a meal than towards the end ŽLuginbuhl et al., 1989a., perhaps to produce large quantities of saliva for rumen buffering, or because they are hungrier. Later in the meal the buffering requirement is met and chewing speed decreases. For the mixed legumergrass hay, donkeys ate at the same speed both when first offered feed following 8 h without food, and after 1 h of eating. When fed grass hay, however, donkeys significantly slowed their chewing rate after 1 h. Although this behaviour resembled that reported for cattle, it cannot be for the same reason, as the donkey has no need to buffer a rumen. It is likely that the mixed forage, containing legume, was more palatable than the grass hay, hence the donkeys remained eager to continue eating even after 1 h of access to food. The grass hay, on the other hand, was dusty and less acceptable. After 1 h of eating, perhaps the donkeys’ motivation for eating diminished and their chewing rate slowed. 4.3. Effect of fiber source on chewing behaÕiour In ruminants, rumination time depends not only on the amount of fiber consumed, but also on fiber characteristics such as length, shape, fragility and specific gravity ŽChai et al., 1985.. Grass hay, the fiber of which breaks into long thin pieces, may elicit a different amount of chewing than alfalfa, which fractures into short round pieces ŽVan Soest, 1994.. In donkeys, however, there was no difference in chewing activity between grass fiber and mixed legumergrass fiber. Possibly the mixed hay did not contain enough legume to be appreciably different in fiber characteristics, or else this effect of fiber type appears only during rumination and hence is not seen in the donkey. 4.4. Effect of dietary protein concentration on chewing behaÕiour Protein-deficient diets may increase total chewing time in the ruminant because microbial digestion is depressed and, in order to maintain sufficient particle breakdown,
P.J. Mueller et al.r Applied Animal BehaÕiour Science 60 (1998) 241–251
249
the animal compensates by increasing rumination ŽWarly et al., 1994.. In a hind-gut fermenter such as the donkey, however, suppression of microbial digestion in the colon and cecum by insufficient dietary protein is unlikely to directly amplify the chewing response in compensation. Therefore, it is not surprising that protein concentration had no effect on chewing efficiency in this study. It may also be true that, although the grass hay had only 50% as much crude protein as the mixed forage, it still provided sufficient dietary protein for the donkey. Although the National Research Council Ž1989. recommends 8.0% protein for the maintenance of horses, no data are available for donkeys and the dietary concentration of 6.5% CP fed in this study was likely sufficient for them, especially at ad libitum intake. This hypothesis is supported by the observation that donkeys were able to maintain body weight for 3 weeks while eating the grass hay.
5. Conclusion Feeding behaviour of equids is thought to be characterized by large intakes with low nutrient extraction. High rates of intake can be achieved via rapid chewing, large bites, effective chewing per bite, or sacrifice in particle size reduction. Neither bite size nor particle size was measured in this study, and chewing rate of the donkey appeared similar to previously published rates for cattle. However, when scaled to either body size or to metabolic body size, donkeys may be able to consume NDF faster than cattle. Whether they do this solely through passage of large particles or through more efficient chewing, related to tooth and jaw structure, is unknown, but merits further study. The donkey differs somewhat from the horse because its narrow muzzle and mobile lips promote greater selectivity in feeding. This allows it to maximize feed quality rather than quantity, yet a relatively rapid intake ability was seen in this study. The donkey may use a selective feeding strategy, searching for high quality bites when foraging over a heterogeneous pasture or rangeland, but when provided with homogenous hay employs an alternative strategy of maximizing intake. In practice, donkeys faced with some perceived need to consume more food quickly, such as following an intentional or unintentional fast, or restricted time in which to eat due to insufficient feeder space, competition from herd mates or long hours spent working, may resort not to faster chewing but to incomplete chewing. This could result in problems such as esophageal obstruction Žchoke. and intestinal impaction. A donkey who ate rapidly following a period of food restriction did suffer from esophageal obstruction Žpers. obs... In contrast to results sometimes seen in cattle, fiber source and protein concentration, to the extent studied in this experiment, had no effect on rate of forage consumption in the donkey. Clearly, much more needs to be known about the donkey’s chewing activity when ingesting feeds of different fiber content, and about modulation of chewing activity in a natural foraging situation when food must be sought and selected rather than simply ingested. Further studies of the donkey, horse and other equids, especially in simultaneous, comparative studies, are of interest to determine whether the chewing behaviour of the donkey represents a unique solution to a feeding constraint, or is characteristic of a typical equid strategy in contrast to that of ruminants.
250
P.J. Mueller et al.r Applied Animal BehaÕiour Science 60 (1998) 241–251
Acknowledgements The authors are grateful to Kim Brockmann and Andrew Skol for patiently assisting with data collection, and to Dr. J.B. Robertson for assistance with laboratory analysis. This material is based upon work supported under a National Science Foundation Graduate Fellowship held by P.J. Mueller.
References Bae, D.H., Gilman, B.E., 1983. Mastication and rumination in relation to body size of cattle. J. Dairy Sci. 66, 2137–2141. Beauchemin, K.A., 1991a. Ingestion and mastication of feed by dairy cattle. Vet. Clin. North Am. Food Anim. Pract. 7, 439–463. Beauchemin, K.A., 1991b. Effects of dietary neutral detergent fiber concentration and alfalfa hay quality on chewing, rumen function, and milk production of dairy cows. J. Dairy Sci. 74, 3140–3151. Beauchemin, K.A., Iwassa, A.D., 1993. Eating and ruminating activities of cattle fed alfalfa or orchard grass harvested at two stages of maturity. Can. J. Anim. Sci. 73, 79–88. Beauchemin, K.A., Buchanan-Smith, J.G., 1989. Effects of dietary neutral detergent fiber concentration and supplementary long hay on chewing activities and milk production of dairy cows. J. Dairy Sci. 72, 2288–2300. Beauchemin, K.A., Farr, B.I., Rode, L.M., Schaalje, G.B., 1994a. Optimal neutral detergent fiber concentration of barley-based diets for lactating dairy cows. J. Dairy Sci. 77, 1013–1029. Beauchemin, K.A., McAllister, T.A., Dong, Y., Farr, B.I., Cheng, K.-J., 1994b. Effects of mastication on digestion of whole cereal grains by cattle. J. Anim. Sci. 72, 236–246. Brouk, M., Belyea, R., 1993. Chewing activity and digestive responses of cows fed alfalfa forages. J. Dairy Sci. 76, 175–182. Cammell, S.B., Osbourn, D.F., 1972. Factors influencing the total time spent chewing by sheep given diets containing long, dried forages. Proc. Nutr. Soc. 31, 63A–64A. Campbell, C.P., Marshall, S.A., Mandell, I.B., Wilton, J.W., 1992. Effects of source of dietary neutral detergent fiber on chewing behavior in beef cattle fed pelleted concentrates with or without supplemental roughage. J. Anim. Sci. 70, 894–903. Chai, K., Kennedy, P.M., Milligan, L.P., Mathison, G.W., 1985. Effects of cold exposure and plant species on forage intake, chewing behavior and digesta particle size in sheep. Can. J. Anim. Sci. 65, 69–76. Colenbrander, V.F., Noller, C.H., Grant, R.J., 1991. Effect of fiber content and particle size of alfalfa silage on performance and chewing behavior. J. Dairy Sci. 74, 2681–2690. Constable, E.C., Houpt, K.A., Janis, C.M., 1994. Effect of fiber content of feed on chewing rate. 65th Annual Meeting, Eastern Psychological Association, Providence, RI, Abstract. Dado, R.G., Allen, M.S., 1994. Variation in relationships among feeding, chewing, and drinking variables for lactating dairy cows. J. Dairy Sci. 77, 132–144. Duncan, P., Foose, T.J., Gordon, I.J., Gakahu, C.G., Lloyd, M., 1990. Comparative nutrient extraction from forages by grazing bovids and equids: a test of the nutritional model of equidrbovid competition and coexistence. Oecologia 84, 411–418. Fujihara, T., 1980. The eating and rumination behavior in sheep fed only grass diets in either fresh or dried form. J. Agric. Sci. ŽCamb.. 95, 729–732. Gallagher, J.R., Hintz, H.F., 1988. Rate of feed intake and horse health. Proc. Aust. Soc. Anim. Prod. 17, 399. Gill, J., Campling, R.C., Westgarth, D.R., 1966. A study of chewing during eating in the cow. Br. J. Nutr. 20, 13–23. Hintz, H.F., Schryver, H.F., Mallette, J., Houpt, K., 1989. Factors affecting rate of grain intake by horses. Equine Prac. 11, 35–42. Hooper, A.P., Welch, J.G., 1982. Chewing efficiency and body size of kid goats. J. Dairy Sci. 66, 2552–2556.
P.J. Mueller et al.r Applied Animal BehaÕiour Science 60 (1998) 241–251
251
Inoue, ´ T., Brookes, I.M., John, A., Hunt, W.F., Barry, T.N., 1994. Effects of leaf shear breaking load on the feeding value of perennial ryegrass Ž Lolium perenne) for sheep: II. Intake, particle breakdown, rumen digesta outflow and animal performance. J. Agric. Sci. ŽCamb.. 123, 137–147. Janis, C.M., 1976. The evolutionary strategy of the Equidae and the origins of rumen and cecal morphology. Evol. 30, 757–774. Janis, C.M., 1979. Aspects of the evolution of herbivory in ungulate mammals. PhD Thesis, Harvard Univ., Cambridge, MA. Jaster, E.H., Murphy, M.R., 1983. Effects of varying particle size of forage on digestion and chewing behavior of dairy heifers. J. Dairy Sci. 66, 802. Luginbuhl, J.-M., Pond, K.R., Burns, J.C., Russ, J.C., 1989a. Eating and ruminating behavior of steers fed coastal bermuda grass at four levels. J. Anim. Sci. 67, 3410–3418. Luginbuhl, J.-M., Pond, K.R., Burns, J.C., Russ, J.C., 1989b. Effects of ingestive mastication on particle dimensions and weight distribution of coastal bermuda grass hay fed to steers at four levels. J. Anim. Sci. 67, 538–546. Mayes, E., Duncan, P., 1994. Temporal patterns of feeding behaviour in free-ranging horses. Behav. 96, 105–129. National Research Council, 1989. Nutrient Requirements of Horses. National Academy Press, Washington, DC. Pearson, R.A., Merritt, J.B., 1991. Intake, digestion and gastrointestinal transit time in resting donkeys and ponies and exercised donkeys given ad libitum hay and straw diets. Equine Vet. J. 23, 339–343. Scott, B.D., Potter, G.D., 1989. Rate of feed consumption and chewing by mature horses fed diets with varying amounts of fiber. Proceedings of the 11th Equine Nutrition and Physiology Society, Oklahoma State University, Stillwater, OK, pp. 234–237. Turnbull, W.D., 1970. Mammalian masticatory apparatus. Fieldiana Geol. 18, 149–156. Van Soest, P.J., 1994. Nutritional Ecology of the Ruminant, 2nd edn. Cornell Univ. Press, Ithaca, NY. Van Soest, P.J., Robertson, J.B., Lewis, B.A., 1991. Methods for dietary fiber, neutral detergent fiber and nonstarch polysaccharides in relation to animal nutrition. J. Dairy Sci. 74, 3583–3597. Warly, L., Fariani, A., Mawuengegah, O.P., Matsui, T., Fujihara, T., Harumoto, T., 1994. Studies on the utilization of rice straw by sheep: IV. Effect of soybean meal and barley supplementation on eating and rumination behavior. Asian Australas. J. Anim. Sci. 7, 272–277. Welch, J.G., 1982. Rumination, particle size and passage from the rumen. J. Anim. Sci. 54, 885–894. Weston, R.H., 1988. Factors limiting the intake of feed by sheep: XII. Digesta load and chewing activities in relation to lactation and its attendant increase in voluntary roughage consumption. Aust. J. Agric. Res. 39, 671–677. Woodford, S.T., Murphy, M.R., 1988. Effect of forage physical form on chewing activity, dry matter intake and rumination of dairy cows in early lactation. J. Dairy Sci. 71, 674–686.
Short communication
Chewing behaviour in the domestic donkey žEquus asinus / fed fibrous forage P.J. Mueller a b
a,)
, P. Protos b, K.A. Houpt b, P.J. Van Soest
a
Department of Animal Science, Cornell UniÕersity, Ithaca, NY 14853, USA College of Veterinary Medicine, Cornell UniÕersity, Ithaca, NY 14853, USA
Abstract A study was conducted to investigate chewing activity in domestic donkeys eating long-stem, high-fiber forage. Five donkeys Žbody weight 198 " 15 kg. were fed 2 types of forage containing equal amounts of fiber Ž65% neutral detergent fiber: NDF. at two levels of crude protein ŽCP.. Forage consumed was either a mixed legumerorchard grass hay ŽCP 13.7%. or a grass hay ŽCP 6.5%.. Chewing rate Žchewsrmin. and rate of feed consumption Žminrkg of dry matter ŽDM. or of NDF. were determined by direct observation. The study was designed as a two-period cross-over design with 3 sets of observations per animal per diet. There was no significant effect of protein level or forage type on average chewing rate Ž53 " 2 chewsrmin., time to consume 1 kg of DM Ž120 " 12 min. or 1 kg of NDF Ž184 " 18 min.. Chewing rate was no different at the start vs. end of a 1-h meal for animals eating mixed legumergrass hay, but was significantly Ž P - 0.05. slower later in the meal for donkeys eating grass hay. Each gram of NDF was chewed approximately 10 times. Donkeys consumed fiber at a faster rate than has been reported for equal or greater-sized ruminants, even though they did not chew at a faster speed. This behaviour could be due to a more efficient tooth and jaw apparatus, the swallowing of larger feed particles, or a combination of factors, and supports the postulated high intake feeding strategy of the donkey. Some donkeys may be prone to consume food, even forage, especially fast, without sufficient chewing, and may therefore be liable to esophageal obstruction. q 1998 Elsevier Science B.V. All rights reserved. Keywords: Chewing rate; Mastication; Intake; NDF; Equids
)
Corresponding author. Department of Physiology, UCLA School of Medicine, 10833 Le Conte Ave., Los Angeles, CA 90095-1751, USA. Tel.: q1-310-825-6076; fax: q1-310-206-5661. 0168-1591r98r$ - see front matter q 1998 Elsevier Science B.V. All rights reserved. PII: S 0 1 6 8 - 1 5 9 1 Ž 9 8 . 0 0 1 7 1 - 3
242
P.J. Mueller et al.r Applied Animal BehaÕiour Science 60 (1998) 241–251
1. Introduction Chewing activity is an important aspect of feeding behaviour in donkeys Ž Equus asinus .. All herbivorous mammals, especially those that derive energy from microbial fermentation of fiber, must chew their food in order prepare it for digestion. Chewing fragments plant cells, reduces the size of feed particles, promotes salivary secretion and allows wetting of feed. Ruminants chew upon initial ingestion Žmastication. and again during rumination. Non-ruminant herbivores, including donkeys, have only one opportunity, during mastication, to complete the physical processing of feed. The amount of time an individual herbivore spends chewing a given amount of food is affected by a variety of factors, including the animal’s species, body size, physiologic state, level of intake, amount of fiber in the diet, physical form of the feed, and the size of the feed particles. Numerous studies of chewing activity have been conducted with cattle, especially dairy cattle, as well as with sheep and goats ŽFujihara, 1980; Hooper and Welch, 1982; Woodford and Murphy, 1988; Luginbuhl et al., 1989a; Beauchemin, 1991a; Campbell et al., 1992; Beauchemin et al., 1994a; Dado and Allen, 1994; Warly et al., 1994.. In contrast, there is little available information on horses ŽGallagher and Hintz, 1988; Scott and Potter, 1989; Constable et al., 1994. and none for donkeys. In the semi-arid regions where the donkey evolved and is most commonly found today, food resources are often limited and of poor quality. Animals must be efficient consumers and processors of these limited resources in order to survive and compete with other species. Donkeys appear able to maintain body condition better than cattle during the dry season, when food is in particularly short supply Žpers. obs... This ability to conserve body reserves may be due to decreased metabolic requirements, increased selectivity for highly nutritious plant parts, tolerance of undesirable foods, or increased consumption and passage of fibrous foods. Probably some combination of strategies is employed. Several authors ŽJanis, 1976; Duncan et al., 1990. have proposed that the equids use a strategy of high intake, rapid transit and low nutrient extraction per unit of feed to compete with ruminants in high fiber environments. In the ruminant, feed particles must be reduced to a size small enough to pass out of the rumen, whereas equids are not similarly constrained. In order to achieve a high rate of intake, one feeding strategy might involve rapid chewing. We hypothesized that the donkey, a small equid, might chew faster and therefore consume feed faster than a ruminant. In this study, we investigated the rate at which donkeys chew forages, and the rate at which feed is ingested, to determine baseline data for this species. Forages are the above-ground portion of herbaceous plants ŽNational Research Council, 1989., characterized as coarse, bulky and containing more than 22% acid detergent fiber. We fed only forages, not grains, since grass, hay, browse and crop residues are the usual feeds of both feral and domestic donkeys in the arid tropical locations where the species evolved and thrives. Recent reports have suggested that, although body size and dietary fiber intake have the greatest effect on chewing activity, fiber source or type ŽWoodford and Murphy, 1988; Campbell et al., 1992. and amount of dietary protein ŽWarly et al., 1994. can also affect chewing. Although determination of the chewing response to different levels of dietary fiber is of interest, we held fiber
P.J. Mueller et al.r Applied Animal BehaÕiour Science 60 (1998) 241–251
243
constant in order to investigate the effects of fiber source and protein content by feeding two forages containing different amounts of protein but equal levels of neutral detergent fiber ŽNDF. from different plant sources.
2. Materials and methods 2.1. Animals and diets Five domestic donkeys Žthree male, two female, mean body weight 198 " 15 kg. were housed in individual box stalls with daily turn-out in a dry lot. Animals were fed one of two forages Žmixed hay or grass hay: see Table 1. ad libitum twice daily except when feed was removed for 8 h preceding a chewing observation. Salt and water were provided free choice; no food other than the assigned forage was allowed. All animals received both diets in a two-period cross-over design. Following seven days of adaptation to the diet, daily food intake was recorded for 21 days, after which chewing observations were made. Forages fed were Ž1. a mixed legumerorchard grass hay and Ž2. a grass hay. Both forages were highly fibrous, as measured by neutral detergent fiber ŽNDF. content. The nutrient composition is shown in Table 1. The two forages were very similar in all nutritive components compared except crude protein ŽCP., which was more than twice as high in the hay containing legume Ž13.7 vs. 6.5%.. Selected bales were identified for each animal so that an animal always ate from the same bale when being observed. Hay samples were analyzed from each bale used during observational studies so that NDF intake could be accurately assessed; average values appear in Table 1. Fiber varied up to 2% among bales. Pooled samples of all hay fed over the adaptation and intake phase were found to be identical in nutrient composition to the individual bales fed during chewing observations. 2.2. Chewing obserÕations Chewing data were collected by visual observation of donkeys eating. Two animals required adaptation to the presence of the observer Žaccomplished through three half-hour
Table 1 Fiber and protein concentrations of forages
Dry matter Ž%. Crude protein Ž% of DM. Neutral detergent Fiber Ž% of DM. Acid detergent fiber Ž% of DM. Ash Ž% of DM. H 2 SO4 lignin Ž% of DM.
Mixed hay
Grass hay
91.5 13.7 64.6 44.9 5.3 8.1
91.8 6.5 65.8 43.8 4.2 7.3
244
P.J. Mueller et al.r Applied Animal BehaÕiour Science 60 (1998) 241–251
Table 2 Chewing activity of donkeys fed forages Ž ns 5., presented as means"S.E. Mixed hay
Grass hay
120"10 183"17
121"18 185"26
Chewing rate (no.r min) Early-meal Late-meal Average
54"4 59"2 a 53"4
52"4 48"1b 54"1
Chewsr g of DM of NDF
6.2"0.3 9.5"0.5
6.5"0.8 9.9"1.2
Time to eat (min. per kg DM per kg NDF
a,b
Means in the same row with unlike letters differ significantly Ž P - 0.05..
sessions. before they would eat under scrutiny. The other three animals ate readily at all times. Since one person could not make all observations required for the experiment, to minimize intra-animal variation one individual was assigned to each donkey; inter-observer variation, however, was not assessed. Observations were made at the same time of day for each animal. The observer sat in plain view and watched the animal, which stood untethered in its customary box stall. To ensure that donkeys would eat, food was removed for 8 h preceding an observation period. Two types of observations were conducted: Ž1. measurement of time to consume feed, and Ž2. determination of chewing rate. For the former, animals were offered a weighed amount of hay and monitored for one hour to determine both the amount of food eaten in 1 h and the minutes spent chewing Žby recording activity each minute.. Chewing rate Žchewsrmin. was determined both at the start Žtermed ‘early-meal’. and at the finish Žtermed ‘late-meal’. of the 1-h eating bout, as follows: animals were offered a known amount of forage and observed. The observer counted chews during a 2- to 5-min bout of continuous chewing. Counting of jaw movement stopped when chewing ceased for more than 5 s, or after 5 min of continuous chewing, whichever came first. Three such bouts were observed and averaged to give early-meal chewing rate on a given day. This was followed by 1 h of
Table 3 Intake of forages by donkeys Ž ns 5., presented as means"S.E.
Dry matter ŽDM. Žkgrday. NDF Žkgrday. Water Žlrday. DM Žkgr100 kg of BW. NDF Žkgr100 kg of BW. BW Žkg.
Mixed hay
Grass hay
3.9"0.5 2.4"0.7 8.7"1.6 1.9"0.4 1.2"0.2 200"15
3.5"0.4 2.2"0.6 8.7"1.4 1.8"0.3 1.1"0.2 197"15
P.J. Mueller et al.r Applied Animal BehaÕiour Science 60 (1998) 241–251
245
food consumption with observation, as described above. The 1-h eating period was termed a meal. Therefore, after 1 h of eating, the chewing rate observations were repeated to determine late-meal chewing rate. Each complete set of observations was repeated three times per animal, on separate days, after which diets were reversed and the experiment repeated. 2.3. Laboratory and statistical analyses Forage samples were ground to pass through a 1-mm screen, dried at 608C and analyzed for nutritional constituents according to Van Soest et al. Ž1991.. Reported values are means " S.E. Diet effects were compared using paired t-tests.
3. Results Chewing activity for donkeys eating the two forages is shown in Table 2. There were no significant Ž P ) 0.05. differences due to forage type in any of the studied variables, with one exception. Only in the animals eating grass hay did chewing rate slow Ž P - 0.05. after one hour’s access to feed. Because of the lack of significant differences between forage types, data were pooled across the two diets. Donkeys consumed an average of 9.0 " 0.7 g of dry matter ŽDM. per minute, chewing 53 " 2 timesrmin. They required 120 " 12 min to eat one kg of DM, and 184 " 18 min to eat 1 kg of NDF. During the 3-week measurement period, there was no significant difference in intake between the two forages ŽTable 3.. Animals were able to maintain their body weight on either forage fed alone, despite the low CP content of the grass hay.
4. Discussion 4.1. Allometry of chewing efficiency Chewing efficiency is a measure of the amount of chewing time required for the physical processing of a unit of food. For clarity, in ruminants, initial chewing upon ingestion will be referred to as eating or mastication, while the term chewing itself is used to describe the combined total of eating plus rumination chews. Total chewing time is the most relevant measure to use when comparing the ruminant to the non-ruminant, for whom chewing consists only of eating. In this study, prehension was not distinguished from mastication, as the donkeys tended to continue chewing previously prehended feed when taking new bites. Chewing efficiency is positively correlated with body size in ruminants, both within ŽBae and Gilman, 1983. and across species ŽWelch, 1982.. Larger animals need less time and fewer chews per unit of feed than do small animals. In a comparative study ŽWelch, 1982., mature cows Ž560 kg. ruminated 1 kg of NDF for 100 min, while sheep Ž82 kg. ruminated 1180 min and goats Ž39 kg. ruminated 1300 min. Such differences in chewing efficiency may be related to mouth size and hence bite size, tooth area and jaw strength.
246
P.J. Mueller et al.r Applied Animal BehaÕiour Science 60 (1998) 241–251
Minutes of total chewing per kg DM ingested has been used as a measure of chewing efficiency but is highly variable. The literature contains values for cattle ranging from 25–35 min ŽJaster and Murphy, 1983; Woodford and Murphy, 1988; Beauchemin, 1991a; Colenbrander et al., 1991; Beauchemin et al., 1994b; Constable et al., 1994; Dado and Allen, 1994. to as high as 130 min per kg DM ŽBeauchemin and Iwassa, 1993., while sheep vary from 400 ŽCammell and Osbourn, 1972; Weston, 1988. to over 1000 min per kg DM ŽFujihara, 1980; Inoue´ et al., 1994; Warly et al., 1994.. Horses apparently can eat 1 kg of grain in 6 to 13 min ŽHintz et al., 1989; Scott and Potter, 1989. and 1 kg of hay in 25–50 min ŽGallagher and Hintz, 1988; Constable et al., 1994.. Donkeys in the present study spent 120 min chewing 1 kg of forage DM; therefore, their behaviour most closely resembled published data for cattle rather than that for horses or sheep. A better criterion for comparison of chewing efficiency is chewing time per unit of NDF, since fiber content is a principal determinant of requisite chewing time. When fed mixtures of concentrate and forage, dairy cattle required 30–60 min to eat a kg of NDF and an additional 50–100 min of rumination to complete the physical processing of the feed ŽWoodford and Murphy, 1988; Beauchemin and Buchanan-Smith, 1989; Beauchemin, 1991b; Colenbrander et al., 1991; Beauchemin et al., 1994a; Dado and Allen, 1994.. Limited studies in which cattle were fed forage-only diets show different results: 100 min for mastication of 1 kg of NDF plus 100–150 of rumination, for a total chewing time per kg NDF of 200–250 min ŽWelch, 1982; Luginbuhl et al., 1989a; Beauchemin and Iwassa, 1993.. Small ruminants such as sheep and goats are much less efficient fiber processors, requiring from 700 to over 1000 min to chew 1 kg of NDF when fed forage-only diets ŽCammell and Osbourn, 1972; Chai et al., 1985; Warly et al., 1994.. The donkeys in the present study accomplished the physical processing of forage NDF at a rate of 184 min per kg fiber. This is only slightly slower than has been reported in cows. If data are adjusted for body weight or metabolic body size, the donkey would appear capable of consuming forage NDF two to three times faster than previously reported in cattle, although the type of fiber fed and animal satiety state could also have contributed to these apparent interspecific differences. Bae and Gilman Ž1983. developed a regression equation, using cattle from 260 to 860 kg BW, to describe chewing efficiency based on body size. Their equation would predict that the donkey should require 261 min to chew 1 kg of fiber; in fact the donkeys in this study required only 184 min. Bae and Gilman used a medium quality Ž65% NDF. long-stem grass hay, a diet very similar to that fed to the donkeys in the present study. This suggests that the donkey can chew long fiber as efficiently or more efficiently than a much larger ruminant, although differences in experimental design between Bae and Gilman and the present study preclude definitive comparison. Is the allometry of chewing conserved, although at a different calibration, within the equids: do horses chew more efficiently than donkeys? Preliminary data from Constable et al. Ž1994., wherein three horses required only 60 to 80 min of chewing per kg of NDF when fed various types of hay, with the smallest horse chewing longest, would suggest that the allometry holds. Similarly, Hintz et al. Ž1989. found that horses consumed grain nearly twice as fast as ponies that were much smaller.
P.J. Mueller et al.r Applied Animal BehaÕiour Science 60 (1998) 241–251
247
Why, and how, does the donkey consume fiber rapidly? Fast eaters must either chew fast, swallow large particles or be highly efficient at reducing particle size on each chew. Speed of chewing does not seem to differ among similar-sized species Žsee below.. If the donkey can consume forage faster than the ruminant, even ruminants of much larger size, then the donkey must either chew the food less Žresulting in larger digesta particles., or must achieve greater mastication efficiency in fewer chews. Possibly some combination of these strategies is used. The hindgut presents less impediment to digesta passage than does the rumen; hence, there is less necessity for the donkey to reduce feed particle size. However, the ingestion of larger particles may compromise digestion, including the digestion and absorption of soluble carbohydrates and protein in the small intestine where residence time may be short if intake is high. Although there is no information on fecal particle size in donkeys, fiber particles found in the feces of ponies are twice as large as those from cattle ŽVan Soest, 1994.. Rapid consumption of fiber implies that the donkey’s feeding behaviour also includes large intakes and minimal particle size reduction through mastication. Cattle have been observed to chew 14–20 times for each gram of hay NDF ingested ŽLuginbuhl et al., 1989a; Beauchemin and Iwassa, 1993; Beauchemin et al., 1994a,b., while sheep chew 70–100 times per gram of NDF ŽChai et al., 1985.. Horses fed hay chewed 4–6 times per gram of hay NDF ŽConstable et al., 1994.. The donkeys, however, chewed 9 times per gram of hay NDF. This indicates one way that the donkey, despite its smaller mouth, might process food at approximately the same rate as larger cattle: fewer chews per gram of food. A stronger jaw and larger molar surface may help the donkey chew each mouthful more effectively. Equids in general have a larger tooth surface area than similarly-sized ruminants, because all premolars are molariform ŽJanis, 1979., and there is greater masticatory musculature ŽTurnbull, 1970.. Whether the donkey has absolutely more tooth surface than the cow is unknown. 4.2. Speed of chewing Although it may vary with type of feed, the chewing rate of similarly-sized adult herbivores eating dried forage is relatively constant. Literature values for chewing speed of ponies, horses, dairy cattle and immature steers fed hay all lie between 49 and 72 chewsrmin ŽTable 4.. Sheep and goats may chew faster because the smaller size of their eating apparatus both allows and requires speed. Bae and Gilman Ž1983., however, found no difference in chewing speed across a 4-fold difference in body size in cattle. Donkeys in the present study chewed on average 54 times per min, similar to many published values for other species ŽTable 4.. The chewing rate observed varied from a low of 43 to as high as 62 chewsrmin, with a tendency for the smaller donkeys to chew more slowly than the larger. Donkeys appeared to process feed more slowly than has been reported for horses ŽGallagher and Hintz, 1988; Constable et al., 1994., which could be the result of a slightly slower chewing rate, or could reflect differences in particle size diminution. The latter could be a factor contributing to observed differences in fiber digestibility between horses and donkeys ŽPearson and Merritt, 1991.. However, the data for both horses and donkeys are from very small samples and have not been obtained within the same study, and thus one can only speculate until further information is obtained.
248
P.J. Mueller et al.r Applied Animal BehaÕiour Science 60 (1998) 241–251
Table 4 Rate of chewing a in selected ungulates Species
Feed
Chew Rate Žchewsrmin.
Reference
Donkey Pony Horse Horse Horse Dairy cow Dairy cow Dairy cow Dairy cow Steer Steer Sheep Sheep Sheep Goat
Hay Hay Hay Grain Fresh grass Hay Hay Hay Total mixed ration Hay Hay Rice Straw Hay Fresh grass Hay
54 49 72 55 35–50 77 40–53 74 62 71 59–65 70 71 120–150 87
This study Sarna, pers. comm. Constable et al., 1994 Scott and Potter, 1989 Mayes and Duncan, 1994 Constable et al., 1994 Brouk and Belyea, 1993 Gill et al., 1966 Dado and Allen, 1994 Luginbuhl et al., 1989b Luginbuhl et al., 1989a Warly et al., 1994 Fujihara, 1980 Inoue´ et al., 1994 Hooper and Welch, 1982
a
In ruminants, average of mastication and rumination rates, where these differ.
Cattle are sometimes seen to chew faster at the start of a meal than towards the end ŽLuginbuhl et al., 1989a., perhaps to produce large quantities of saliva for rumen buffering, or because they are hungrier. Later in the meal the buffering requirement is met and chewing speed decreases. For the mixed legumergrass hay, donkeys ate at the same speed both when first offered feed following 8 h without food, and after 1 h of eating. When fed grass hay, however, donkeys significantly slowed their chewing rate after 1 h. Although this behaviour resembled that reported for cattle, it cannot be for the same reason, as the donkey has no need to buffer a rumen. It is likely that the mixed forage, containing legume, was more palatable than the grass hay, hence the donkeys remained eager to continue eating even after 1 h of access to food. The grass hay, on the other hand, was dusty and less acceptable. After 1 h of eating, perhaps the donkeys’ motivation for eating diminished and their chewing rate slowed. 4.3. Effect of fiber source on chewing behaÕiour In ruminants, rumination time depends not only on the amount of fiber consumed, but also on fiber characteristics such as length, shape, fragility and specific gravity ŽChai et al., 1985.. Grass hay, the fiber of which breaks into long thin pieces, may elicit a different amount of chewing than alfalfa, which fractures into short round pieces ŽVan Soest, 1994.. In donkeys, however, there was no difference in chewing activity between grass fiber and mixed legumergrass fiber. Possibly the mixed hay did not contain enough legume to be appreciably different in fiber characteristics, or else this effect of fiber type appears only during rumination and hence is not seen in the donkey. 4.4. Effect of dietary protein concentration on chewing behaÕiour Protein-deficient diets may increase total chewing time in the ruminant because microbial digestion is depressed and, in order to maintain sufficient particle breakdown,
P.J. Mueller et al.r Applied Animal BehaÕiour Science 60 (1998) 241–251
249
the animal compensates by increasing rumination ŽWarly et al., 1994.. In a hind-gut fermenter such as the donkey, however, suppression of microbial digestion in the colon and cecum by insufficient dietary protein is unlikely to directly amplify the chewing response in compensation. Therefore, it is not surprising that protein concentration had no effect on chewing efficiency in this study. It may also be true that, although the grass hay had only 50% as much crude protein as the mixed forage, it still provided sufficient dietary protein for the donkey. Although the National Research Council Ž1989. recommends 8.0% protein for the maintenance of horses, no data are available for donkeys and the dietary concentration of 6.5% CP fed in this study was likely sufficient for them, especially at ad libitum intake. This hypothesis is supported by the observation that donkeys were able to maintain body weight for 3 weeks while eating the grass hay.
5. Conclusion Feeding behaviour of equids is thought to be characterized by large intakes with low nutrient extraction. High rates of intake can be achieved via rapid chewing, large bites, effective chewing per bite, or sacrifice in particle size reduction. Neither bite size nor particle size was measured in this study, and chewing rate of the donkey appeared similar to previously published rates for cattle. However, when scaled to either body size or to metabolic body size, donkeys may be able to consume NDF faster than cattle. Whether they do this solely through passage of large particles or through more efficient chewing, related to tooth and jaw structure, is unknown, but merits further study. The donkey differs somewhat from the horse because its narrow muzzle and mobile lips promote greater selectivity in feeding. This allows it to maximize feed quality rather than quantity, yet a relatively rapid intake ability was seen in this study. The donkey may use a selective feeding strategy, searching for high quality bites when foraging over a heterogeneous pasture or rangeland, but when provided with homogenous hay employs an alternative strategy of maximizing intake. In practice, donkeys faced with some perceived need to consume more food quickly, such as following an intentional or unintentional fast, or restricted time in which to eat due to insufficient feeder space, competition from herd mates or long hours spent working, may resort not to faster chewing but to incomplete chewing. This could result in problems such as esophageal obstruction Žchoke. and intestinal impaction. A donkey who ate rapidly following a period of food restriction did suffer from esophageal obstruction Žpers. obs... In contrast to results sometimes seen in cattle, fiber source and protein concentration, to the extent studied in this experiment, had no effect on rate of forage consumption in the donkey. Clearly, much more needs to be known about the donkey’s chewing activity when ingesting feeds of different fiber content, and about modulation of chewing activity in a natural foraging situation when food must be sought and selected rather than simply ingested. Further studies of the donkey, horse and other equids, especially in simultaneous, comparative studies, are of interest to determine whether the chewing behaviour of the donkey represents a unique solution to a feeding constraint, or is characteristic of a typical equid strategy in contrast to that of ruminants.
250
P.J. Mueller et al.r Applied Animal BehaÕiour Science 60 (1998) 241–251
Acknowledgements The authors are grateful to Kim Brockmann and Andrew Skol for patiently assisting with data collection, and to Dr. J.B. Robertson for assistance with laboratory analysis. This material is based upon work supported under a National Science Foundation Graduate Fellowship held by P.J. Mueller.
References Bae, D.H., Gilman, B.E., 1983. Mastication and rumination in relation to body size of cattle. J. Dairy Sci. 66, 2137–2141. Beauchemin, K.A., 1991a. Ingestion and mastication of feed by dairy cattle. Vet. Clin. North Am. Food Anim. Pract. 7, 439–463. Beauchemin, K.A., 1991b. Effects of dietary neutral detergent fiber concentration and alfalfa hay quality on chewing, rumen function, and milk production of dairy cows. J. Dairy Sci. 74, 3140–3151. Beauchemin, K.A., Iwassa, A.D., 1993. Eating and ruminating activities of cattle fed alfalfa or orchard grass harvested at two stages of maturity. Can. J. Anim. Sci. 73, 79–88. Beauchemin, K.A., Buchanan-Smith, J.G., 1989. Effects of dietary neutral detergent fiber concentration and supplementary long hay on chewing activities and milk production of dairy cows. J. Dairy Sci. 72, 2288–2300. Beauchemin, K.A., Farr, B.I., Rode, L.M., Schaalje, G.B., 1994a. Optimal neutral detergent fiber concentration of barley-based diets for lactating dairy cows. J. Dairy Sci. 77, 1013–1029. Beauchemin, K.A., McAllister, T.A., Dong, Y., Farr, B.I., Cheng, K.-J., 1994b. Effects of mastication on digestion of whole cereal grains by cattle. J. Anim. Sci. 72, 236–246. Brouk, M., Belyea, R., 1993. Chewing activity and digestive responses of cows fed alfalfa forages. J. Dairy Sci. 76, 175–182. Cammell, S.B., Osbourn, D.F., 1972. Factors influencing the total time spent chewing by sheep given diets containing long, dried forages. Proc. Nutr. Soc. 31, 63A–64A. Campbell, C.P., Marshall, S.A., Mandell, I.B., Wilton, J.W., 1992. Effects of source of dietary neutral detergent fiber on chewing behavior in beef cattle fed pelleted concentrates with or without supplemental roughage. J. Anim. Sci. 70, 894–903. Chai, K., Kennedy, P.M., Milligan, L.P., Mathison, G.W., 1985. Effects of cold exposure and plant species on forage intake, chewing behavior and digesta particle size in sheep. Can. J. Anim. Sci. 65, 69–76. Colenbrander, V.F., Noller, C.H., Grant, R.J., 1991. Effect of fiber content and particle size of alfalfa silage on performance and chewing behavior. J. Dairy Sci. 74, 2681–2690. Constable, E.C., Houpt, K.A., Janis, C.M., 1994. Effect of fiber content of feed on chewing rate. 65th Annual Meeting, Eastern Psychological Association, Providence, RI, Abstract. Dado, R.G., Allen, M.S., 1994. Variation in relationships among feeding, chewing, and drinking variables for lactating dairy cows. J. Dairy Sci. 77, 132–144. Duncan, P., Foose, T.J., Gordon, I.J., Gakahu, C.G., Lloyd, M., 1990. Comparative nutrient extraction from forages by grazing bovids and equids: a test of the nutritional model of equidrbovid competition and coexistence. Oecologia 84, 411–418. Fujihara, T., 1980. The eating and rumination behavior in sheep fed only grass diets in either fresh or dried form. J. Agric. Sci. ŽCamb.. 95, 729–732. Gallagher, J.R., Hintz, H.F., 1988. Rate of feed intake and horse health. Proc. Aust. Soc. Anim. Prod. 17, 399. Gill, J., Campling, R.C., Westgarth, D.R., 1966. A study of chewing during eating in the cow. Br. J. Nutr. 20, 13–23. Hintz, H.F., Schryver, H.F., Mallette, J., Houpt, K., 1989. Factors affecting rate of grain intake by horses. Equine Prac. 11, 35–42. Hooper, A.P., Welch, J.G., 1982. Chewing efficiency and body size of kid goats. J. Dairy Sci. 66, 2552–2556.
P.J. Mueller et al.r Applied Animal BehaÕiour Science 60 (1998) 241–251
251
Inoue, ´ T., Brookes, I.M., John, A., Hunt, W.F., Barry, T.N., 1994. Effects of leaf shear breaking load on the feeding value of perennial ryegrass Ž Lolium perenne) for sheep: II. Intake, particle breakdown, rumen digesta outflow and animal performance. J. Agric. Sci. ŽCamb.. 123, 137–147. Janis, C.M., 1976. The evolutionary strategy of the Equidae and the origins of rumen and cecal morphology. Evol. 30, 757–774. Janis, C.M., 1979. Aspects of the evolution of herbivory in ungulate mammals. PhD Thesis, Harvard Univ., Cambridge, MA. Jaster, E.H., Murphy, M.R., 1983. Effects of varying particle size of forage on digestion and chewing behavior of dairy heifers. J. Dairy Sci. 66, 802. Luginbuhl, J.-M., Pond, K.R., Burns, J.C., Russ, J.C., 1989a. Eating and ruminating behavior of steers fed coastal bermuda grass at four levels. J. Anim. Sci. 67, 3410–3418. Luginbuhl, J.-M., Pond, K.R., Burns, J.C., Russ, J.C., 1989b. Effects of ingestive mastication on particle dimensions and weight distribution of coastal bermuda grass hay fed to steers at four levels. J. Anim. Sci. 67, 538–546. Mayes, E., Duncan, P., 1994. Temporal patterns of feeding behaviour in free-ranging horses. Behav. 96, 105–129. National Research Council, 1989. Nutrient Requirements of Horses. National Academy Press, Washington, DC. Pearson, R.A., Merritt, J.B., 1991. Intake, digestion and gastrointestinal transit time in resting donkeys and ponies and exercised donkeys given ad libitum hay and straw diets. Equine Vet. J. 23, 339–343. Scott, B.D., Potter, G.D., 1989. Rate of feed consumption and chewing by mature horses fed diets with varying amounts of fiber. Proceedings of the 11th Equine Nutrition and Physiology Society, Oklahoma State University, Stillwater, OK, pp. 234–237. Turnbull, W.D., 1970. Mammalian masticatory apparatus. Fieldiana Geol. 18, 149–156. Van Soest, P.J., 1994. Nutritional Ecology of the Ruminant, 2nd edn. Cornell Univ. Press, Ithaca, NY. Van Soest, P.J., Robertson, J.B., Lewis, B.A., 1991. Methods for dietary fiber, neutral detergent fiber and nonstarch polysaccharides in relation to animal nutrition. J. Dairy Sci. 74, 3583–3597. Warly, L., Fariani, A., Mawuengegah, O.P., Matsui, T., Fujihara, T., Harumoto, T., 1994. Studies on the utilization of rice straw by sheep: IV. Effect of soybean meal and barley supplementation on eating and rumination behavior. Asian Australas. J. Anim. Sci. 7, 272–277. Welch, J.G., 1982. Rumination, particle size and passage from the rumen. J. Anim. Sci. 54, 885–894. Weston, R.H., 1988. Factors limiting the intake of feed by sheep: XII. Digesta load and chewing activities in relation to lactation and its attendant increase in voluntary roughage consumption. Aust. J. Agric. Res. 39, 671–677. Woodford, S.T., Murphy, M.R., 1988. Effect of forage physical form on chewing activity, dry matter intake and rumination of dairy cows in early lactation. J. Dairy Sci. 71, 674–686.