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POULTRY WELFARE SYMPOSIUM |
Department of Animal and Avian Sciences, University of Maryland, College Park 20742
1 Corresponding author: iestevez{at}umd.edu
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ABSTRACT |
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 TOP ABSTRACT DENSITY ALLOWANCES AND BROILER...EFFECTS OF DENSITY IN...WHERE TO SET THE...REFERENCES |
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Key Words: broiler • density • welfare • environment
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DENSITY ALLOWANCES AND BROILER WELFARE |
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TOPABSTRACTDENSITY ALLOWANCES AND BROILER...EFFECTS OF DENSITY IN...WHERE TO SET THE...REFERENCES |
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If guidelines have to be established, any recommendation should be based on sound science. However, setting limits to density based on scientific evidence may not be as easy as it may initially appear because 1) The decline in animal health and welfare is progressive, and therefore it is difficult to set a number limit on what can be considered acceptable and beyond what point further increments in density should not be allowed. 2) Limits may vary depending on the parameters used to define health and welfare. 3) Housing conditions and management practices have a tremendous impact on animal welfare; animals raised at identical densities may have very different health and welfare status. 4) Requirements may be different for different genetic lines. 5) There may not be sufficient scientific studies to determine where the limit should be, or because these studies are mostly conducted in experimental settings, results may differ substantially from the results that would be obtained under commercial conditions.
Because it is difficult to determine a clear cutoff point for maximum density allowances, current established guidelines include recommendations that vary markedly. Although this lack of consistency may trigger discussion, it may also confuse consumers. For example, the welfare guidelines of the National Chicken Council (NCC, 2005) recommend a range of densities from 6.5 lb/ft2 (0.07 m2/ bird) for light broilers (below 4.5 lb of final BW) to 8.5 lb/ft2 for roasters, compared with the current average industry density of 7.4 lb/ft2 during the winter and 6.1 lb/ft2 during the summer. The Food Market Institute and National Council of Chain Restaurants (FMI-NCCR, 2003) have established the limit at 6 lb/ft2 (0.073 m2/bird) similar to the recommendations of the Royal Society for the Prevention of Cruelty to Animals (RSPCA, 2002) of 30 kg/m2 (6.14 lb/ft2; 0.073 m2/bird). Based on the findings reported from the Scientific Committee on Animal Health and Welfare (2000), upcoming legislation within the European Union will limit maximum densities for broilers at 30 kg/m2 (0.073 m2/bird). In the meantime, industry densities in Europe are found to range markedly from 45 to 54 kg/m2 (approximately 9.2 to 11.6 lb/ft2) for Denmark and the Netherlands, 40 kg/m2 in the United Kingdom, to as low as 30 to 36 kg/m2 for Switzerland and Sweden (reported in Sørensen et al., 2000; Sanotra et al., 2001a). Obviously there is a wide gap between recommended guidelines for broilers. The question is: can any of these recommendations be supported by the scientific data available?
One challenge to this review paper is that densities in the scientific literature are reported in ft2, cm2, dm2, or m2/bird, number of birds per m2, and more recently as kg/m2. For comparative purposes, all the densities have been transformed to m2/bird. The equivalences in number of birds or kg/m2 are often included.
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EFFECTS OF DENSITY IN BROILERS |
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TOPABSTRACTDENSITY ALLOWANCES AND BROILER...EFFECTS OF DENSITY IN...WHERE TO SET THE...REFERENCES |
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A relatively large number of scientific work has focused on the effects of stocking density in broilers, in part motivated by its large economic impact on profitability and returns. Because the very early investigations, results have consistently indicated a decline in final BW and performance associated with high densities (Tomhave and Seeger, 1945; Heishman et al., 1952). Initially it was argued that this decline could be related to insufficient feeder space, but Hansen and Becker (1960) demonstrated that even by maintaining constant feeding space per bird the negative effects of density on final BW prevailed (density range 0.046, 0.069, 0.092, 0.116 m2/bird). However, the results of these experiments do not have practical value to help establish guidelines for current conditions because the chickens as well as the housing and management practices have dramatically changed. However, they do show that the negative effects of density have been a concern for producers even when chickens grew at a much slower pace requiring close to 12 wk of rearing.
Similarly, the more recent literature consistently reported negative effects of density primarily in BW, carcass damage, and mortality. Results varied substantially regarding the density threshold at which the decline in bird performance was most affected. For broilers raised to 8 wk and densities ranging from 0.047 to 0.093 m2/bird, Bolton et al. (1972) did not find differences in final BW, although effects of density were significant by 10 wk of age. Conversely, Proudfoot et al. (1979) showed that higher densities (range 0.037, 0.055, 0.074, 0.0927 m2/bird) resulted in lower final BW, increased carcass damage, poorer feathering condition, and a linear increase in the percentage of downgrades related to breast blisters. Effects were particularly prevalent when space allowances dropped below 0.055 m2/bird, but Deaton et al. (1968), Estevez et al. (1997), and Sørensen et al. (2000) found that decline in BW was evident when space per bird dropped below 0.066 or 0.0625 m2. This would correspond to approximately 15 to 16 birds/m2. These patterns were comparable to the results obtained by Cravener et al. (1992) at a similar range of densities (0.05, 0.07, 0.09, and 0.11 m2/bird) and suggested that space allowances below 0.07 m2/bird (14 birds/m2) compromised broiler welfare as indicated by growth and observed carcass damage. Other studies found differences in mild (43 vs. 71%) and severe scratches (12 vs. 30%) when densities were experimentally increased from 0.14 to 0.07 m2/bird (Elfadil et al., 1996), and increments from 0.066 to 0.045 m2 also resulted in higher incidence of scabby hips (Frankenhuis et al., 1991). The most recent studies conducted by Dozier indicated that a density beyond 30 kg/m2 consistently produced a decline in BW, explained by a reduction in feed consumption, and increased the incidence of food-pad lesions and skin scratches (Dozier et al., 2005b). Mortality was also higher for densities above 30 kg/m2 (3.6 vs. 7.5%) but was not significantly different. In this study, space availability was much larger than for other studies with targeted densities of 30 kg/m2 and corresponded to 0.106 m2/ bird. This is related to the fact that birds were grown to 49 d of age and equivalent densities were calculated on 3.2 kg of final BW, much higher that in other studies; therefore, results of this study are hard to compare with others. For lower targeted BW, Dozier et al. (2006) found a 6% decline in BW for densities above 35 kg/m2 (0.052 m2/bird).
Contrarily, Shanawany (1988) indicated that although final BW declined with density (ranging from 0.10 to 0.02 m2/bird), the effects were more prevalent when space allowances were at or below 0.035 m2/bird (30 birds/ m2), which is substantially higher that the critical densities reported in all other studies. Nevertheless, in the Shanawany (1988) study a decline in average feed intake with density was clear, dropping from approximately 110 g/ bird per day for broilers maintained at 0.1 and 0.05 m2/ bird (10 and 20 birds/m2, respectively), to less than 100 and 70 g for densities of 0.035 and 0.2 m2/bird (50 birds/ m2) respectively. A small but significant effect of density on BW was reported by Martrenchar et al. (2000) comparing densities of 0.09 with 0.045 m2/bird, but failed to find differences in terms of feed efficiency or carcass damage. Pettit-Riley and Estevez (2001) found no effects on final BW or feed conversion for densities between 0.1 and 0.05 m2/bird (10 to 20 birds/m2), but mortality due to heat stress was significantly higher at densities above 0.066 m2 (15 birds/m2).
Although economic return per bird decreased at higher densities, total kilogram produced per unit of space increased (Proudfoot et al., 1979; Shanawany, 1988; Cravener et al., 1992), resulting in higher profits. Puron et al. (1995) in a study on broilers showed that kilograms produced per meters squared increased with increasing stocking density. However, the relationship between density and economic returns is not a linear one. The authors showed that this relationship was only valid up to a certain point because bird performance declined if densities were excessive, resulting in similar kilograms of meat produced at higher and lower densities if densities surpassed 17 birds/m2 for males and 19 for females. These results suggest that farm profitability and animal welfare will be hurt by going above such a density limit.
2. Physiological Stress
Some of the studies related to density looked not only to performance parameters but also to indicators of physiological stress. None of the results by Bolton et al. (1972) that looked to the effects of density on the weight of the adrenals, or Cravener et al. (1992) that measured that variation of heterocite:lymphocyte, found evidence of physiological stress as related to increases in density. Similar to the results of Dozier et al. (2006) for birds grown to lower final BW, Thaxton et al. (2006) failed to detect any effects of density on corticosterone, glucose, and cholesterol levels in broilers reared between 0.14 and 0.052 m2 space allowance per bird (20 and 55 kg/m2). Dawkins et al. (2004) and Jones et al. (2005) found differences in corticosterone levels in broilers; however, the differences were related to variations in environmental parameters and not to density per se. On the other hand, Heckert et al. (2002) reported a significant reduction in bursa weights and bursa/BW ratios with increasing densities (ranging from 0.10, to 0.05 m2 per bird), suggesting a higher degree of stress particularly for birds at densities above 0.066 m2/ bird (15 birds/m2). Other parameters such as humoral immune response to SRBC, heterocite:lymphocyte ratios, or lymphocyte blastogenesis were not different across densities (Heckert et al., 2002).
3. Leg Health and Walking Ability
As social pressure to insure animal welfare has become more important, recent studies have focused on the implications of increasing density in terms of broiler welfare rather than on the economic impact for production. Leg health and walking ability are good estimators of overall welfare levels in poultry (Wang et al., 1998; Sanotra et al., 2001a, 2002). Gait scores (GS), a parameter used to evaluate walking ability (Kestin et al., 1992; Garner et al., 2002), became increasingly poor in response to increased density. In particular, the proportion of birds with scores 4 and 5 (which indicate severely compromised walking ability) were significantly higher when space allowance was equal to or lower than 0.0625 m2/bird (Sørensen et al., 2000) and when comparing a wider set of density ranges (Sanotra et al., 2001b). Also, broilers at higher densities in Sørensen et al. (2000), Arnould and Faure (2003), and Dozier et al. (2005b) had an elevated incidence of foot and hock burns, and both parameters correlated with poor GS (Sørensen et al., 2000). Poorer GS may be related to a reduction in exercise as seen by the decline in distance traveled by broilers at high densities (Lewis and Hurnik, 1990; Andrews et al., 1997; Estevez et al., 1997), or may be a result of the rapid decline in litter quality associated with high densities, which is known to affect leg health (Ekstrand, 1993; Wang et al., 1998), or a combination of both factors. In Dozier et al. (2005b), higher incidence in foot-pad lesions could be explained by the significantly higher levels of litter moisture; however, they did not find differences in GS.
Tibial dischondroplasia (TD) is another leg health parameter that is commonly included in investigations related to the welfare of broilers. Tibial dischondroplasia is a pathology that is relatively frequent in broilers, although its incidence is on the decline because of proactive selection against it because it is a deformity with strong genetic basis (Wong-Valle et al., 1993; Zhang et al., 1995). The incidence of TD does not appear to be affected by density when comparing low and moderately high densities (for densities between 0.1 and 0.045 m2/bird; Sørensen et al., 2000; Tablante et al., 2003). Contrarily, Sanotra et al. (2001b) reported higher TD levels when comparing higher ranges of densities; 27% of the birds showed signs of a severe degree of TD for densities of about 0.033 m2/bird (30 birds/ m2). The results detailed above provide undoubted evidence that high densities can compromise not only broiler performance but also leg health and overall welfare levels.
4. Behavioral Effects
As mentioned above, distance moved and time spent walking in broilers is affected by density (Estevez et al., 1997; Hall, 2001; Febrer et al., 2006), even when the compared densities would be considered low for production (Lewis and Hurnik, 1990; Andrews et al., 1997). Although much speculation has centered around the possibility that reductions in space use are a result of social restrictions of movement, so far the evidence has indicated that this may be a barrier effect as described by Newberry and Hall (1990) and supported by results from Estevez et al. (1997) because the frequency of aggressive interactions remained very low at high densities. Furthermore, Febrer et al. (2006) showed that broiler chickens are socially attracted to one another and even at high commercial densities will seek to maintain close proximity with other birds. However, the frequency of disturbances, defined as interruptions of resting periods caused by disruptions from other birds, increased with density under experimental (densities 0.20 to 0.5 m2/bird, Estevez, 1994; 0.12 to 0.08 m2/bird, Cornetto et al., 2002) and under commercial conditions (0.055 and 0.046 m2/bird, Hall, 2001; 0.073 to 0.047 m2/bird, Febrer et al., 2006). Disturbances are not related to aggression but can cause severe carcass damage as a result of the scratches to the back of the birds being disturbed. This behavior would explain the deterioration in carcass quality associated with increasing densities found in other studies (Proudfoot et al., 1979; Frankenhuis et al., 1991; Cravener et al., 1992; Bilgili and Hess, 1995). Besides these behavioral effects in movement and disturbances, other main behavioral categories such as the frequency of resting, preening, standing, feeding, drinking, and foraging do not appear to be affected at densities ranging between 0.12 to 0.08 m2/bird (Cornetto and Estevez, 2001), from 0.5 to 0.066 m2/bird (Arnould and Faure, 2003), or in commercial houses with densities ranging from about 0.073 to 0.047 m2/bird (Febrer et al., 2006). Similarly, in a comparative study between free range and deep litter broilers, the differences in behavior were minimal (Weeks et al., 1994). Only Hall (2001), working with densities of 0.055 and 0.046 m2/bird, and Sanotra et al. (2002), working with 0.034 as compared with 0.041 m2/ bird, found reduced activity levels in broilers and less ground pecks and litter scratches.
The mechanism of action to explain the reduction in bird performance associated with density remains a critical unanswered question. In the studies that look to the effects of density on feed intake researchers found that birds at higher densities consumed less food (e.g., Shanawany, 1988; Dozier et al., 2005b; Han et al., 2005). Similar to Malone et al. (1980) and Sørensen et al. (2000), Dozier et al. (2006) suggested that the reduction in final BW may be related to reduce feed intake because of limited feeding space and indicated that providing a larger number of feeders may help to reduce the negative consequences of density. Broilers spend a low proportion of their budgeted time feeding (11% according to Cornetto and Estevez, 2001), and no studies have yet found any indication of less feeding behavior at higher densities (Andrews et al., 1997; Han et al., 2005; Febrer et al., 2006) or that maintaining constant feeding space alleviates the negative consequences of density (Hansen and Becker, 1960). These findings suggest that it is unlikely that the effects of density on performance are related to feeding space limitations. Furthermore, providing additional feeders may in fact exacerbate the negative effects of density. This is because feeders would occupy more space, leaving less free room available for the movement of the birds, thereby possibly increasing stress, similar to the findings of Heckert et al. (2002) when perches were added to broilers reared at high densities. Interestingly, in an experiment geared toward determining the effects of air velocities and air temperature, Dozier et al. (2005a) found that similar to the effects of density, birds raised under still air ate less and were consequently lighter than birds subjected to improved environmental conditions. The low aggression observed in broilers at high densities, lack of differences in feeding behavior or time spent at the feeder but lower feed intake, together with the evidence that feed intake is also reduced when environmental conditions deteriorate at constant density, suggest that reduced final BW may result from a reduction in appetite related to the deterioration of environmental conditions that goes along with higher densities. This mechanism of action would also explain the differences in bird performance that are commonly observed across producers that grow birds under similar densities but that may vary in the quality of the environment that they are able to supply. This is, of course, just a hypothesis at this time, but worth testing.
5. Commercial Conditions and the Environment
Part of the variability in response to density across studies could be related to variations across flocks (Sanotra et al., 2001a), the genetic line used, type of experimental facilities, available technology to control the environment (Estevez, 1999), season of the year when experiments were conducted (Dawkins et al., 2004), management, and other factors. Differences in response to the effects of density dependent upon environmental variables had been reported earlier by Deaton et al. (1968) and more recently by Weaver and Meijerhof (1991), Ekstrand (1993), Ekstrand et al. (1997), and Ekstrand and Carpenter (1998). For example, they reported between 35.4 to 75.5% in the incidence of foot-pad dermatitis depending on whether litter quality was dry or wet, and from 36.4 to 80.7% depending on litter depth, with litter below 5 cm being the best (Ekstrand et al., 1997). Given that the environment has such a strong effect on the health and welfare of broilers, we should consider how predictions of the effects of increasing density will hold when applied to commercial settings where good environmental control may be difficult to achieve. Studies on the effects of density under commercial conditions may be much more relevant and valuable to get a more realistic view of what goes on when the study population consists of several thousands rather than several dozens and birds are reared under experimental conditions of good environmental control.
In recent years there has been a number of published research on the effects of density under commercial conditions. For example, Hall (2001) compared the behavior and welfare status of broilers at space allowances of 0.055 and 0.046 m2/bird (34 and 40 kg/m2) under UK commercial conditions. In this study there was significantly higher daily mortality at the largest density toward the end of rearing (but no differences in total mortality), a higher mean daily percentage of culls due to leg problems as well as increased carcass bruising (0.46 vs. 0.99%), breast blisters (0.24 vs., 0.41 %), scratches (0.259 vs. 0.517%), and hock burns (0.997 vs. 2.350%). Also in a large epidemiological study Nijdam et al. (2004) conducted in commercial flocks in the Netherlands and Germany, the authors noted an increment in the percentage of birds dead on arrival associated with density.
On the other hand, in an epidemiological study of over 50 commercial broiler flocks in France Martrenchar et al. (2002) reported a very low incidence of foot-pad dermatitis and no detectable effects of density. However, they indicated that a poor fan ventilation system was a significant risk factor for incidence of foot-pad dermatitis. These results are in line with the findings of 2 more recent studies (Dawkins et al., 2004; Jones et al., 2005) that found surprisingly few effects of density per se on the health and welfare of broiler chickens in commercial flocks in the United Kingdom. Results indicated that for a range of densities from 30 to 46 kg/m2 (0.073 to 0.047 m2/ bird), broiler health and welfare was to a great extent determined by the quality of the environment provided by producers (Dawkins et al., 2004), and particularly relevant to welfare was the proportion of time that relative humidity in the facilities was maintained within the recommended guidelines (Jones et al., 2005). These results are also supported by the findings of Berg (1998) in a study of commercial flocks in Sweden. As indicated by Dawkins et al. (2004), the effects of density in this large study were overshadowed by much larger differences regarding management practices between the different companies. To evaluate health and welfare status, they included parameters such as the incidence of poor GS, leg condition, corticosterone levels, behavior, percentages of downgrades, and mortalities. Only the proportion of broilers with GS of 0 (indicating good leg condition), growth rate, and percentage of litter moisture were affected by density. Nonetheless, the proportion of birds with dirty pads, leg deformation, and corticosterone levels varied according to changes in temperature, ventilation, and humidity. They concluded that control over environment conditions and in particular a good ventilation system and management practices geared toward the maintenance of adequate relative humidity are critical to improve broiler welfare (Jones et al., 2005). Dawkins et al. (2004) also pointed out that limiting stocking densities without adequate control over the environment will not lead to the expected improvements in welfare.
Although all of these studies have an immense value in our attempt to get a clear picture of what goes on in commercial farms, we must keep in mind that these studies were conducted in Europe, particularly in the United Kingdom. Although it is likely that studies in the United States would yield similar results, important variations exist in terms of buildings, dietary ingredients, and management practices. Particularly relevant are the differences in litter management; in Europe litter is fully replaced after each flock. These differences may have an impact on how birds respond to increased density, which is still unknown for North American producers.
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WHERE TO SET THE LIMITS? |
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TOPABSTRACTDENSITY ALLOWANCES AND BROILER...EFFECTS OF DENSITY IN...WHERE TO SET THE...REFERENCES |
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It is difficult to compare the effects of density across all the studies reported in this paper because experiments were conducted in different types of facilities, with diverse genetic lines of broilers grown for varying periods of time and to different final BW. For example, this means that densities of 30 kg/m2 can range from 9.32 birds/m2 (Dozier et al., 2005b) to as high as 16.15 birds/m2 (Dozier et al., 2006). Keeping this in mind, the majority of the data available today with few exceptions (e.g., Bolton et al., 1972; Proudfoot et al., 1979; Shanawany, 1988) suggests that the most severe effects of high density occur when space available per bird drops somewhere below 0.07 or 0.0625 m2/bird, approximately 14 to 16 birds/m2 and between 34 to 40 kg/m2, assuming an average final BW of approximately 2.5 kg (Deaton et al., 1968; Cravener et al., 1992; Elfadil et al., 1996; Estevez et al., 1997; Sørensen et al., 2000; Pettit-Riley and Estevez, 2001; Dawkins et al., 2004). Results by Dozier et al. are slightly different from other studies because final BW were much higher (3.2 kg in Dozier et al., 2005b) or much lower than the others (1.8 kg, Dozier et al., 2006), similar to Hall (2001) in which average final BW was around 1.8 kg. For these 2 latest studies reduced welfare was observed for densities higher than 34 and 35 kg/m2 (Hall, 2001; Dozier et al., 2006). This suggests that recommended densities, as measured by the number of birds/m2, can possibly go higher (to about 18 birds/m2) without major negative impact in comparison with when birds are grown to higher final BW.
A Model to Balance Performance and Broiler Welfare
As discussed in previous sections, the results from Puron et al. (1995) showed that kilograms of meat produced increases following a quadratic pattern until the point that further bird additions do not result in higher yield per unit of space, a consequence of the decline in bird performance, but it does exponentially increase the negative effects on the health and welfare of broilers (Figure 1
). By looking at the data provided by Puron et al. (1995), it is easy to see that the densities in which yield per unit of space plateaus (17 birds/m2 for males and 19 for females) are not far from the densities recommended to minimize the negative welfare impact as discussed above. Therefore, maximum production with the least possible potential for welfare problems should occur at the point in which yield per unit of space start to plateau (represented by I in Figure 1). Comparatively, returns for the poultry industry should not be drastically different because although there could be a lower yield per unit of space, parameters such as carcass quality may actually be improved (as a consequence of reduced scratches, bruising, and dermatitis) and dead-on-arrival birds may possibly be fewer, to a certain extent compensating for the cost of rearing birds at slightly lower densities. At this point no study has looked at the overall picture of the effects of density from a system perspective by considering not only health and welfare aspects, but also all of the economic implications for the broiler industry. The results may be surprising.
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), the impact of environmental quality is reflected in the changes in the slope of the curve for the welfare problems (dashed lines) in such a way that for a given density the number and severity of welfare problems seen can be rather variable. Likewise, equivalent welfare levels may be achieved at different densities as long as good environmental quality is achieved. Therefore, perhaps a more realistic way of addressing the upper limit to density for broilers should be to insure that proper environmental conditions are met for a (reasonable) range of densities. This can be achieved, for example, by limiting maximum relative humidity, litter moisture, ammonia, and temperature ranges for the different rearing phases. This approach has the advantage of not imposing a unique limit of density per se to producers, but affords them the ability to raise a larger number of broilers (within a reasonable range of densities) as long as they are able to maintain the right environmental quality to preserve and ensure the health and welfare of the thousands of birds raised in their facilities.
This approach, however, has challenges of its own because environmental parameters are dynamic and will constantly be changing depending on the time of day, weather conditions, measurement location, etc. One possibility is to evaluate environmental quality by its consequences on broiler health, for example, by looking at the incidence of foot-pad dermatitis at the processing plant. The Swedish Broiler Welfare program has been very successful in improving the health and welfare of broilers (and turkeys), but most importantly they have involved the producers in the process. By taking this approach, the prevalence of severe foot-pad dermatitis in Sweden has decrease from 11% in 1994 to 5% in 1997 with well over 70% of the producers rearing broilers at the highest densities allowed of 36 kg/m2 (Berg, 1998).
Finally, do we have scientific data to determine what the exact density should be to ensure broiler welfare? I would suggest that science consistently indicates that the health and welfare of broilers can be achieved at a range of densities (rather than at a single density) most likely varying between 34 to 38 kg/m2. And this can be achieved as long as more emphasis is placed on educating companies and producers regarding the impact of environmental quality on broiler health and welfare.
Received for publication February 22, 2007. Accepted for publication February 22, 2007.
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