breed suitability

Modern egg layer breeds have been developed mainly for high performance in intensive egg production, e.g. cage systems, and will therefore not necessarily show the same level of egg production when tested on floor conditions (Sørensen et al., Reference SØRENSEN, DANELL, BRENØE and TUISKULA-HAAVISTO2004). Furthermore, poultry breeding stock is kept and tested in environments that are generally very different from those in which organic birds are kept (Pryce et al., Reference PRYCE, CONINGTON, SØRENSEN, KELLY and RYDHMER2004), although nowadays breeding stock is also kept in floor systems. There are health and welfare risks associated with keeping high yielding hens in outdoor systems. Despite generally high production levels, such breeds appear to be more susceptible to nutritional imbalances with possible consequences such as feather pecking, cannibalism, reduced disease resistance or inadequate behaviour such as mislaying of eggs (Sørensen et al., Reference SØRENSEN, DANELL, BRENØE and TUISKULA-HAAVISTO2004; Knierim, Reference KNIERIM2006). Information from UK egg producers suggests that there is a realisation that pursuing levels of egg output comparable to conventional systems (i.e. in excess of 300 eggs per annum) is likely to lead to problems.

Until recently, the few main breeding companies operating world-wide have not developed breeding programmes focused specifically on free-range or free-range organic production. The hybrids they currently market for free-range are the results of cross combinations with lines current in existing gene banks (Sørensen et al., Reference SØRENSEN, DANELL, BRENØE and TUISKULA-HAAVISTO2004). With the growth of the free-range sector over the last decade (Joret, Reference JORET2004), the demand for breeds more suitable for free-range conditions has increased. Breeding companies are now selecting for traits such as low levels of floor eggs, ease of management, good feathering and efficient feed conversion, in addition to high egg numbers and good liveability. Behavioural traits such as a low propensity to feather peck have also been included, as these characteristics are also heritable (Kjaer et al., 2001). The primary breeding objectives for organic farming are likely to include disease resistance and longevity, whereas production is seen as secondary because significant advances have already been made for production traits in most species in conventional farming (Pryce et al., Reference PRYCE, CONINGTON, SØRENSEN, KELLY and RYDHMER2004). This selection for production has led to deterioration in animal health (Rauw et al., Reference RAUW, KANIS, NOORDHUIZEN-STASSEN and GROMMERS1998). Other characteristics such as the ability to use roughage and reaction to predators could potentially be worthy goals for organic poultry breeding (Pryce et al., Reference PRYCE, CONINGTON, SØRENSEN, KELLY and RYDHMER2004). Organic standards recommend the use of traditional breeds for organic poultry production. Interest in restoring and improving the use of these breeds is growing. Some of the traditional, local breeds may have potential for use as laying stock in free-range production systems as they are better adapted to free range, are capable of producing on a less protein-rich diet, have satisfactory behaviour and reasonable productivity (Sørensen et al., Reference SØRENSEN, DANELL, BRENØE and TUISKULA-HAAVISTO2004).

As for laying hens, the breeding goals for boilers have been developed for conventional intensive indoor systems and not extensive outdoor (organic) systems. The breeding goals for conventional boiler production have focused on rapid growth, increased feed efficiency and increased processing yield. The high productivity of these strains depends on high levels of feed, health treatments and other inputs. Without these inputs, disease and poor welfare could result (Pryce et al., Reference PRYCE, CONINGTON, SØRENSEN, KELLY and RYDHMER2004). Therefore, conventional broiler genotypes are generally not suitable for organic systems.

Genetic selection for high productivity in conventional broilers has led to deterioration in animal health, and rapid growth rates are seen as an important cause of welfare problems in broilers (EC Scientific Committee on Animal Health and Animal Welfare, Reference EC SCIENTIFIC COMMITTEE ON ANIMAL HEALTH and ANIMAL WELFARE2000; Kestin et al., Reference KESTIN, GORDON, SU and SØRENSEN2001; Rauw et al., Reference RAUW, KANIS, NOORDHUIZEN-STASSEN and GROMMERS1998). Organic production standards require slower growing breeds that have a live weight gain that does not exceed 45 grams per day (Council Regulation (EC) 834/2007; Commission Regulation (EC) No. 889/2008), this means that chickens will reach slaughter weight after about 11 weeks, compared to the 5-6 weeks in conventional production.

Another difference between conventional and organic broiler production is that most modern genotypes are bred to suit a specific market destination (e.g. well-fleshed birds for processing ready-meal markets and smaller birds for roasting) (Pryce et al., Reference PRYCE, CONINGTON, SØRENSEN, KELLY and RYDHMER2004), whereas organic broilers tend to be produced for a more specialty niche market (Gordon and Charles, Reference GORDON and CHARLES2002a).

Reduced nutrient supply, especially at the beginning of the fattening phase, can be expected to have positive effects by reducing growth rates, thereby reducing the risk of metabolic disorders and limb damage (EC Scientific Committee on Animal Health and Animal Welfare, Reference EC SCIENTIFIC COMMITTEE ON ANIMAL HEALTH and ANIMAL WELFARE2000). Fanatico et al. (Reference FANATICO, CAVITT, PILLAI, EMMERT and OWENS2005a; Reference FANATICO, PILLAI, CAVITT, OWENS and EMMERT2005b) evaluated slow, medium and fast growing genotypes and showed that slow growing breeds had higher feed intake (and lower feed efficiency), lower breast yield and a greater leg quarter yield in comparison with fast-growing genotypes. Outdoor access stimulated locomotion, thus causing greater bone strength in the tibia, and made the meat more yellow. Castellini et al. (Reference CASTELLINI, MUGNAI and DAL BOSCO2002) compared Ross male chickens under conventional indoor conditions and organic outdoor conditions and found that the organic chickens had carcasses with higher breast and drumstick percentages and lower levels of abdominal fat. In addition, the sensory quality of the breast muscle was better.

Sørensen and Kjær (Reference SØRENSEN and KJÆR2000) investigated the potential of traditional breeds for organic egg production in Denmark. New Hampshire and White Leghorn and their crosses (selected for floor systems with a mild selection pressure on laying traits) were compared with the hybrid most commonly sold for commercial organic egg production in Denmark (ISA-Brown). This was done under organic experimental conditions. Although ISA-Brown had the highest egg yield, mortality due to cannibalism was several-fold higher (average 16% from 18-43 weeks) compared to the other traditional breeds and crosses (average 0.0-1.1% from 18-43 weeks). This highlights the potential conflict between production demands and welfare. The search for alternative breeds/hybrids has not yet produced the ideal ‘organic hen’ (Sørensen, Reference SØRENSEN2001).

In commercial practice, the UK organic sector provides some examples of successful organic systems being developed based on breeds such as the Columbian Blacktail. The success of these systems is not likely to be solely based on breed selection, but a combination of production level, breed type, and the type of management applied to achieve a successful outcome. The existence of an integrated supply chain is often a key factor in facilitating collective improvement, through better sharing of information and more direct market signals.

For broilers, local and indigenous breeds are often slow growing and these genotypes can show a good adaptation to extensive rearing conditions (Fanatico et al., Reference FANATICO, PILLAI, CAVITT, OWENS and EMMERT2005b). Gordon (Reference GORDON2002) evaluated a wide range of breeds of (organic) table birds on their suitability for use in extensive production systems, taking into account the effects of diet composition and diurnally fluctuating post-brooding temperatures (as would be experienced by outdoor chickens). Four breed-types that differed in growth rate were evaluated:

• • Fast growing breeds (broiler hybrids Ross 308, Ross 508, and Ross YA x PM3)

• • Medium to fast growing breeds (commercial hybrids Hubbard ISA 757, ISA 957, Redbro, and Master Gris)

• • Slow growing breeds (commercial hybrids Hubbard ISA 457, ISA 657, and Gris Barre)

• • Very slow growing breeds (traditional UK breeds Light Sussex, White Sussex, Ixworth and White Dorking)

Project recommendations were that breeds should be chosen for use in an extensive production system according to their growth profile (when daytime access to feed is not restricted) and desired market live weight at slaughter age. Suitable breeds will be those that are active and inquisitive as they are likely to be better rangers and foragers than the less active broiler hybrids. Breeds that show extreme escape responses and ground peck in a stereotypic manner should be avoided as they will be more difficult to manage and there may be a risk of aggressive feather pecking. Another factor to take into consideration when selecting a breed for an organic system is plumage colour, as this may affect the chickens’ ability to hide from predators; white feathering may increase the risk of predation.

Modern poultry production has specialised in the production of a single poultry product, either eggs or meat. Hence, the suitability of many hybrids for dual purpose production has been lost (Pryce et al., Reference PRYCE, CONINGTON, SØRENSEN, KELLY and RYDHMER2004). The development of dual-purpose breeds, combining both egg and meat production, could potentially fulfil a role in organic production if demands on production are not as high as for conventional production. The development of dual-purpose breeds may also resolve the ethical issue of killing redundant male chicks of egg laying hybrids (Nauta et al., Reference NAUTA, ROEP, VEERKAMP and BAARS2003). This practice conflicts with the organic philosophy to respect the integrity of the animal. Within a dual-purpose breed, males could be fattened for the meat market, which would in turn require the development of economic markets for young meat birds.

It is open to debate whether organic production systems are sufficiently different from conventional free-range systems to make switching to an alternative breed or strain worth while (Pryce et al., Reference PRYCE, CONINGTON, SØRENSEN, KELLY and RYDHMER2004). Information from UK Certification Bodies suggest that while long-term there may be benefits from better genetic selection, or breed substitution, much improvement in organic production systems could be achieved even with existing breeds and strains. Including traits that are important for health and welfare alongside the more conventional traits in poultry breeding indexes may help capture a market opportunity for breeding birds that are more robust and that are specifically tailored to the organic market. The organic sector could also consider differentiating itself from conventional breeding by including ethical, welfare and social factors (all with a low economic value) into breeding goals.

Sørensen (Reference SØRENSEN2001) suggests two strategies to solve the organic breed issue, firstly, a continuous search for breeds or lines that show suitability for organic conditions and secondly, to initiate a breeding programme for laying hens that takes account of the specific requirements for organic egg and meat production. Broiler breeds should be selected for the type of systems they are to perform in. The use of slower growing breeds in organic farming is justified as it aims to limit welfare problems due to fast growth. Practically, the choice of breed or strain may be limited by the cost of day-old chicks and availability, although more robust hybrids are becoming available that are better suited to free range systems.

Pryce et al. (Reference PRYCE, CONINGTON, SØRENSEN, KELLY and RYDHMER2004) suggests that because populations of many local or indigenous breeds are too small to make efficient genetic progress, a better way forward may be to cross valuable genes from indigenous breeds into another population. Furthermore, existing breeds and lines can be selected under organic conditions so that resulting hybrids are adapted for organic production (Nauta et al., Reference NAUTA, ROEP, VEERKAMP and BAARS2003). Nauta et al. (Reference NAUTA, ROEP, VEERKAMP and BAARS2003) further suggested that it could be beneficial for organic agriculture to establish a central organisation that could coordinate breeding activities.

nutrition

Feeding a wholly organic diet to poultry can present a health risk primarily because of the difficulty in sourcing a consistent supply of nutrients, and the legislative prohibition of synthetic amino acids and vitamins in organic poultry feed. These risks are likely to be exacerbated by an increasing requirement for local self-sufficiency in organic feed supply to reduce the reliance on brought-in feeds.

The supply of nutrients to egg layers in a balanced manner, so that their requirements for production and health are fully met, has been highlighted as one of the most challenging aspects of organic egg production (Gordon et al., Reference GORDON, COTTRILL, TOMICZEK, VERHOEVEN, WEIGHTMAN, SAFFORD, NICHOLSON, HOLMES, TURNER and VAN DE WEERD2006; Lampkin, Reference LAMPKIN1997; Zollitsch et al., Reference ZOLLITSCH, KRISTENSEN, KRUTZINNA, MACNAEIHDE and YOUNIE2004). The range of organic proteinaceous ingredients available for feeding organic laying hens is relatively small and all sources are deficient in certain essential amino acids, particularly methionine and lysine (Gordon and Charles, Reference GORDON and CHARLES2002b; Gordon, Reference GORDON2004; Hancock et al., Reference HANCOCK, WELLER and MCCALMAN2003; Zollitsch et al., Reference ZOLLITSCH, KRISTENSEN, KRUTZINNA, MACNAEIHDE and YOUNIE2004). Therefore, there is less scope for balancing nutrient supply.

Whilst short-term allowances to feed small percentages of non-organic feedstuffs exist, the legislative requirement for a 100% organic feed for laying hens will be put in place as from 1^st of January 2012 (Council Regulation (EC) 834/2007; Commission Regulation (EC) No. 889/2008). Under these conditions, and to meet the nutritive requirements of laying hens, methionine-rich organic protein sources are needed. Diets low in methionine can reduce egg mass output, but more importantly there may be adverse effects on immuno-competence and feather pecking (Gordon et al., Reference GORDON, COTTRILL, TOMICZEK, VERHOEVEN, WEIGHTMAN, SAFFORD, NICHOLSON, HOLMES, TURNER and VAN DE WEERD2006). Elwinger et al. (Reference ELWINGER, TUFVESSON and HARTMANN2002) found reduced feather cover and reduced egg weight in hens fed on organic diets with reduced methionine content. Laying hens are able to compensate partially for a suboptimal supply of limited amino acids by an increase in feed intake, although a diet with relatively high energy content will limit consumption (Sundrum et al., Reference SUNDRUM, SCHNEIDER and RICHTER2005). Furthermore, implications of limited availability of feedstuffs for growth and health heavily depends on the capacity of animals at various stages of their development to adapt to, and compensate for, changes in nutrient supply. Sundrum et al. (Reference SUNDRUM, SCHNEIDER and RICHTER2005) recommend that special attention should be given to young animals in their first week of life, as they are more sensitive to an unbalanced nutrient supply and require high quality protein.

The energy requirements of free range (organic) laying hens are higher than those of birds in conventional cage systems due to increased demand for movement and thermo-regulation in potentially more variable environmental conditions (Sundrum et al., Reference SUNDRUM, SCHNEIDER and RICHTER2005). Furthermore, since the hybrids currently widely used as organic laying hens are of a very high genetic potential, originally developed for intensive systems, they require high quality feed (Weller et al., Reference WELLER, MCCALMAN and HANCOCK2003; Zollitsch et al., Reference ZOLLITSCH, KRISTENSEN, KRUTZINNA, MACNAEIHDE and YOUNIE2004). Weller et al. (Reference WELLER, MCCALMAN and HANCOCK2003) highlight the practical and economic issue of inconsistency of supply of locally produced organic feed with the desired high nutrient concentration and energy density. This reduces the flexibility to incorporate a variety of organic feed ingredients and places reliance on imported feeds with a high nutrient density. Not only does this place economic constraints on the growth of organic poultry production, but is also contrary to the organic principles of utilising local resources and cycling of nutrients in the system (Horsted et al., Reference HORSTED, HAMMERSHØJ and HERMANSEN2006). This demonstrates the need for alternative feeding strategies based on organic feedstuffs and for alternative poultry breeds and strains that may be more adapted to the restricted availability of limiting amino acids (Baars et al., Reference BAARS, WAGENAAR, PADEL and LOCKERETZ2004; Zollitsch et al., Reference ZOLLITSCH, KRISTENSEN, KRUTZINNA, MACNAEIHDE and YOUNIE2004; Sundrum et al., Reference SUNDRUM, SCHNEIDER and RICHTER2005).

Gordon et al. (Reference GORDON, COTTRILL, TOMICZEK, VERHOEVEN, WEIGHTMAN, SAFFORD, NICHOLSON, HOLMES, TURNER and VAN DE WEERD2006) identified a number of promising novel protein sources for feeding to organic laying hens. The novel proteins were evaluated for their nutritional value, effects on bird health and welfare and methods for production and processing. Promising invertebrates, with good protein contents and suitable amino acid profiles, included fly pupae or larvae and earthworms. The protein provided by these invertebrates is of very good quality and the amino acid profile is similar to that of fish meal. Promising plant sources were microalgae such as Chlorella (a single-celled, non-motile green alga), Micractinium (a colonial algae) and Spirulina (Arthrospira, a filamentous, spiral-shaped, multicellular blue-green algae, cyanobacteria), protein-rich herbs such as purslane and to a lesser extent aquatic plants such as duckweed (e.g. Lemna gibba). The study concluded that novel protein sources are a huge biomass that is currently under-utilised and that there is potential to develop some as feedstuffs for organic laying hens. They also offer potential to recycle nutrients, which is in-keeping with the organic ethos. However, if these protein sources are to be utilised, it will be most efficient to produce and process them and feed them as meals, after drying and grounding. Whether this is cost-effective is currently unknown. Such feeds would also have to be included on the approved list of organic feed sources.

In a similar way that nutrition is a risk factor for health and welfare in organic laying hens, it is also a risk factor for organic broiler production. Although organic chicken producers do not aim for the same growth rates as conventional broiler flocks (81 days minimum killing age rather than 42), the organic slower growing strains are still growing quickly, and their amino acid requirement is very high (Weller et al., Reference WELLER, MCCALMAN and HANCOCK2003). The risk of imbalanced diets is likely to be increased with the imminent move to 100% organic diets in 2012 (Council Regulation (EC) 834/2007; Commission Regulation (EC) No. 889/2008). In addition, changes in feed formulation during manufacture, because certain ingredients become unavailable or are too expensive, could also lead to problems. A further factor in broiler production is that oversupply of total protein (if too much low quality protein is fed) can result in excess N excretion (Sundrum et al., Reference SUNDRUM, SCHNEIDER and RICHTER2005). This can have detrimental effects on litter quality and ammonia levels in the poultry house, which are risk factors for contact dermatitis. Furthermore, imbalanced diets can increase the risk of feather pecking (Van de Weerd and Elson, Reference VAN DE WEERD and ELSON2006). Reports from organic producers indicate that this is a real concern, and that feather pecking in broilers is seen at an increasing rate (pers. comm. large UK broiler company).

There is currently little information available about feeding practices in organic broiler production (Sundrum et al., Reference SUNDRUM, SCHNEIDER and RICHTER2005). A limited number of studies suggest that feeding a 100% organic diet to broilers is possible, although there are possible implications for costs and health and welfare (O'Brien et al., Reference O'BRIEN, ASPRAY and PHILIPPS2006). O'Brien et al. (Reference O'BRIEN, ASPRAY and PHILIPPS2006) compared an 80% and 100% organic diet fed to organic chickens. No overall growth, health or welfare concerns were identified when comparing the two rations, nor were there increases in production costs. These assessments were done over a summer period, but early results of the winter trial indicated that there was a larger difference in the performance of the birds as well as increased costs associated with the 100% ration. This shows that costs can be dependent on seasonal availability of raw materials and market value. Bellof and Schmidt (Reference BELLOF and SCHMIDT2005) investigated the effect of organic diets when using a slow growing strain (ISA J 257). The rations differed in the level of energy and essential amino acids. Feed intake in the different feeding groups negatively correlated with the energy level of the diets. Performance and carcass yield reached a high level under the organic production conditions. The authors concluded that the organic rations enabled a 100% organic feed with an acceptable performance and with low animal losses.

Sundrum et al. (Reference SUNDRUM, SCHNEIDER and RICHTER2005) provided a list of measures that an organic poultry producer can adopt to improve production:

• • Use slow growing strains, thereby reducing nutrient requirements in the different stages of growth and development

• • Implement multiple phase feeding, to adapt supply more closely to requirements during the various stages of growth and development, and thereby make optimum use of high quality proteins

• • Segregate housing for the sexes, to allow for the differing requirements of both genders

• • Increase feed intake by optimising feeding and housing arrangements, or by reducing the energy content of the diet, thereby providing opportunities to increase the use of home-grown feedstuffs (e.g. on the range)

• • Use compensatory growth potential in the genotype selected, thereby reducing the demand for high protein feedstuffs

• • Purchase protein sources like rapeseed cake, soybean cake, or skim milk powder of organic origin to compensate for deficits in limiting amino acid supply, especially for animals in the first weeks of life

Providing balanced diets to organic hens is a challenge and ongoing concern for the organic producer. Some studies reveal that organic egg production can achieve performances comparable with those of conventional husbandry by using high-value feed sources (Sundrum et al., Reference SUNDRUM, SCHNEIDER and RICHTER2005). However, there is a need for further research to investigate options to optimise the production of eggs under organic conditions, as not enough is known about the relationship between nutritional imbalances and health and welfare. There is also a need for studies on the implications of organic conditions on broiler production and the capacity of broiler strains to adapt to changes in nutrient supply (Sundrum et al., Reference SUNDRUM, SCHNEIDER and RICHTER2005). Increased outdoor foraging of poultry is consistent with the principle of increasing the utilisation of local resources and increased cycling of nutrients within the farm system (Gordon and Charles, Reference GORDON and CHARLES2002a; Horsted et al., Reference HORSTED, HAMMERSHØJ and HERMANSEN2006). This would further ease the transition to 100% organic feed and save feed costs. However, if individual birds do not use the range this feed source will not be available to them, so the need to provide a complete feed in the house will remain. If optimal use of a variable outdoor area is to be achieved, rotation within a flock may be necessary, not just between flocks.

feed contribution from range

Providing poultry with an outdoor area gives them access to an extra source of feed, in addition to the feed supplied by the farmer (Gordon and Charles, Reference GORDON and CHARLES2002a). Depending on the type of outdoor area, birds can consume vegetation, fruit, seeds and will also feed on a wide variety of macro invertebrates (such as beetles, spiders and earthworms) from the soil surface (Clark and Gage, Reference CLARK and GAGE1996, Reference CLARK and GAGE1997; Mwalusanya et al., Reference MWALUSANYA, KATULE, MUTAYOBA, MINGA, MTAMBO and OLSEN2002). Grassland can also add to the birds’ nutrient requirements if high nutrient-value species are present. The potential contribution is very seasonal, as the nutritional value of grass changes throughout the year, with protein concentrations highest in spring and summer (Walker and Gordon, Reference WALKER A. and GORDON2003). In addition, the sward must be managed so that it is suitable for foraging and ingestion; otherwise there is a risk of crop compaction (Gordon and Charles, Reference GORDON and CHARLES2002a; Christensen, Reference CHRISTENSEN1998).

Freedom to range gives individual birds the opportunity to supplement their diet with the nutrients they need. Nutritional requirements can vary between individuals, and can also change over time according to the individuals’ health, growth and egg laying status. Hens are able to distinguish different nutrients from different feed sources, enabling them to compose their diets according to their needs (Burel et al., Reference BUREL, CISZUK, BRÄNNÄS, WIKLUND, KIESSLING and LILJEDAHL2000). This is not possible when standard compounded poultry feed is offered, as is the case in indoor systems. Organic farms can have greater biodiversity than conventional farms (Fuller et al., Reference FULLER, NORTON, FEBER, JOHNSON, CHAMBERLAIN, JOYS, MATHEWS, STUART, TOWNSEND, MANLEY, WOLFE, MACDONALD and FIRBANK2005; Hole et al., Reference HOLE, PERKINS, WILSON, ALEXANDER, GRICE and EVANS2005; Soil Association, Reference SOIL ASSOCIATION2000) with greater wildlife abundance and diversity (higher weed levels, greater plant species richness or higher invertebrate numbers). These are all potential feed sources for poultry and will give organic birds a wide range of (natural) feed sources for foraging on the range.

Gordon et al. (Reference GORDON, COTTRILL, TOMICZEK, VERHOEVEN, WEIGHTMAN, SAFFORD, NICHOLSON, HOLMES, TURNER and VAN DE WEERD2006) investigated the nutritional value of insects (fly pupae or larvae) and earthworms as alternative protein sources for organic laying hens. However, relying on the hens own intake of fresh invertebrates to provide for their protein needs is a risk, as the crude protein content of fresh fly pupae/larvae or earthworms is considerably reduced due to a high moisture content (in comparison to concentrated dry feeds). Supplies in an outdoor area can also be exhausted very quickly by a large group of foraging hens, as they prefer highly nutritious earthworms and insects (Horsted and Hermansen, Reference HORSTED and HERMANSEN2007). Furthermore, the contribution of fresh invertebrates to the hen's protein requirements is likely to be variable and unreliable, being affected by factors such as range usage, season, climate and management (Clark and Gage, Reference CLARK and GAGE1996; Mwalusanya et al., Reference MWALUSANYA, KATULE, MUTAYOBA, MINGA, MTAMBO and OLSEN2002; Sonaiya, Reference SONAIYA2004; Bassler et al., Reference BASSLER, CISZUK and SJELIN2000).

Few studies exist on the amount of feed that poultry actually ingest from an outdoor area, but recently Horsted and colleagues conducted the first extensive studies on nutrient intake from the range (Horsted et al., Reference HORSTED, HAMMERSHØJ and HERMANSEN2006, Horsted and Hermansen, Reference HORSTED and HERMANSEN2007). Organic hens (nutrient restricted and non-restricted hens) were offered different forage crops in a series of experiments. Productivity and welfare, egg quality, amount of forage consumed and selectivity of feed from forage were investigated by analysing crop contents. A range of forage crops were offered in different combinations, these were grass/clover (Lolium perenne and Trifolium repens), a mixture of forbs (Fagopyrum esulentum, Phacelia tanacetifolia, Linum usitatissimum, expected to attract a lot of insects in the flowering season), chicory (Cichorium intybus cv. Grassland Puna) and pea/vetch/oats, lupin and quinoa. The results indicated that the hens consumed a considerable amount of herbage from the plots. The intake of grass/clover was 10-30 g per hen per day, increasing to 20-40 g per hen per day for hens that were nutrient-restricted. Although they lost weight during the study, it was estimated that the forage area on average had supplied the nutrient-restricted hens with approximately 70% of their lysine and methionine requirements and approximately 25% of their calcium requirements. It was estimated that after a period of adaptation, hens could consume up to 0.25 MJ ME of their requirements of ME from forage. The hens showed a preference for quinoa seeds (compared with seeds of lupin and pea/vetch/oats). Chicory was also popular, and the hens showed relatively high egg production, consistent with the fact that chicory leaves contain relatively high levels of lysine and methionine. Nutrient-restricted hens had more plant material, grit stone, soil and oyster shells found in their crops, and ingested significantly more earthworms and insects than non-restricted hens. This indicated that they were trying to fulfil their nutrient requirements through a higher intake of supplementary food items from the plots. The nutrient-restricted hens needed a period of adaptation, but then produced well in the crop rotation system, since laying rate was comparable to the non-restricted hens. The authors concluded that high-producing (organic) layer strains are able to consume considerable amounts of herbage and that the forage can provide important nutrients.

If good forage is constantly available on the outdoor area, it seems possible to lower the levels of important nutrients in the feed supplied to the hens, as they can supplement their feed from the range. However, supply in an outdoor area can become exhausted very quickly and therefore a good plot rotation system is required.

range use

Range use is important as it has been linked to a number of issues that can affect health and welfare. In addition to providing an additional source of nutrition (see previous section), several studies in laying hens have found that increasing range use is inversely related to the prevalence of feather pecking (see reviews in Knierim, Reference KNIERIM2006; Van de Weerd and Elson, Reference VAN DE WEERD and ELSON2006). Free range organic flocks that spend more time outside are generally healthier, more productive and better feathered than those that do not range well (Bestman and Keppler, Reference BESTMAN and KEPPLER2005). The risk of feather pecking in organic flocks was found to increase when less than 66% of the flock used the range (Bestman and Wagenaar, Reference BESTMAN and WAGENAAR2003). A range area can also stimulate increased activity for organic broilers thereby improving leg health (Rodenburg et al., Reference RODENBURG, VAN DER HULST-VAN ARKEL and KWAKKEL2004).

The fact that organic farming requires an outdoor area does not mean that all the birds in a flock actually use the range. A number of measures can be implemented to stimulate range use. These include an attractive range, a good rotation system, the use of smaller flocks, access to the range from a young age and protection against predators. Scientific evidence for these measures has been reviewed in this section.

Outdoor use can be stimulated by offering a range that is attractive to the chickens in that it provides cover in the form of trees, bushes or hedges or artificial structures (Bestman and Wagenaar, Reference BESTMAN and WAGENAAR2003, Bestman and Keppler, Reference BESTMAN and KEPPLER2005; Hegelund, et al., 2005). Range quality is more important than size (Bestman and Keppler, Reference BESTMAN and KEPPLER2005). Zeltner and Hirt (Reference ZELTNER and HIRT2003) found that a higher percentage of hens used the furthest quarter of the range if there were structures present and the quality and variation of the structures influenced the use of the range more than the amount of structures per se (Zeltner et al., Reference ZELTNER, HIRT and HAUSER2004). Another means of making the range area more attractive is to offer attractive forage crops as a supplement to the daily ration (Horsted et al., Reference HORSTED, HAMMERSHØJ and HERMANSEN2006).

As for laying hens, good cover on the range will also encourage broilers to range. The number of birds found to be ranging outside was positively correlated with the amount of tree cover on farms rearing slower growing broilers (Dawkins et al., Reference DAWKINS, COOK, WHITTINGHAM, K.A. and HARPER2003). Studies on slow growing 'Label Rouge' chickens in France suggested that trees are attractive to chickens, as they offer a place of cover for rest and shelter (Lubac and Mirabito, Reference LUBAC and MIRABITO2001). However, Jones et al. (Reference JONES, FEBER, HEMERY, COOK, JAMES, LAMBERTH and DAWKINS2007) found that there was no effect of the presence of young trees on ranging behaviour, suggesting that trees have to be reasonably mature to provide sufficient cover to affect the behaviour of the birds. Hedges also provide cover and protection from the wind and sun, and can positively influence ranging (Jones et al., Reference JONES, FEBER, HEMERY, COOK, JAMES, LAMBERTH and DAWKINS2007). The level of plant canopy can also influence bird activity in the area visited, as in heavily shaded areas e.g. under established trees, birds tended to lie down, whereas standing was the predominant activity in non-shaded areas (Mirabito and Lubac, Reference MIRABITO and LUBAC2001). Outside temperature influences ranging behaviour of broilers directly, with least ranging in winter, spring and in bright sunshine (Dawkins et al., Reference DAWKINS, COOK, WHITTINGHAM, K.A. and HARPER2003; Jones et al., Reference JONES, FEBER, HEMERY, COOK, JAMES, LAMBERTH and DAWKINS2007). Despite the provision of cover, the maximum number of broilers seen ranging in a flock is generally low. Dawkins et al. (Reference DAWKINS, COOK, WHITTINGHAM, K.A. and HARPER2003) observed that the maximum number of birds outside was 15% of the total flock. Another free-range broiler study reported an average of 12% and 14% of the flocks ranging on two different farm sites (Jones et al., Reference JONES, FEBER, HEMERY, COOK, JAMES, LAMBERTH and DAWKINS2007). In the 'Label Rouge' study, the percentage of chickens outside increased significantly with age from 11% to 23% between seven and eleven weeks (Mirabito and Lubac, Reference MIRABITO and LUBAC2001).

There is a risk that the majority of birds stay near the house if the range is not made attractive (Bassler et al., Reference BASSLER, CISZUK and SJELIN2000; Zeltner and Hirt, Reference ZELTNER and HIRT2003; Hegelund, et al., 2005; Hirt et al., Reference HIRT, HÖRDEGEN and ZELTNER2000). Aarnink et al. (Reference AARNINK, HOL and BEURSKENS2006) measured that up to 45% of chicken manure was deposited in the 20 m next to a hen house, indicating that a large proportion of the flock stayed near the house. Besides the health implications, this has environmental implications as the nutrient load will be high near the house (Aarnink et al., Reference AARNINK, HOL and BEURSKENS2006, Elbe et al., Reference ELBE, ROß, STEFFENS, VAN DEN WEGHE and WINCKLER2005). These nutrients (N, P, K) will be in excess of plant growth requirements, as often there is no plant cover next to the hen house, so these will be lost through run off, leaching to the groundwater or accumulating in the soil (Aarnink et al., Reference AARNINK, HOL and BEURSKENS2006). Elbe et al. (Reference ELBE, ROß, STEFFENS, VAN DEN WEGHE and WINCKLER2005) calculated that when approximately 10% of a flock of 4500 organic hens used the range, approximately 5% of the total faeces output was deposited outside of the house.

Rotating the use of the range will help to prevent loss of vegetation. Fürmetz et al. (Reference FÜRMETZ, KEPPLER, KNIERIM, DEERBERG and HEß2005) monitored the use of the range (15 m² per hen) in conjunction with the rotation schedule in a small flock of 700 organic chickens. The hens ranged well in this flock (35% of hens on average outside). In order to fully maintain a green run without permanent loss of vegetation, a rotation interval of about two weeks was needed during the growing season. During winter, the interval could be extended to 6 weeks without any harm to the sward.

Compared with conventional free range flocks, organic farms have on average, smaller flock sizes (Berg, Reference BERG2001; Hörning et al., Reference HÖRNING, TREI and SIMANTKE2004). Research has shown that in small flocks generally more laying hens range simultaneously than in large flocks (Bubier and Bradshaw, Reference BUBIER and BRADSHAW1998; Zeltner et al., Reference ZELTNER, HIRT and HAUSER2004; Hegelund et al., Reference HEGELUND, SØRENSEN, KJÆR and KRISTENSEN2005). In small flocks (<500 hens) about 40% of the hens can be seen to range (Bubier and Bradshaw, Reference BUBIER and BRADSHAW1998; Zeltner et al., Reference ZELTNER, HIRT and HAUSER2004), whereas in organic large flocks (>1500) this has been reported to be only 5-10% (Elbe et al., Reference ELBE, ROß, STEFFENS, VAN DEN WEGHE and WINCKLER2005; Hegelund et al., Reference HEGELUND, SØRENSEN, KJÆR and KRISTENSEN2005). However with a range providing good cover even in flocks of 2000 hens, more than 75% of the hens could be seen outside (Bestman and Wagenaar, Reference BESTMAN and WAGENAAR2003).

Ranging behaviour is influenced by the age at which laying pullets first get access to the range. Experience of the outside environment during rearing, increases the hens’ readiness to use an outdoor area as adults (Grigor et al., Reference GRIGOR, HUGHES and APPLEBY1995a). For organic production, Bestman and Keppler (Reference BESTMAN and KEPPLER2005) recommend acclimatising pullets to the outside area from an early age (around 6 weeks of age) on a range that offers good overhead cover to stimulate ranging behaviour.

In every poultry system in which chickens have access to an outdoor area there is a risk of predation by birds of prey, crows, foxes or badgers (e.g. Dawkins, et al., 2003; Hegelund et al., Reference HEGELUND, SØRENSEN, KJÆR and KRISTENSEN2005; Jones et al., Reference JONES, FEBER, HEMERY, COOK, JAMES, LAMBERTH and DAWKINS2007; Knierim, Reference KNIERIM2006; Moberley et al., Reference MOBERLEY, WHITE and HARRIS2004). Dawkins et al. (Reference DAWKINS, COOK, WHITTINGHAM, K.A. and HARPER2003) reported attacks by crows on broilers where two or three crows would co-operate to kill a chicken. The mortality rate can vary between farms. In a survey of Swiss farms with non-cage systems (mean number of birds per farm was 3042), the average estimated loss to predators in the free-range area was 6.7 birds per year per farm, but on 9% of the farms, losses exceeded 20 birds per year (Häne et al., Reference HÄNE, HUBER-EICHER and FRÖHLICH2000). Mortalities caused by predators in organic egg production systems in Denmark was on average 6.4% of the flock (Hegelund et al., Reference HEGELUND, SØRENSEN and HERMANSEN2006). A survey of UK certified organic pullet producers revealed predation to be a main cause of mortality. This was mentioned by 12.5% of the producers (Sparks et al., Reference SPARKS, CONROY and SANDILANDS2008). Whilst terrestrial predators can be kept away by using electric fencing, a majority of free-range farmers surveyed, reported fox predation despite the use of electric fencing (Moberley et al., Reference MOBERLEY, WHITE and HARRIS2004). This suggests that the farm manager plays a significant role in keeping predators away using active elimination. Maintaining cockerels within a flock has been recommended as a deterrent, as they instinctively scan the sky and warn the hens in case of danger such as the presence of any predators (Bassler et al., Reference BASSLER, CISZUK and SJELIN2000; Bestman and Keppler, Reference BESTMAN and KEPPLER2005).

Free-range birds can have a high motivation to drink from puddles on the range. This was observed by Jones et al. (Reference JONES, FEBER, HEMERY, COOK, JAMES, LAMBERTH and DAWKINS2007) where a large number of broilers birds flocked out of the house after a rain shower to drink from standing water. This behaviour is not to be encouraged, because of concerns for bio-security, in that puddles and standing water could potentially facilitate the transmission of infectious diseases such as Avian Influenza (Gordon and Charles, Reference GORDON and CHARLES2002a).

Good range use has been shown to be beneficial for health and welfare, although ranging behaviour in broilers has hardly been studied. However, the benefits may have to be off-set against certain risks associated with outdoor use (e.g. predation, parasites, reduced bio-security). The white plumage colour of many broiler breeds may not help in reducing predation, as they will stand out in the environment. This could be taken into consideration when selecting a breed for an organic system.

group size

Optimal group size is often a point of discussion amongst organic producers, and different certification bodies allow different maximum group sizes. The underlying assumptions are that smaller groups offer better hen welfare. Relatively little is known about the social priorities of hens (i.e. how they value belonging to different group sizes or different group compositions), but group size has been shown to influence feather pecking, aggression and ranging. Research has mainly focussed on laying hens.

The relationship between group size and feather pecking is complicated and contradictory findings have been reported. Larger groups (non-cage) have been shown to perform more feather pecking and/or cannibalism (Nicol et al., Reference NICOL, GREGORY, KNOWLES, PARKMAN and WILKINS1999; Bilcik and Keeling, Reference BILCIK and KEELING2000). These studies were done in groups of less than 400 birds. Niebuhr et al. (Reference NIEBUHR, ZALUDIK, BAUMUNG, LUGMAIR and TROXLER2005) suggests that the relatively low levels of injurious pecking in Austrian free range and organic flocks with intact beaks is partly explained by the relatively small flock size (approx. 1000 birds on average). In contrast, others have found lower levels of feather pecking in large commercial (non-cage) flocks compared with smaller flocks (from 2450-4200 birds) (Zimmerman et al., Reference ZIMMERMAN, LINDBERG, POPE, GLENN, BOLHUIS and NICOL2006). Gunnarsson et al. (Reference GUNNARSSON, KEELING and SVEDBERG1999) did not find a correlation between group size and cannibalism (flocks from 225 to 9954 birds). Aggressive behaviour is infrequent in large flocks (many hundreds or thousands) compared to that reported in small to medium-sized flocks, possibly due to hens not recognising flock mates as familiar or unfamiliar (Hughes et al., Reference HUGHES, CARMICHAEL, WALKER and GRIGOR1997). Laying hens are able to discriminate between different individuals within their own social group and therefore seem to prefer to associate with familiar rather than strange individuals or groups of hens (Hughes, Reference HUGHES1977; Bradshaw, Reference BRADSHAW1992; Grigor et al., Reference GRIGOR, HUGHES and APPLEBY1995b). There is limited evidence that hens prefer smaller group sizes (below 100 birds) in which they can recognise other hens as individuals (Nicol et al., Reference NICOL, GREGORY, KNOWLES, PARKMAN and WILKINS1999).

Flock size can influence hen welfare, but the relationship is unclear. Furthermore, there is some evidence that hens give greater priority to (personal) space than to group size (Lindberg and Nicol, Reference LINDBERG and NICOL1996; Albentosa and Cooper, Reference ALBENTOSA and COOPER2004).

feather pecking

Feather pecking and cannibalism are welfare problems that can occur in every poultry system (Appleby and Hughes, Reference APPLEBY and HUGHES1991) and are therefore not specific to organic egg production. However, it has become clear over recent years that high mortality can occur in free range systems, including organic, and that feather pecking and cannibalism can be a main contributory factor (Van de Weerd and Elson, Reference VAN DE WEERD and ELSON2006). A higher level of feather pecking has been correlated with higher mortality, although this relationship is not so clear for other forms of cannibalism (such as cloacal cannibalism or vent-pecking) (Hughes and Duncan, Reference HUGHES and DUNCAN1972; Allen and Perry, Reference ALLEN and PERRY1975; Kjaer and Sørensen, Reference KJAER and SØRENSEN2002). Niebuhr et al. (Reference NIEBUHR, ZALUDIK, BAUMUNG, LUGMAIR and TROXLER2005) state that feather pecking is a valuable predictor for injurious pecking. They found that good feather cover in conventional and organic free range birds was associated with a reduced risk of injurious pecking of approximately 93%.

Compared to cages, once feather pecking and cannibalism occur in non-cage housing systems, there is a greater tendency for such behaviour to spread throughout the flock because of the larger group sizes, thus potentially affecting more individual birds (Abrahamsson and Tauson, Reference ABRAHAMSSON and TAUSON1995; Van de Weerd and Elson, Reference VAN DE WEERD and ELSON2006). Feather pecking is not aggressive behaviour. In laying hens it can start due to several factors, such as feed deficiencies, absence or poor quality of litter, boredom and insufficient opportunity to perform their natural behaviour (Menke et al., Reference MENKE, WAIBLINGER, STUDNITZ and BESTMAN2004). Feather pecking behaviour has been studied extensively, and a range of contributory factors have been identified (Van de Weerd and Elson, Reference VAN DE WEERD and ELSON2006).

In conventional systems, beak trimming is used as a preventative measure. Beak-trimming does not necessarily prevent feather pecking as such (e.g. Croxall and Elson, Reference CROXALL and ELSON2007), but limits the damage that hens can do when they have intact beaks, and reduces mortality rates compared with non-beak trimmed hens (Blokhuis et al., Reference BLOKHUIS, FIKS VAN NIEKERK, BESSEI, ELSON, GUÉMENÉ, KJAER, LEVRINO, NICOL, TAUSON, WEEKS and VAN DE WEERD2007). In organic systems, beak-trimming is not allowed for routine use, and is prohibited by some Certification Bodies. Beak trimming only reduces the symptoms of an inappropriate environment, without solving the underlying problems (Menke et al., Reference MENKE, WAIBLINGER, STUDNITZ and BESTMAN2004). Feather pecking can be viewed both as a symptom of reduced animal welfare and a cause of further welfare deterioration (Menke et al., Reference MENKE, WAIBLINGER, STUDNITZ and BESTMAN2004)

Non-cage systems (including organic) have the potential to provide good welfare in comparison to cage systems, as they enable a much fuller expression of normal behaviour and allow hens to fulfil behaviour priorities such as nesting, perching, foraging and dust bathing, however, the presence of apparently purposeless behaviour or of high levels of redirected behaviours such as feather pecking and cannibalism, indicate that a particular management system is not satisfactory for bird welfare (Blokhuis et al., Reference BLOKHUIS, FIKS VAN NIEKERK, BESSEI, ELSON, GUÉMENÉ, KJAER, LEVRINO, NICOL, TAUSON, WEEKS and VAN DE WEERD2007). Whether organic systems realize their welfare potential can be assessed by comparing prevalence data of feather pecking in different housing systems.

endoparasites

Organic poultry production requires access to outdoors. This carries a higher risk of acquiring infections in comparison with indoor poultry systems, where applying high levels of biosecurity is relatively easy (Dahl et al., Reference DAHL, PERMIN, CHRISTENSEN, BISGAARD, MUHAIRWA, PETERSEN, POULSEN and JENSEN2002; Permin et al., Reference PERMIN, BISGAARD, FRANDSEN, PEARMAN, KOLD and NANSEN1999). An outdoor area allows closer contact between birds and faeces, parasites or hosts (wild birds), increasing the risk of infections and potentially resulting in the emergence (or re-emergence) of new parasitic infections (Permin et al., Reference PERMIN, BISGAARD, FRANDSEN, PEARMAN, KOLD and NANSEN1999; Thamsborg and Roepstorff, Reference THAMSBORG and ROEPSTORFF2003). The restricted use in organic farming of anthelminthics and anti-parasiticides makes controlling parasitic infections more difficult.

Roundworms such as Ascaridia and Heterakis have a direct lifecycle meaning that they will directly contaminate the environment by releasing infectious material without the need for an intermediate host organism (Jacobs, Reference JACOBS2007). On the other hand, tapeworms such as Railietina, require an intermediate host such as insects, crustaceans, earthworms or snails. Infection with this tapeworm is an emerging problem in floor housed poultry, which become infected by ingesting beetles (that breed in contaminated litter) or other intermediate hosts from the outdoor environment. It has been shown that hens with access to an outdoor range area often have higher faecal worm egg counts than hens without access to range (Permin et al., Reference PERMIN, BISGAARD, FRANDSEN, PEARMAN, KOLD and NANSEN1999; Häne et al., Reference HÄNE, HUBER-EICHER and FRÖHLICH2000).

High parasitic infection rates may affect health and reduce growth rates (through loss of appetite). Some breeds are more susceptible than others. Gauly et al. (Reference GAULY, BAUER C., PREISINGER and ERHARDT2002) observed significantly higher faecal egg outputs from Ascaridia galli, in white laying hens (Lohmann LSL) than in brown hens (Lohmann Brown), and estimated sufficiently high heritabilities in faecal egg count to allow for selection for resistance. However, parasite resistance is not a major criterion in poultry breeding at present (Maurer et al., Reference MAURER, AMSLER, HECKENDORN and PERLER2007). Low infection rates may not cause a problem for the animals, but there is the additional risk that nematodes act as vectors of pathogens (Knierim, Reference KNIERIM2006). The egg of Heterakis gallinarum provides the most natural route of transmission for the protozoan Histomonas meleagridis, the causative organism for blackhead disease, which can cause high mortality rates within one week after the first clinical signs emerge (see http://www.organicvet.co.uk). Infections with parasites such as the roundworm Ascaridia also carry the risk that animals become more susceptible to other pathogens, as their immune system may be suppressed. Dahl et al. (Reference DAHL, PERMIN, CHRISTENSEN, BISGAARD, MUHAIRWA, PETERSEN, POULSEN and JENSEN2002) showed that combined infections of Ascaridia galli and Pasteurella multocida (causing fowl cholera) had more severe effects on the birds’ health than single infections. These findings have implications for organic systems if they do not treat against gastro-intestinal parasites.

The use of anthelminths in organic farming is restricted. Flubendazole is the only product registered for use in organic poultry in most European countries. As a consequence it is used extensively; potentially leading to residues in eggs and increased resistance in the parasite population. Managing this issue may be problematic for organic egg production (Maurer et al., Reference MAURER, AMSLER, HECKENDORN and PERLER2007). Furthermore, effective alternative methods are almost completely lacking (Maurer et al., Reference MAURER, AMSLER, HECKENDORN and PERLER2007). Flubendazole is effective against most roundworms, but less effective in controlling heavy tapeworm infections (Jacobs, Reference JACOBS2007).

In order to prevent and control endoparasite infections, preventive strategies should be adopted, including good litter hygiene and management in the house and veranda, good range management preventing puddles on pasture and maintaining, cultivation and rotation of paddocks in order to reduce the number of infectious worm eggs on the range (Gordon and Charles, Reference GORDON and CHARLES2002a; Knierim, Reference KNIERIM2006; Maurer et al., Reference MAURER, AMSLER, HECKENDORN and PERLER2007; Maurer et al., Reference MAURER, AMSLER, PERLER and HECKENDORN2009a). In the case of tapeworms that use intermediate hosts, control of the hosts is also required (Jacobs, Reference JACOBS2007). Another important measure is to rear young hens with early access to an outdoor area, so that they can build up their immunity against infections from an early age onwards (Sommer and Vasicek, Reference SOMMER and VASICEK2000). At present, management practices such as pasture rotation is the only way to prevent the building up of helminth infections in the outdoor environment (Thamsborg and Roepstorff, Reference THAMSBORG and ROEPSTORFF2003). Rotations are a required practice for all organic arable production and form an integral part of the system (Soil Association, Reference SOIL ASSOCIATION2000). In arable systems, rotations usually involve grass/clover leys and are key means of achieving pest and weed control. In poultry systems long resting periods before the reuse of any area are needed for efficient endoparasite control. Resting periods of one year (Thamsborg et al., Reference THAMSBORG, ROEPSTORFF and LARSEN1999) or even two to three years (Bassler et al., Reference BASSLER, CISZUK and SJELIN2000) have been suggested to prevent transmission between flocks. An integrated approach to achieve a better use of the run while at the same time avoiding sward destruction and deterioration, is the use of a mobile housing system within a crop rotation (Knierim, Reference KNIERIM2006). Mobile houses will also make rotation across the land area easier.

If flocks show a low level of ranging behaviour, hens will stay near the house and a high proportion of manure deposition will occur close to the house (Aarnink et al., Reference AARNINK, HOL and BEURSKENS2006). Aarnink et al. (Reference AARNINK, HOL and BEURSKENS2006) measured that 20-45% of chicken manure was deposited in the 20 m next to a hen house. This has health implications as a high worm burden near the house will increase the risk of (re)infection with worm eggs (Aarnink et al., Reference AARNINK, HOL and BEURSKENS2006; Bray and Lancaster Reference BRAY and LANCASTER1992). Encouraging hens to range, using range enhancement, will have added health benefits. Bassler et al. (Reference BASSLER, CISZUK and SJELIN2000) suggested that on permanent pasture, a dense sward can carry between 50 to 100 hens for seven days without the birds damaging the sward near to the house (stocking rate 15 hens per ha per year). However, in commercial organic systems stocking densities are much higher and therefore adoption of a rotation system (across the land area) will be necessary. Sward damage is also dependent on flock size (not just stocking density) and for larger flocks rotation is likely to be even more important. Future preventive treatments may involve the use of nematophagus fungi that can reduce populations of larval nematodes in faeces, or egg parasitic fungi that attack their eggs (Larsen, Reference LARSEN1999).

ectoparasites

The poultry red mite Dermanyssus gallinae is the most important ectoparasite of laying hens in organic as well as in conventional egg production in Europe (Häne et al., Reference HÄNE, HUBER-EICHER and FRÖHLICH2000; Guy et al., Reference GUY, KHAJAVI, HLALEL and SPARAGANO2004; Fiddes et al., Reference FIDDES, LE GRESLEY, PARSONS D.G. and COLES G.C.2005; Tauson et al., Reference TAUSON, K., HOLM and WALL2006; Maurer et al., Reference MAURER, AMSLER, HECKENDORN and PERLER2007; Sparagano et al., Reference SPARAGANO, PAVLIĆEVIĆ, MURANO, CAMARDA, SAHIBI, KILPINEN, MUL, ·VAN EMOUS, LE BOUQUIN, HOEL and CAFIERO2009). The haematophagous mite is a nocturnal feeder, and spends the day in the surrounding environment. At high population densities they can cause significant levels of distress to victim birds when they suck blood (mainly at night). They can cause severe anaemia, to the extent that birds may die due to loss of blood and infestations can also lead to reduced egg production and increased egg downgrading (Guy et al., Reference GUY, KHAJAVI, HLALEL and SPARAGANO2004; Tauson et al., Reference TAUSON, K., HOLM and WALL2006; Maurer et al., Reference MAURER, AMSLER, HECKENDORN and PERLER2007). Red mites have also been associated with the transmission of pathogens (e.g. Salmonella and E-coli; Moro et al., Reference MORO, DE LUNA, TOD, GUY, SPARAGANO and ZENNER2009). At a lower infestation level, red mites may irritate the hens to an extent that they refuse to go into the henhouse or rest on the perches, or may start feather pecking (Tauson et al., Reference TAUSON, K., HOLM and WALL2006; Maurer et al., Reference MAURER, AMSLER, HECKENDORN and PERLER2007). Among the most common routes of entry for red mites into a flock of birds are pullets, egg trays, visitors and wild birds (Tauson et al., Reference TAUSON, K., HOLM and WALL2006). Due to lack of permitted chemical treatments and partly to the build up of immunity, this parasite has become a very common threat for the bird themselves, for egg quality and for the working environment of the poultry keeper. Controlling the mite during the life of flocks is difficult. De-infestation of a building prior to repopulation should be carried out, using mite traps to monitor success. When mite infestation is at a high level, the mites will populate all areas of a hen house. Housing systems should avoid the creation of cracks and crevices where the red mite can survive even longer without the presence of a host bird (Maurer et al., Reference MAURER, AMSLER, HECKENDORN and PERLER2007; Tauson et al., Reference TAUSON, K., HOLM and WALL2006).

foot, hock and breast health

In both conventional and organic systems, broilers are kept in groups under loose-housing conditions, which puts a high demand on the environment the birds are kept in. Although organic broiler flocks are often much smaller than conventional flocks (Tuyttens et al., 2007), safeguarding bird welfare in organic flocks of 500-1500 birds will require equally good stockmanship as that found in large (conventional) flocks.

Leg, foot and hock health are seen as important measures of welfare for broilers (Berg, Reference BERG2004; Haslam and Kestin, Reference HASLAM and KESTIN2003, Haslam et al., Reference HASLAM, KNOWLES, BROWN, WILKINS, KESTIN, WARRISS and NICOL2007). Haslam and Kestin (Reference HASLAM and KESTIN2003) used expert opinion to assess the relative importance of various welfare measures for broiler welfare in UK husbandry systems. The experts were asked to assess six measures relevant to bird welfare (based on the literature relevant to broiler welfare) and that were considered practical to record during an audit. The experts’ combined opinion was analysed using conjoint analysis to reveal the weighting factors of welfare measures selected. There was a good level of agreement in the ranking of welfare measures, in decreasing order of importance - mortality; level of leg weakness; level of hock burn; stocking density; enrichment provision and emergency provisions. Hock burn, breast burn (or breast blisters) and foot pad dermatitis (or pododermatitis) are ulcerative conditions of the skin, more generically called contact dermatitis (Haslam et al., Reference HASLAM, KNOWLES, BROWN, WILKINS, KESTIN, WARRISS and NICOL2007). The conditions involve lesions including hyperkeratosis, necrosis, ulcerations and inflammations (Berg, Reference BERG2004). Foot pad dermatitis manifests itself on the ventral footpads, hock burn on the hocks (for description of conditions and references see Berg, Reference BERG2004). Contact dermatitis can also appear on the breast, as so-called breast blisters. A report by the EC Scientific Committee on Animal Health and Animal Welfare (Reference EC SCIENTIFIC COMMITTEE ON ANIMAL HEALTH and ANIMAL WELFARE2000) concluded that contact dermatitis was a widespread problem in European boiler production and that management practices are likely to be the most important factor in prevention.

Another major source of welfare problems in broilers are leg disorders (such as lameness). Leg problems have been associated with metabolic disorders leading to skeletal abnormalities (problems in the intertarsal joints, the hips and the knees), high live weights and rapid growth rates (Kestin et al., Reference KESTIN, GORDON, SU and SØRENSEN2001; Sanotra et al., Reference SANOTRA, BERG and LUND2003). FAWC concluded in 1992 that the level of leg problems in the UK broiler industry was unacceptably high (FAWC, 1992). Both contact dermatitis and leg disorders are caused principally as side effects of a one-sided selection for growth and feed utilization in chickens kept for meat production (EC report, 2000).

Foot pad dermatitis is caused by a combination of wet litter and unspecified chemical factors in the litter (Berg, Reference BERG2004). Several risk factors for contact dermatitis have been identified (see overviews in: Berg, Reference BERG2004; Haslam et al., Reference HASLAM, BROWN, WILKINS, KESTIN, WARRISS and NICOL2006; Pagazaurtundua and Warriss, Reference PAGAZAURTUNDUA and WARRISS2006b; Haslam et al., Reference HASLAM, KNOWLES, BROWN, WILKINS, KESTIN, WARRISS and NICOL2007). Most of these factors affect litter quality directly or indirectly, e.g. litter depth, type and quality; floor type; water drinker design; bird age; feed composition (including fat and protein quality and levels, salt content) micronutrient deficiencies (such as biotin), house climate (temperature and relative humidity, affected by heating and ventilation system and thermal quality of wall and ceiling materials), outdoor climate, lighting programmes, health of flock, hybrids, and stocking density. More recent studies have found that the relationship between stocking density and foot burn, hock burn and breast burn is less direct than initially thought (Dawkins et al., Reference DAWKINS, DONNELLY and JONES2004; Haslam et al., Reference HASLAM, BROWN, WILKINS, KESTIN, WARRISS and NICOL2006; Haslam et al., Reference HASLAM, KNOWLES, BROWN, WILKINS, KESTIN, WARRISS and NICOL2007). These studies have shown that the housing environment has potentially more impact on broiler welfare than stocking density per se. The prevention of contact dermatitis should focus on improvement of litter quality. This will have beneficial effects in several ways, not only by decreasing the prevalence of contact dermatitis but also improving environmental quality. Reduced ammonia emissions, improved air quality and improved hygiene lead to decreased risks of disease outbreaks and to a general improvement in bird cleanliness (Berg, Reference BERG2004).