Introduction
Commercial egg production in industrial systems began to expand develop rapidly in the USA after World War II, and soon after in Western Europe. Its main characteristics include confinement facilities, artificial lighting and ventilation, a large number of highly productive hybrid laying hens kept mostly in battery cages that provide a limited amount of space, use of complete feeds (that may contain antibiotics, stimulants, hormones, artificial colourants, etc.), use of many farm hygiene and maintenance products. This type of production provides a ready supply of eggs for consumers throughout the year in large amounts and at a relatively low price (Pavlovski et al., Reference PAVLOVSKI, ŠKRBIĆ, LUKIĆ, KRNJAJA, BIJELIĆ and TRENKOVSKI2010), due to which the battery farming system has become the most common table egg production system in the world (Matt et al., Reference MATT, REMBIALKOWSKA, LUIK, PEETSMANN and PEHME2011).
However, over the last few decades, new laying hen rearing systems have been rapidly introduced into poultry production in an effort to harmonise poultry health and welfare with consumer, producer, industry and environmental demands (Matković et al., Reference MATKOVIĆ, VUČEMILO and MATKOVIĆ2007). Most producers in the USA list soil fertility improvement and safe food production among major benefits from this type of production (Hilmire, Reference HILMIRE2012).
Henry (Reference HENRY2002) reported the most common alternative laying hen rearing systems as being free run, free range, pastured, organic and omega 3 supplemented hens. Most of these rearing systems involve free range hens, providing birds with a natural environment, fresh air, inorganic grit (pebbles) and organic (plant and animal-based) feed from the range which can satisfy up to 20% of their daily nutritional requirements (Henry, Reference HENRY2002; Oberholtzer et al., Reference OBERHOLTZER, GREENE and LOPEZ2006). Moreover, birds are exposed to the effect of environmental climatic factors as well as to the threat of parasitic and predator attacks.
Certain countries already obtain a significant percentage of eggs from alternative rearing systems. For instance, in Switzerland, as much as 80% of laying hen flocks have access to free range (Matković et al., Reference MATKOVIĆ, VUČEMILO and MATKOVIĆ2007). Organic egg sales in the USA have had annual growth rates of 20% since the 1990s, suggesting that the organic egg market is the fastest growing part of the organic agriculture sector (Oberholtzer et al., Reference OBERHOLTZER, GREENE and LOPEZ2006). Among European countries, Italy has the largest market for organic products, followed by Spain (Mesias et al., Reference MESIAS, MARTINEZ-CARRASCO, JOSE MARTINES and GASPAR2011).
Free range systems may involve the use of hybrids or indigenous breeds adapted to existing environmental conditions (these breeds can also serve as a powerful marketing tool). The type of genotype used often depends on the colour of eggs laid. White Leghorns are among the most popular and productive layers of white eggs, whereas Rhode Island Reds are the second most popular, and produce large brown eggs in the USA (Burbaugh et al., Reference BURBAUGH, TORO and GERNAT2010). Hilmire (Reference HILMIRE2012) stated that Plymouth Rocks and Ameraucanas breeds are mainly used for the production of brown-shelled eggs. Problems typically associated with the use of commercial hybrids bred for production under strictly controlled conditions in a free range system include weak legs, excessive rates of heart attacks, a high incidence of congestive heart failure (ascites), poor foraging ability and poor heat tolerance, and so producers are often discouraged from rearing these hybrids in alternative production systems (Fanatico et al., Reference FANATICO, POLSON and BORN2005).
Egg production
Egg production is the most important production trait of laying hens, denoting the number of eggs laid per year expressed as a percentage. A large number of researchers have observed this trait across different rearing systems. Anderson (Reference ANDERSON2010) compared Hy-Line Brown layers, and obtained a statistically significant difference in egg production between caged and free-range layers (81.9% and 77.7%, respectively). Castellini et al. (Reference CASTELLINI, PERELLA, MUGNAI and DAL BOSCO2006) compared White Leghorn birds reared under caged, organic and organic plus systems. Organic birds showed a lower egg production rate than the control (organic 63.4%, organic plus 61.4%; control 74.1%) probably due to the more intense motor activity and to the concomitant lower energy and protein ingestion which was diluted by grass intake - mainly in the organic-plus group. Furthermore, compared to the control, the laying rate of organic birds was more affected by seasonal conditions (temperature and photoperiod). A similar experiment, using Ancona laying hens, was carried out by Mugnai et al. (Reference MUGNAI, DAL BOSCO and CASTELLINI2009) who produced similar results (laying rate: organic 60.6%, organic plus 59.6%; control 70.9%). Differences in productive performance between caged system (80.82%) and free range system (72.88%) were reported by Senčić and Butko (Reference BUTKO2006) in Lohmann Brown hens, as well as by Yakubu et al. (Reference YAKUBU, SALEKO and IGE2007) who reported the superiority of Bovans Brown and Lohmann Brown birds in cages (74%) to those on deep litter (69%) in terms of laying performance. Similar results were published by Suto et al. (Reference SUTO, HORN and UJVARI1997) and Flock et al. (Reference FLOCK, LAUGHLIN and BENTLEY2005).
A study by Ferrante et al. (Reference FERRANTE, LOLLI, VEZZOLI and CAVALCHINI2009) showed no difference in laying rate between Hy-Line Brown birds reared under organic and barn systems. Peak laying was reached at 25 weeks, and was higher in organic hens than in barn housed hens (94.5% vs. 93%), whereas from 25 to 58 weeks, the laying rate was higher in barn hens, with the final result, however, being identical (86.40% vs. 86.35%). These findings are different from those of Tauson and Holm (Reference TAUSON and HOLM2001), who found 3% lower egg mass in barn hens compared to caged hens. This difference may be due to the high level of management in the two farms of this study. Barbosa Filho et al. (Reference BARBOSA FILHO, SILVA, SILVA and COELHO2005) found no difference in the laying performance of Hy-Line W36 and Hy-Line Brown hens reared under litter and cage systems. Similarly, Basmacioglu and Ergul (Reference BASMACIOGLU and ERGUL2005) reported no difference in Babcock-300 and Isa Brown housed in either floor pens or cage systems.
Apart from rearing systems, egg production is significantly affected by layer genotype, as confirmed by Rizzi and Chiericato (Reference RIZZI and CHIERICATO2005) who compared two hybrid strains (Hy-Line Brown - HLB, Hy-Line White - HLW) and two Italian indigenous breeds (Robusta maculata - RM and Ermellinata of Rovigo - ER) under organic farming conditions. At 32 weeks, the performance of HLB and HLW was 94.1% and 88.7%, whereas that of RM and ER was 63% and 56.8%, respectively, which confirmed the role of genotype in egg production. Kucukyilmaz et al. (Reference KUCUKYILMAZ, BOZKURT, HERKEN, CINAR, CATH, BINTAS and COVEN2012) compared performance between two hybrids - Lohmann LSL and ATAK-S - reared under conventional cage or organic rearing systems. White Lohmann LSL layers yielded more eggs in the cage facility (89.8%) than in the organic system (87.2%), in contrast to the brown ATAK-S laying hens which exhibited lower laying performance in the conventional system (80.4%) than in the organic system (82.5%). These results suggest that some genotypes will show better performance under conventional cage rearing systems, whereas some other genotypes will respond positively when allowed fresh air and freedom of movement.
Hegelund et al. (Reference HEGELUND, SORENSEN and HERMANSEN2006) compared 18 organic farms in Denmark using five different genotypes (Isa Brown (six flocks), Isa Babcock (four flocks), Hy-Line Brown (five flocks), Lohmann Brown (two flocks) and Hellevad White (one flock)), and determined an average performance of 70.4% with, however, marked variations across certain farms (maximum performance: 90.7%, minimum performance: 53.4%). The laying performance of organic birds can be improved by the use of synthetic methionine in organic poultry feed. Its potential inclusion in the list of permissible dietary supplements for organic poultry is being discussed in the USA, but not in Europe (Koreleski and Świątkiewicz, Reference KORELESKI and ŚWIATKIEWICZ2009).
Mortality
When analysing mortality, overall conditions in both penned chickens and free range environments must be considered, since many circumstances and unfavourable conditions can cause bird death (Bogosavljević-Bošković et al., Reference BOGOSAVLJEVIĆ-BOŠKOVIĆ, RAKONJAC, DOSKOVIĆ and PETROVIĆ2012). Under free range systems, the system is a problem in itself. In that respect, Sossidou et al. (Reference SOSSIDOU, DAL BOSCO, ELSON and FONTES2011) showed increased mortality in these production systems due to a broad range of diseases and parasitic infestations due to exposure to outdoor conditions, and identified predation as a specific problem. Newcastle Disease is believed to be one of the most important diseases in free-range systems. During outbreaks of the disease, up to 80% of the population may die (Permin and Pedersen, Reference PERMIN and PEDERSEN2001). Some of the main reasons for moving poultry into indoor, controlled facilities include disease, parasites and predator attacks (Fanatico, Reference FANATICO2000).
Under all rearing systems, birds can develop undesirable behaviour such as feather pecking and cannibalism, which are major causal agents of mortality in laying hens (Rakonjac et al., Reference RAKONJAC, BOGOSAVLJEVIĆ-BOŠKOVIĆ, DOSKOVIĆ and PETROVIĆ2013). Blokhuis et al. (Reference BLOKHUIS, FIKS VAN NIEKERK, BESSEI, ELSON, GUEMENE, KJAER, LEVIRNO, NIKOL, TAUSON, WEEKS and VAN DE WEERD2007) investigated different layer rearing systems and found one-third of all mortality was caused by feather pecking and cannibalism, whereas Weitzenburger et al. (Reference WEITZENBURGER, VITS, HAMANN and DISTEL2005) reported that cannibalism accounted for as much as 65.5% of mortality in laying hens housed in a variety of furnished cages. Sparks et al. (Reference SPARKS, CONROY and SANIDILANDS2008) surveyed British certified organic pullet producers and found annual mortality to range from <2% to > 7%. Causes of mortality included smothering, non-specific diseases, unknown causes and predation, with smothering and cannibalism accounting for the highest and lowest percentage (25% and 6.2%) of all mortality, respectively. In Sweden, Fossum et al. (Reference FOSSUM, JANSSON, ETTERLIN and VAGSHOLM2009) showed a significantly higher occurrence of bacterial and parasitic diseases and cannibalism in laying hens kept in litter-based housing systems and free-range systems compared to hens kept in cages. Oden et al. (Reference ODEN, KEELING and ALEGERS2002) found that rearing white-feathered genotypes can lead to reduced layer mortality due to their lower susceptibility to feather pecking and cannibalism as primary causes of mortality. However, Van de Weerd et al. (Reference VAN DE WEERD, KEATINGE and RODERICK2009) recommended rather the contrary - advocating breeding non-white genotypes for free range systems in order to be less conspicuous to predators as one of major causative agents of layer mortality. The most common predators listed by Henry (Reference HENRY2002) include eagles, raccoons and foxes.
Mostert et al. (Reference MOSTERT, BOWES and VAN DEN VALT1995) found considerably higher mortality in birds reared on floor and free range systems than in caged hens. Anderson (Reference ANDERSON2010) reported higher mortality of Hy-Line layers in free range flocks (28.4%) compared to conventional systems (8.9%). Senčić and Butko (Reference BUTKO2006) reported that Lohmann Brown layers had higher mortality under free range systems (6.8%) than in cages (5.5%).
In contrast, the lower mortality in free range systems compared to closed systems, as reported by some researchers, was due to higher comfort and bird resistance attained through the daily availability of sunlight and fresh air. Ferrante et al. (Reference FERRANTE, LOLLI, VEZZOLI and CAVALCHINI2009) reported considerably lower mortality in Hy-Line hybrids reared under a free range system (2.43%) than under barn conditions (4.24%). Mugnai et al. (Reference MUGNAI, DAL BOSCO and CASTELLINI2009) observed lower mortality in Ancona laying hens reared under organic (2.4%) and organic plus systems (1.8%) than in conventional, intensive systems (4.15%). Mortality is most affected by farming conditions, as confirmed by Hegelund et al. (Reference HEGELUND, SORENSEN and HERMANSEN2006), who studied 18 different organic farms with an average mortality rate of 22.5%, ranging from 8.6% to up to 62.3%. The majority of mortality cases were caused by Pasturella spp. and predator attacks.
Yakubu et al. (Reference YAKUBU, SALEKO and IGE2007) reported a lower weekly mortality rate for caged Bovans Brown and Lohmann Brown layers (0.68%) than for hens on deep litter (1.1%). In a 40-week experiment, conducted by Wężyk et al. (Reference WĘŻYK, KRAWCZYK, CALIK and POŁTOWICZ2006), the overall mortality rate was considerably higher for HyLine White (14%) and HyLine Brown (35%) layers reared on litter, compared to the birds kept in cages, whereby mortality of both hybrids was under 6%. Most cases of mortality were due to feather pecking and cannibalism.
Egg weight
Egg weight is primarily affected by layer genotype (Holt et al., Reference HOLT, DAVIES, DEWULF, GAST, HUWE, JONES, WALTMAN and WILLIIAN2011). Moreover, laying performance is an important factor contributing to egg weight. Castellini et al. (Reference CASTELLINI, PERELLA, MUGNAI and DAL BOSCO2006) found that the total egg weight was negatively correlated with egg production rate. The more productive birds, independent of group and season, produced lighter eggs. Other important factors include layer age (Rizzi and Chiericato, Reference RIZZI and CHIERICATO2005; Rizzi and Cassandro, Reference RIZZI and CASSANDRO2009; Akyrek and Okur, Reference AKYREK and OKUR2009; Škrbić et al., Reference ŠKRBIĆ, PAVLOVSKI, LUKIĆ, VITOROVIĆ, PETRIČEVIĆ and STOJANOVIĆ2011), feed energy and nutritive value, particularly the dietary content of essential amino acids and protein level (Elwinger et al., Reference ELWINGER, TUFVESSON and HARTMAN2002; Krawczyk, Reference KRAWCZYK2009).
Eggs from free-range production systems have been shown to weigh more on average than those from battery and conventional cages (Hughes et al., Reference HUGHES, DUN and McCORQUODALE1985; Hidalgo et al., Reference HIDALGO, ROSSI, CLERICI and RATTI2008). Hughes et al. (Reference HUGHES, DUN and McCORQUODALE1985) reported that the differences in egg weight could be due to differences in environmental temperature between the free-range and caged systems. Plochberger (Reference PLOCHBERGER1989) found differences in egg weight between organic and conventional birds of the same genotype, with organic eggs weighing more (55.1g vs. 51.9g). Krawczyk (Reference KRAWCZYK2009) compared three production systems: organic, backyard (small flocks of 30-100 birds fed mainly cereals and ground grains) and conventional, using a Greenleg partridge indigenous Polish breed. Egg weight was affected by production system, and was highest in organic system (57.3g), somewhat lower in conventional system (56.5g) and lowest in backyard system (54.1g). Likewise, Senčić and Butko (Reference BUTKO2006) obtained greater egg weights from Lohmann Brown hens in a free range system (62.40g) than from caged birds (60.50g). Even in retail eggs from unknown genotypes, Hidalgo et al. (Reference HIDALGO, ROSSI, CLERICI and RATTI2008) determined greater egg weight in eggs from alternative systems (cage:free range:barn:organic = 63.4g:66.7g:62.1g:64.9g). These results comply with the findings of authors who showed that access to free range leads to increased egg weight (Mostert et al., Reference MOSTERT, BOWES and VAN DEN VALT1995; Van Den Brand et al., Reference VAN DEN BRAND, PARMENTIER and KEMP2004; Rossi, Reference ROSSI2007).
In contrast, some authors found that average egg weight was lower in birds reared under free range systems. Krawczyk (Reference KRAWCZYK2009) attributed this finding to situations when birds cannot satisfy their protein requirements on the range. Ferrante et al. (Reference FERRANTE, LOLLI, VEZZOLI and CAVALCHINI2009) found Hy-Line Brown layers to have greater weight in barn eggs (65.49g) than in organic eggs (63.44g). Minelli et al. (Reference MINELLI, SIRRI, FOLEGATTI, MELUZZI and FRANCHINI2007) obtained statistically significant differences between eggs from caged hens (66.2g) and organic hens (64.4g) of the same hybrid. Also, Đukić-Stojčić et al. (Reference ĐUKIĆ-STOJČIĆ, PERIĆ, BJEDOV and MILOŠEVIĆ2009) reported greater egg weight in ISA Brown hybrids under caged system (66.74g) compared to hens from floor systems with free range (65.25g), and free range (64.75g). Similar results were obtained by Sekeroglu et al. (Reference SEKEROGLU, SARICA, DEMIR, ULUTAS, TILKI and SAATCI2008). Samman et al. (Reference SAMMAN, KUNG, CARTER, FOSTER, AHMAD, PHUYAL and PETOCZ2009) used eggs purchased from supermarkets, and showed greater weight of conventional eggs (61.70g) than that of organic (59.62g) and omega-3 eggs (54.92g). However, these results must be treated with caution, since hen genotypes used in the study were not identified; therefore, these differences might be due to the use of different genotypes in different rearing systems.
Pištekova et al. (Reference PIŠTEKOVA, HOVORKA, VEČEREK, STRAKOVA and SUCHY2006) found that ISA Brown layers had greater egg weights when kept on floor systems (62.02g) compared to cage systems (60.63g). Similar results for the same hybrid were published by Englmaierova and Tumova (Reference ENGLMAIEROVA and TUMOVA2009), who reported greater egg weight in birds reared on litter (64.5g) than in caged layers (63.3g). In contrast to these results, Yakubu et al. (Reference YAKUBU, SALEKO and IGE2007) determined significantly greater egg weight in Bovans Brown and Lohmann Brown hens reared under cage systems (53.4g) than on deep litter (52.7g), as did Suto et al. (Reference SUTO, HORN and UJVARI1997).
These examples clearly show that rearing system in itself does not necessarily have a crucial impact on egg weight; rather, the effect of diet is of much greater significance (Minelli et al., Reference MINELLI, SIRRI, FOLEGATTI, MELUZZI and FRANCHINI2007). This has also been confirmed by the results of some authors, who found no significant differences in egg weight under different rearing systems. No differences were observed by Basmacioglu and Ergul (Reference BASMACIOGLU and ERGUL2005) in Babcock-300 and Isa Brown layers between cage and floor pen systems or by Rizzi et al. (Reference RIZZI, SIMIOLI, MARTELLI, PAGANELLI and SARDI2006) using Isa Brown hens in conventional cages and free range systems. Similar findings were reported by Wężyk et al. (Reference WĘŻYK, KRAWCZYK, CALIK and POŁTOWICZ2006) in Hy Line Brown and Hy Line White between litter and cage rearing systems and Zemkova et al. (Reference ZEMKOVA, SIMEONOVA, LICHOVNIKOVA and SOMERLIKOVA2007) in ISA Brown birds reared in conventional cages, enriched cages, litter and outdoor systems. Mugnai et al. (Reference MUGNAI, DAL BOSCO and CASTELLINI2009) reported the same findings in Ancona laying hens in conventional, organic or organic plus systems as well as Anderson (Reference ANDERSON2010) using Hy-Line Brown hens in cage and free range systems and Kucukyilmaz et al. (Reference KUCUKYILMAZ, BOZKURT, HERKEN, CINAR, CATH, BINTAS and COVEN2012) studying Lohmann LSL and ATAK-S in cage and organic rearing systems. Nevertheless, Anderson (Reference ANDERSON2010) observed that caged hens produced a significantly greater numbers of Grade A eggs (90.0% vs. 85.9%), while free-range hens produced a significantly greater numbers of Grade B eggs (5.9% vs. 11.5%).
Egg composition
Different rearing systems may induce certain variations in main egg components; the yolk, albumen and shell. Hidalgo et al. (Reference HIDALGO, ROSSI, CLERICI and RATTI2008) compared eggs purchased from supermarkets originating from different rearing systems (cage, free range, barn, and organic systems) and found significant differences in shell percentage (11.0%:10.2%:10.8%:10.2%, respectively), with a small difference in albumen percentage (64.2%:65.4%:63.9%:65.3%), and no difference in yolk percentage. Pištekova et al. (Reference PIŠTEKOVA, HOVORKA, VEČEREK, STRAKOVA and SUCHY2006) reported small differences in the percentage of both albumen and shell in ISA Brown layers reared in cage or deep litter systems, with no differences in egg yolk. Kouba (Reference KOUBA2003) obtained a higher proportion of yolk from organic eggs (35%) compared to conventional eggs (33.8%), and a lower albumen percentage (54.6% vs. 55.7% respectively). These differences were statistically confirmed, whereas the shell percentage was identical in both production systems at 10.4%. Kucukyilmaz et al. (Reference KUCUKYILMAZ, BOZKURT, HERKEN, CINAR, CATH, BINTAS and COVEN2012) found a higher proportion of yolk (27.29%) and shell (10.58%) in LSL Lohmann organic eggs compared to those from caged birds (26.73% and 10.36% respectively), whereas the albumen percentage was lower in organic eggs (62.56%) than in conventional eggs (63.39%). The same experiment showed no significant differences in the proportions of main egg parts between organic and caged ATAK-S laying hens.
In an experiment on Babock-300 and ISA brown layers, Basmacioglu and Ergul (Reference BASMACIOGLU and ERGUL2005) determined a significantly higher average yolk percentage in caged birds (25.08%) than in floor pen layers (24.16%), whereas the caged birds had a lower proportion of albumen 65.07% vs. 65.91% and shell 9.89% vs. 9.94%. The lower yolk proportion may be due to a deficiency of some nutrients, primarily methionine (Shafer et al., Reference SHAFER, CAREY and PROCHASKA1996). This can often be observed in organic eggs, given the fact that methionine is the first limiting amino acid in organic diets for laying hens (Hancock et al., Reference HANCOCK, WELLER and McCALMAN2003; Zollitsch et al., Reference ZOLLITSCH, KRISTIANSEN, KRUTYINNA, MACNAEIHDE and YOUNIE2004). Elwinger et al. (Reference ELWINGER, TUFVESSON and HARTMAN2002) found the same effects due to dietary deficiencies when feeding low methionine organic diets.
Cherian et al. (Reference CHERIAN, HOLSONBAKE and GOEGER2002) observed differences in egg components in an analysis of six types of eggs: animal fat-free-high n-3 (SP1), free range organic brown eggs (SP2), uncaged- non-medicated brown eggs (SP3), vegetarian diet cage-free brown eggs, (SP4) or cage-free naturally nested no steroids no stimulants (SP5). Regular white-shelled eggs were used as the control. The results for yolk percentage were: control 30.2%; SP1 29.7%:SP2 25.9%; SP3 33.4%; SP4 25.6%; SP5 29.8%, albumen control 59.6%; SP1 59.4%; SP2: 63.7%; SP3 56.3%; SP4 64.5%; SP5 60.7% and shell control 10.1%; SP1 10.8%; SP2 10.3%; SP3 10.2%; SP4 9.9%; SP5 9.5%.
In contrast, Rizzi et al. (Reference RIZZI, SIMIOLI, MARTELLI, PAGANELLI and SARDI2006), Senčić and Butko (Reference BUTKO2006) and Krawczyk (Reference KRAWCZYK2009) found no significant differences in the proportion of egg components in hens reared with and without outdoor access. Naturally, this trait can be significantly affected by other factors, primarily layer age, as confirmed by Rizzi and Chiericato (Reference RIZZI and CHIERICATO2005) who studied four genotypes: Hy-Line Brown (HLB), Hy-Line White (HLW), Robusta maculata (RM) and Ermellinata of Rovigo (ER) under organic systems, and found that, from 30 to 42 weeks of laying, the percentage of egg yolk significantly increased while albumen decreased. Layer age had an impact on the percentage of shell only in HLB and ER genotypes.
Haugh units
The Haugh unit is an objective measure of egg quality based on the logarithmic function of albumen height and egg weight. Many factors are reported to affect Haugh Units: storage time and temperature, hen age, breed, nutrition (dietary protein and amino acid content e.g. lysine, methionine, feed enzymes, grain type/protein source), disease (IB), supplements (ascorbic acid, vitamin E), artificial exposure to ammonia, induced moult and medication (Roberts, Reference ROBERTS2004). This clearly shows that, depending on rearing systems, these factors can have a significant effect on the content of Haugh units in an egg; therefore, contradictory results on this topic are often reported. Castellini et al. (Reference CASTELLINI, PERELLA, MUGNAI and DAL BOSCO2006) conducted an experiment with White Leghorn laying hens in cages, organic and organic plus systems, and found that the Haugh unit was always higher in the organic plus eggs, which was superior to the other two groups during the final productive phase, probably due to less stress in the oviduct tract of the organic plus hens. The same production systems in Ancona laying hens were compared by Mugnai et al. (Reference MUGNAI, DAL BOSCO and CASTELLINI2009) who reported higher Haugh unit values in eggs from hens raised under organic plus systems (92.4) than in organic (87.7) and conventional systems (86.6), but only during the autumn productive period, which was due to the higher vitamin C content in the eggs. Đukić-Stojčić et al. (Reference ĐUKIĆ-STOJČIĆ, PERIĆ, BJEDOV and MILOŠEVIĆ2009) compared the effect of cages and floor systems with range access, and free range systems on ISA Brown hens, and observed that free range birds had higher Haugh units (91.25) compared to birds on the floor system with range access (89.36) and caged hens (87.08). Similar conclusions were drawn by Minelli et al. (Reference MINELLI, SIRRI, FOLEGATTI, MELUZZI and FRANCHINI2007) who measured considerably higher Haugh unit values of eggs from Hy-Line Brown hens in organic systems (78.6) compared to those in cages (70.9). In an experiment with Greenleg partridge chickens under organic, backyard and conventional systems, Krawczyk (Reference KRAWCZYK2009) obtained Haugh unit ratios of 65.9, 80.0 and 74.2 respectively, thereby corroborating the results of similar studies by Kosmidou et al. (Reference KOSMIDOU, FORTOMARIS, SOSSIDOU and YANNAKOPOULOS2007) and Sekeroglu et al. (Reference SEKEROGLU, SARICA, DEMIR, ULUTAS, TILKI and SAATCI2008). Meanwhile, Rossi (Reference ROSSI2007) obtained lower Haugh units for the eggs from hens kept under organic production systems compared to caged layers. Similar results were reported by Hidalgo et al. (Reference HIDALGO, ROSSI, CLERICI and RATTI2008) who obtained the highest Haugh unit score in eggs from cages (69.2), and those from litter (67.6), whereas free range (66.2) and organic eggs (61.0) had lower numbers. Rizzi et al. (Reference RIZZI, SIMIOLI, MARTELLI, PAGANELLI and SARDI2006) found higher Haugh units in Isa Brown birds kept in cages than in free range hens. Conversely, Mostert et al. (Reference MOSTERT, BOWES and VAN DEN VALT1995) found no difference in Haugh units between cage, floor and free range reared birds, nor did Barbosa Filho et al. (Reference BARBOSA FILHO, SILVA, SILVA and COELHO2005), Wężyk et al. (Reference WĘŻYK, KRAWCZYK, CALIK and POŁTOWICZ2006), Englmaierova and Tumova (Reference ENGLMAIEROVA and TUMOVA2009), and Kucukyilmaz et al. (Reference KUCUKYILMAZ, BOZKURT, HERKEN, CINAR, CATH, BINTAS and COVEN2012).
Yolk colour and carotenoids
Carotenoids are natural pigments in hen egg yolks. They confer its yellow colour, which can range from very pale yellow to dark brilliant orange. Carotenoids represent less than 1% of yolk lipids, mainly composed of carotene and xanthophylls (lutein, cryptoxanthin, and zeaxanthin). The total concentration of lutein and zeaxanthin is ten times greater than that of cryptoxanthin and carotene, combined (Shenstone, Reference SHENSTONE1968). The xanthophylls lutein and zeaxanthin have attracted a lot of interest ever since it was presumed that an increased nutritional uptake of both compounds may prevent adult macula degeneration (AMD) and age-related cataract formation (Schlatterer and Breithaupt, Reference SCHLATTERER and BREITHAUPT2006). The same authors determined that egg contains between 400 and 500 µg xanthophylls. Economically, the colour is important because it is a quality criterion for consumers (Matt et al., Reference MATT, REMBIALKOWSKA, LUIK, PEETSMANN and PEHME2011). The intensity of yolk colour is usually measured using the Roche Scale. A darker colour is highly desirable by consumers in many countries, for example, in Australia, the preferred yolk colour is 11 on the Roche scale (Roberts, Reference ROBERTS2004). While comparing White Leghorn hens under organic, organic plus and conventional production systems, Castellini et al. (Reference CASTELLINI, PERELLA, MUGNAI and DAL BOSCO2006) suggested that yolk colour was positively affected by grass consumption, as the highest value Roche scale was found in eggs from organic-plus hens (10.6) compared to conventional hens (9.6). Mugnai et al. (Reference MUGNAI, DAL BOSCO and CASTELLINI2009), in a similar experiment with Ancona laying hens, obtained a higher intensity of yolk colour in organic plus eggs (11.2) than in control and organic eggs (9.7). In addition, Senčić and Butko (Reference BUTKO2006) measured 12 and 10 Roche values in free range and cage systems respectively, and Van den Brand et al. (Reference VAN DEN BRAND, PARMENTIER and KEMP2004) reported a superior 11:9.3 Roche value with free range birds. Moreover, Van Ruth et al. (Reference VAN RUTH, ALEWIJN, ROGERS, NEWTON-SMITH, TENA, BOLLEN and KOOT2011) determined significantly higher concentrations of lutein and zeaxanthin, and significantly lower relative concentrations of canthaxanthin in organic eggs in comparison with non-organic eggs. Karadas et al. (Reference KARADAS, WOOD, SURAI and SPARKS2005), Rizzi et al. (Reference RIZZI, SIMIOLI, MARTELLI, PAGANELLI and SARDI2006), Horsted et al. (Reference HORSTED, HAMMERSHOJ and HERMANSEN2006), Dvorak et al. (Reference DVORAK, SUCHY, STARKOVA and DOLEŽALOVA2010) and Anderson (Reference ANDERSON2010) showed that eggs from organically-reared (and free-range) systems have more carotenoids in the yolk. This is because of access to grass and other substances rich in carotenoid pigments. There may be quite dramatic differences between free range and conventionally raised hens in β-carotene content, as eggs from free range systems have seven times more (Long and Alterman, Reference LONG and ALTERMAN2007), or even eight times more β-carotene (http://www.motherearthnews.com/eggs.aspx). Pištekova et al. (Reference PIŠTEKOVA, HOVORKA, VEČEREK, STRAKOVA and SUCHY2006) found egg yolk colour intensity to be somewhat higher in floor-reared laying hens (6.68) than in caged hens (6.43).
Unlike the above published data, Ferrante et al. (Reference FERRANTE, LOLLI, VEZZOLI and CAVALCHINI2009), Đukić-Stojčić et al. (Reference ĐUKIĆ-STOJČIĆ, PERIĆ, BJEDOV and MILOŠEVIĆ2009) and Krawczyk (Reference KRAWCZYK2009) found no effect of rearing system on yolk colour, most likely due to the fact that the difference in feed carotene content in the rearing systems analysed was not high enough to affect yolk colour.
Layer age can have a significant effect on yolk colour, although the findings are contradictory. Rizzi and Chiericato (Reference RIZZI and CHIERICATO2005) reared four different hybrids (Hy-Line Brown, Hy-Line White, Robusta maculata and Ermellinata of Rovigo) under organic systems, and determined that yolk colour increased with age by two to three Roche units for all genotypes. However, Škrbić et al. (Reference ŠKRBIĆ, PAVLOVSKI, LUKIĆ, VITOROVIĆ, PETRIČEVIĆ and STOJANOVIĆ2011) reported that increasing age induced a decrease in yolk colour intensity in Naked Neck layers under free range system and Lohmann Brown hens under cage systems.
Conclusions
This review presents the results of many studies dealing with the effects of laying hen rearing systems on the following parameters: egg production, mortality, egg weight, proportions of main egg parts, Haugh units, yolk colour and carotenoids. The literature suggests that alternative laying hen rearing systems are an integral part of modern egg production. These systems have substantial effects on performance traits of layers, and external and internal egg quality traits. Although laying performance in alternative systems is often reduced compared to conventional layers, eggs from alternative systems have been proven in numerous studies to have better nutritional properties. Moreover, the results analysed indicate differences within rearing systems. Conflicting reports from some authors may be due to the effect of a number of other factors, such as use of different genotypes, layer age, diet formulations, storage period (from egg sampling to analysis), access to free range and quality of the range. In any case, none of the laying hen rearing systems can be regarded as superior, since each has both advantages and disadvantages. Future research should focus on different genotypes reared under certain climates and environments in search of the most suitable genotypes for a particular production region. Furthermore, organic production would benefit from future studies regarding improvements in performance and product quality. Therefore, specific importance should be given to nutrition-related issues, such as different diet formulations and quality of the outdoor range, as well as issues regarding the cost-efficiency of this production. Accordingly, optimum length of exploitation of different genotypes under this system would be a particularly interesting research topic.
Acknowledgement
This study is part of the Project No. 31033 titled ‘Sustainable Conventional and Revitalized Traditional Production of Value-Added Poultry Meat and Eggs’ funded by the Ministry of Science and Technological Development of the Republic of Serbia.
