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Soil macrofauna under laying hens’ grazed fields in two different agroecosystems in Portugal

  • Pedro R. Soares EMAIL logo , Rosa Guilherme , Antónia Conceição and Cristina Galhano
Published/Copyright: March 30, 2023
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Open Agriculture
From the journal Open Agriculture Volume 8 Issue 1

Abstract

Although chickens can improve the chemical properties of soil through the deposition of excreta, their effects on soil macrofauna are poorly known. This work assessed the effects of grazing indigenous laying hens on soil macrofauna of two agroecosystems in Portugal: an organic horticultural field and a conventional orchard. At the horticultural field, laying hens were used to control weeds and the results were compared with those of two other weed control treatments: mechanical (rototiller) and thermal (flame weeding). At the orchard, the effects of hens were compared to that of the orchard understory vegetation, as a control. Soil epigeic macrofauna was collected in both locations, and earthworms were only collected in the horticultural field. Relative to the other treatments, grazing in the horticultural field increased the density of earthworms in the medium term (ranging from 150 to 625 earthworms/m2), without harming the density and diversity of epigeic macrofauna. However, at the orchard, the grazed soils presented lower soil epigeic macrofauna diversity, as well as significantly lower density of spiders than the control (4.67 vs 8.67 individuals/sample, respectively). These results suggest that the grazing effects can be affected by several factors, including the type of agroecosystem and farm management. Further research is required to optimize grazing management in different farming systems, considering animal density and grazing duration, thus ensuring the best contributions of chickens to soil fertility.

Keywords: earthworms; insects; laying hens; soil biology; spiders; weed control

1 Introduction

Chickens are multipurpose animals that can provide additional sources of income through the production of meat and/or eggs, while providing natural services such as pest and weed control and soil fertilization [1]. The general effects of chickens on the chemical properties of soil, due to the deposition of excreta, have been reported by several authors [2,3,4,5]. However, little is understood regarding their influence on soil ecological dynamics and their effects on the biological properties of soil, such as soil macrofauna. It has been reported that in free-range systems, indigenous chickens can take advantage of several insects, worms, and larvae, due to their scavenging behavior. According to previous studies, this intake may vary between 0.99 and 12% of their total intake [6,7]. However, these results were obtained through the crop content analysis, disregarding other effects of grazing on soil organisms, such as trampling and the deposition of droppings. Clark and Gage [8] evaluated the effects of free-range chickens on the abundance of beneficial soil macroinvertebrates in a nonchemical apple orchard. According to the authors, the presence of chicken resulted in a reduction in spider (Araneae) and harvestmen (Opiliones) activity based on pitfall trap catches, but no reduction in ground beetle (Carabidae) or rove beetle (Staphylinidae) activity. Earthworms, sampled through hand-sorting, were also unaffected.

Chickens can probably contribute to improvements in soil macrofauna through the deposition of excreta, stimulating the activity of organisms. But they can also have negative effects, through ingestion and trampling. Considering the multiplicity and infinity of scenarios, which include breeds, regions, altitudes, and season variations, obtaining more knowledge in this matter may enlighten farmers to better manage their grazing chickens. Finding a balance in which the animals feed on the pasture resources, without eradicating it, and understanding the effects of these animals on the aforementioned subject are particularly important since macrofauna plays a key role in soil fertility, which is sometimes overlooked, especially in the agricultural sphere [9,10]. Soil macrofauna significantly contributes to regulating the important physical and chemical properties of soil, as well as influencing the activities of soil microorganisms, such as fungi and bacteria [11,12,13,14,15]. However, despite the relevant role these organisms play in soil fertility, and the perception that integrating chickens with crops can significantly contribute to farm sustainability, to the best of our knowledge, the effects of grazing chickens on soil macrofauna are still largely unknown, taking into account the limited amount of literature that is currently available. Thus, the main objective of this study was to evaluate the effects of grazing Portuguese indigenous laying hens on soil macrofauna abundance and diversity in two agroecosystems: an organic horticultural field and a conventional orchard.

2 Materials and methods

2.1 Study region

The research took place in the central region of Portugal, which has a Mediterranean climate temperate by the Atlantic influence. The historical annual total precipitation is 905.1 mm, with most rain falling in autumn and spring, and the historical annual average temperature is 15.5°C [5]. The assessments were made in two different locations, 0.5 km apart, both belonging to Coimbra Agriculture School (Figure 1). The soils of both locations are Eutric Fluvisols, according to the World Reference Base for Soil Resources [16], with sandy loam texture (sand: 73%; clay: 7%; and silt: 20%).

Figure 1 Geographic location of the study site (A: horticultural field and B: orchard).
Figure 1

Geographic location of the study site (A: horticultural field and B: orchard).

2.2 Description of the conducted experiments

2.2.1 Horticultural field

This experiment was carried out in a certified organic farming field focused on horticultural production. The latitude, longitude, and altitude are, respectively, 40°13′ N, 8°26′ W, and 12 m above the sea level. The soil characteristics were measured before the beginning of the experiment and were as follows: organic matter 2.0%, pH (H2O) 6.7, total N 1.2 g/kg, NH 4 + –N 21.4 mg/kg, NO 3 − –N 9.8 mg/kg, and plant available nutrients P2O5 50.0 mg/kg and K2O 171.8 mg/kg.

In this location, we compared the effects of endangered Portuguese indigenous laying hens (breeds Preta Lusitânica and Amarela) on soil epigeic macrofauna and abundance of earthworms with two other weed control treatments allowed in organic farming and usually used in the research field: mechanical (rototiller) and thermal (flame weeding). We hypothesized that the use of laying hens could be a viable alternative to other weed control treatments, causing less impact on soil epigeic macrofauna and/or earthworms (data regarding the effects on weeds are not published here). The treatments were applied between rows of horticultural crops. Four between rows of crops were studied per treatment (n = 4), 0.75 m wide and 30 m long (a total area of 22.5 m2). Each row was occupied by three organic certified crops, planted at random in each one-third of the row, namely, sweet pepper (Capsicum annuum L., var. Entinas), kale (Brassica oleracea L., var. Winterbor), and red onion (Allium cepa L., var. Red Bull). Before plantation, the soil was tilled with a hammer shredder, a disk harrow, a spading machine, and a power harrow, by this order. Crops were planted on May 6, 2020, and thereafter irrigated by a drip system. The most abundant weeds found during the experiment period are as follows: Cyperus rotundus L., Digitaria sanguinalis L. (Scop.), Amaranthus spp. L., Portulaca oleracea L., Raphanus raphanistrum L., Panicum repens L., and Oxalis pes-caprae L.

The animals grazed for 84 days (entrance on June 3, 2020; and exit on August 26, 2020), in fixed tunnels, 30 m along the between-vegetable crops rows. The animal management was made according to the European regulations for organic production, specifically Regulation (EU) 2018/848 and Commission Regulation (EC) No 889/2008. Each tunnel was occupied by five laying hens, respecting the outdoor minimum density of 4 m2 per hen. The tunnels were provided with two shelter structures, one at each end. Each shelter structure supplied a nest, 0.8 m of perch, and ad libitum water. Furthermore, each hen was fed with 80 g day−1 of certified organic compound feed.

The mechanical and thermal treatments were intermittent and intervened six and nine times, respectively, between May and August 2020, according to the growth of weeds. The last interventions of these treatments were approximately coincident with the end of the grazing chickens (difference of ca. 50 h) to allow comparisons among treatments in time.

  1. Ethical approval: The research related to animal use has complied with all the relevant national regulations and institutional policies for the care and use of animals. The experiment was approved by the Animal Welfare Board (ORBEA) of Coimbra Agriculture School, in agreement with Directive 2010/63/EU and with the Portuguese Decree Law No. 113/2013 of August 7, 2013, on the protection of animals used for scientific purposes.

2.2.2 Orchard

This experiment was carried out in a conventional farming plot focused on fruit production. The latitude, longitude, and altitude are 40°12′ N, 8°27′ W, and 20 m above the sea level, respectively. The soil characteristics were measured before the experiment and are as follows: organic matter 2.6%, pH (H2O) 6.7, total N 1.4 g/kg, NH4 +–N 64.7 mg/kg, NO3 −–N 1.8 mg/kg, and plant available nutrients P2O5 254.17 mg/kg and K2O 570.00 mg/kg.

In this location, we compared the effects of indigenous laying hens (breed Preta Lusitânica) on soil epigeic macrofauna with the orchard understory vegetation without treatments, as a control, to evaluate the positive and/or negative effects of hens on the natural density of the existing fauna. The experiment was installed on a row of persimmons (Diospyros kaki L., var. Fuyu), 35 m long. The understory of the orchard was composed of a mixture of several herbaceous species, such as Bromus rigidus Roth, Poa annua L., Lolium rigidum Gaud., Avena spp. L., Vicia sativa L., and Medicago nigra L. We randomly chose three fruit trees per treatment (n = 3), which were wire-fenced to obtain plots of 3.5 m long and 2 m wide (total area of 7 m2). Each plot of the chicken treatment was occupied by one shelter structure and two laying hens, with an animal outdoor density of 3.5 m2 per chicken. Each shelter structure provided a nest, 0.8 m of perch, ad libitum water, and certified organic compound feed.

The chicken treatment was intermittent, with two grazings, in the same fixed plots. The first grazing lasted 34 days (entrance on November 11, 2020, and exit on December 15, 2020), and the second grazing lasted 33 days (entrance on February 4, 2021, and exit on March 9, 2021). On November 20, 2020, a laying hen went missing and was replaced on November 24, 2020, by another hen of the same breed. During the experiment period, no fertilizers or plant protection products were applied in the field.

2.3 Data collection

2.3.1 Horticultural field

Soil epigeic macrofauna was sampled with pitfall traps (7 cm in diameter, with 145 mL of antifreeze solution) before and after grazing in 5 points per treatment (n = 5), randomly chosen, within rows of crops. Each sampling event took place for 7 days. The biological material was then sorted and identified to the morphospecies level.

Earthworms were sampled on November 4, 2020, in 5 points per treatment (n = 5), randomly chosen, in between rows of horticultural crops. Soil moisture and soil temperature were assessed before sampling, to confirm the existence of good living conditions for earthworms and, thus, ensure a successful collection. Soil moisture was measured at five points per treatment (n = 5), following the gravimetric method [17], and soil temperature was measured on-site at three points per sample (n = 3). Earthworms were hand-sorted and extracted according to Lavelle et al. [18], with adaptations. One soil block per point, with a volume of 20 × 20 × 30 cm3, was dug out and hand-sorted. Then, 4.44 L of 0.33% mustard flour suspension was applied into the dug-out hole [19,20]. Collected earthworms were weighed and counted within 8 h after the extraction to avoid weight loss. Individuals were classified into juveniles and adults. Adults were then classified into their ecological distribution in soil, as defined by Bouché [21].

2.3.2 Orchard

Soil epigeic macrofauna was sampled with pitfall traps (7 cm in diameter, with 145 mL of antifreeze solution) after the last grazing, in 6 points per treatment (n = 6), randomly chosen. The sampling event took place for 7 days. The biological material was then sorted and identified to the morphospecies level.

2.4 Data analysis

Results are presented as mean values (±standard deviation). In the horticultural field, data were compared by the Kruskal–Wallis test combined with Dunn’s multiple comparisons test. At the orchard, comparisons were made using the Mann–Whitney t-test for discrete variables (individuals and morphospecies per sample) and an unpaired t-test for continuous variables (exponent of Shannon index). The normality of continuous variables was tested (Shapiro–Wilk test) and data with non-normal distribution were transformed to meet assumptions of normality, through the logarithmic transformation. Statistical analysis was performed using GraphPad Prism software version 8.0.2 (GraphPad Software, Inc. San Diego, USA), with the alpha level set at 0.05.

Morphospecies diversity was quantified using Hill numbers, differing from each other in the parameter q, which controls the weight of the relative abundance of species and includes advantageous diversity indexes, such as species richness (q = 0), the exponent of Shannon entropy (q = 1), the inverse of the Simpson concentration index (q = 2), and the inverse of Berger–Parker index (q = 3). Additional consecutive Hill numbers (q = 4 and q = 5) were calculated and plotted as a continuous function of the q parameter.

3 Results

3.1 Horticultural field

3.1.1 Soil epigeic macrofauna

A total of 1,767 individuals of soil epigeic macrofauna were caught and identified into 88 different morphospecies. The dominant groups belong to four Arthropod orders, namely, spiders (Arachnidae: Araneae) and insects (Hexapoda: Coleoptera, Hymenoptera, and Diptera), representing 48.16, 20.09, 18.96, and 8.15% of the total population, respectively (Table 1). The remaining individuals, making up the other 4.64% of the population, belong to five Arthropod orders, namely, insects (Uniramia: Hemiptera, Lepidoptera, and Orthoptera), myriapods (Myriapoda: Scolopendromorpha), and crustaceans (Crustacea: Isopoda), and one Annelida order, namely, worms (Annelida: Haplotaxida).

Table 1

Density of soil epigeic macrofauna and diversity (exponent of Shannon index) of the dominant groups and all groups at the horticultural field (mean ± standard deviation)

Period regarding grazing Treatments p-value
Chicken (C) Mechanical (M) Thermal (T) C vs M C vs T M vs T
Araneae
 Individuals/sample Before 4.80 ± 2.39a 23.40 ± 41.36a 39.00 ± 24.57a >0.9999 0.0532 0.1822
After 38.20 ± 19.61a 33.00 ± 7.97a 31.80 ± 26.28a >0.9999 >0.9999 0.9627
 Morphospecies/sample Before 4.60 ± 2.07a 3.60 ± 2.41a 4.80 ± 0.84a >0.9999 >0.9999 >0.9999
After 6.80 ± 1.64a 8.20 ± 2.05a 5.60 ± 1.14a 0.7689 >0.9999 0.1209
 Exponent of Shannon Ind. Before 4.55 ± 2.00a 2.38 ± 1.09a 2.81 ± 1.07a 0.1965 0.7711 >0.9999
After 3.72 ± 1.03a 5.61 ± 1.91a 3.81 ± 0.45a 0.1980 >0.9999 0.3594
Coleoptera
 Individuals/sample Before 11.80 ± 7.12a 11.20 ± 4.82a 10.00 ± 3.00a >0.9999 >0.9999 >0.9999
After 12.80 ± 5.02a 12.60 ± 7.99a 15.75 ± 7.80a >0.9999 >0.9999 >0.9999
 Morphospecies/sample Before 2.80 ± 0.84a 3.20 ± 1.64a 2.80 ± 0.84a >0.9999 >0.9999 >0.9999
After 2.80 ± 0.84a 2.40 ± 1.14a 2.50 ± 0.58a >0.9999 0.9429 >0.9999
 Exponent of Shannon Ind. Before 2.14 ± 0.49a 1.98 ± 0.71a 2.05 ± 0.82a >0.9999 >0.9999 >0.9999
After 1.95 ± 0.32a 1.81 ± 0.85a 1.51 ± 0.33a 0.8665 0.1017 0.8665
Hymenoptera
 Individuals/sample Before 8.80 ± 5.45a 4.25 ± 2.99a 9.80 ± 6.87a 0.3554 >0.9999 0.1530
After 12.00 ± 3.94a 13.80 ± 3.42a 19.20 ± 6.06a >0.9999 0.1808 0.4686
 Morphospecies/sample Before 2.60 ± 0.55a 2.25 ± 1.50a 2.20 ± 0.45a 0.6991 >0.9999 >0.9999
After 3.80 ± 1.10a 3.60 ± 1.14a 3.00 ± 1.00a >0.9999 0.6397 >0.9999
 Exponent of Shannon Ind. Before 2.23 ± 0.41a 2.19 ± 1.40a 1.94 ± 0.63a 0.9627 >0.9999 >0.9999
After 3.16 ± 1.14a 2.81 ± 0.84a 2.36 ± 0.64a >0.9999 0.5015 >0.9999
Diptera
 Individuals/sample Before 4.25 ± 2.75a 1.33 ± 0.58a 1.33 ± 0.58a 0.4562 0.4562 >0.9999
After 8.60 ± 4.72a 6.60 ± 2.88a 10.75 ± 8.14a >0.9999 >0.9999 >0.9999
 Morphospecies/sample Before 3.25 ± 1.71a 1.33 ± 0.58a 1.33 ± 0.58a 0.4562 0.4562 >0.9999
After 4.60 ± 1.52a 3.00 ± 0.71a 4.25 ± 2.50a 0.3136 >0.9999 >0.9999
 Exponent of Shannon Ind. Before 3.09 ± 1.57a 1.33 ± 0.58a 1.33 ± 0.58a 0.4562 0.4562 >0.9999
After 4.06 ± 1.28a 2.70 ± 0.94a 3.28 ± 2.11a 0.5015 0.5015 >0.9999
All groups
 Total individuals Before 167 197 309 — — —
After 374 343 377 — — —
 Individuals/sample Before 33.40 ± 16.10a 39.40 ± 45.95a 61.80 ± 25.32a >0.9999 0.5373 0.1980
After 74.80 ± 22.24a 68.60 ± 10.06a 75.40 ± 28.64a >0.9999 >0.9999 >0.9999
 Total morphospecies Before 43 31 29 — — —
After 45 39 41 — — —
 Morphospecies/sample Before 14.60 ± 3.58a 10.00 ± 4.85a 12.40a ± 2.07 0.3465 >0.9999 >0.9999
After 20.00 ± 4.24a 18.60 ± 3.13a 16.20 ± 3.96a >0.9999 0.4339 0.8102
 Exponent of Shannon Ind. Before 10.74 ± 2.76a 5.41 ± 2.38a 6.84 ± 2.84a 0.0486* 0.3116 >0.9999
After 11.35 ± 2.62a 11.44 ± 2.78a 9.22 ± 0.95a >0.9999 0.4127 0.8665

Within each period, different small letters mean statistical differences between treatments (Kruskal–Wallis test combined with Dunn’s multiple comparisons test; p-value <0.05).

After the intervention of treatments, no significant differences were found between treatments regarding the number of individuals per sample, morphospecies richness, and the exponent of the Shannon index in any of the dominant orders, nor the set of all groups (p > 0.05; Table 1). Moreover, considering the whole diversity profiles (Hill numbers; Figure 2), the chicken treatment and the mechanical treatment have virtually identical profiles, suggesting identical diversities between these two treatments. In contrast, the thermal treatment presented values slightly lower than the other treatments in the first Hill numbers (q = 0, q = 1, and q = 2), with matching profiles thereafter, suggesting a slightly lower diversity than the other studied treatments. Figure 3 presents the diversity profiles before and after the intervention of each treatment, showing a general increase in diversity in all treatments over time, despite the performance of the treatments.

Figure 2 Diversity profiles (Hill numbers) of the different treatments after the intervention of treatments at the horticultural field.
Figure 2

Diversity profiles (Hill numbers) of the different treatments after the intervention of treatments at the horticultural field.

Figure 3 Diversity profile (Hill numbers), at the horticultural field, in the two studied periods, for the different treatments: (a) chicken treatment, (b) mechanical treatment, and (c) thermal treatment.
Figure 3

Diversity profile (Hill numbers), at the horticultural field, in the two studied periods, for the different treatments: (a) chicken treatment, (b) mechanical treatment, and (c) thermal treatment.

3.1.2 Earthworms

During the sampling event, soil moisture contents in the chicken, mechanical, and thermal treatments were 19.8, 18.5, and 16.3%, and the soil temperatures were 15.4, 15.0, and 15.1°C, respectively.

In general, almost all the collected earthworms were juveniles (98%). Very few adult individuals were found, and none of them belong to the ecological category of epigeic earthworms. In the chicken treatment, five adults/m2 of endogeic species were found (biomass of 4.9 g/m2). In the mechanical treatment, five adults/m2 of anecic species were found (biomass of 3.8 g/m2). No adults were found in the thermal treatment.

Regarding biomass, the results in the chicken treatment varied between 84.0 and 367.9 g/m2, with a mean value of 183.5 g/m2. Although the ranges of variation in the mechanical treatment (between 6.8 and 135.8 g/m2) and the thermal treatment (between 12.1 and 163.3 g/m2) were lower than those found in the treatment with chickens, no statistical differences were found between treatments concerning this parameter (p > 0.05; Figure 4).

Figure 4 Earthworms’ density (individuals/m2) and biomass (g/m2), for each treatment, at the horticultural field (mean ± standard deviation). Different small letters mean statistical differences between treatments (Kruskal–Wallis test combined with Dunn’s multiple comparisons test; p-value < 0.05).
Figure 4

Earthworms’ density (individuals/m2) and biomass (g/m2), for each treatment, at the horticultural field (mean ± standard deviation). Different small letters mean statistical differences between treatments (Kruskal–Wallis test combined with Dunn’s multiple comparisons test; p-value < 0.05).

However, the density of earthworms was significantly higher in the treatment with chickens (p < 0.05; Figure 4), compared to the other treatments. The population of earthworms in this treatment ranged from 150 to 625 earthworms/m2, with a mean value of 320 earthworms/m2, while in both other treatments, it did not exceed 175 earthworms/m2 with a minimum density of 25 earthworms/m2.

3.2 Orchard

3.2.1 Soil epigeic macrofauna

A total of 275 individuals of soil epigeic macrofauna were caught and identified into 50 different morphospecies. The dominant groups belong to five Arthropod orders, namely, spiders (Arachnidae: Araneae), insects (Hexapoda: Hymenoptera, Coleoptera), crustaceans (Crustacea: Isopoda), and millipedes (Diplopoda: Julida), representing 29.09, 32.73, 9.09, 10.91 and 9.09% of the total population, respectively (Table 2). The remaining individuals, making up the other 9.09% of the population, belong to five Arthropod orders, namely, insects (Hexapoda: Diptera; Uniramia: Hemiptera and Orthoptera), millipedes (Diplopoda: Polydesmida), myriapods (Myriapoda: Scolopendromorpha), and one Mollusca order, namely, terrestrial mollusks (Gastropoda: Pulmonata).

Table 2

Density of soil epigeic macrofauna and diversity (exponent of Shannon index) of the dominant groups and all groups, after grazing, at the orchard (mean ± standard deviation)

Treatments p-value
Control Chicken
Hymenoptera
 Individuals/sample 8.83 ± 9.66a 6.17 ± 3.66a 0.9675
 Morphospecies/sample 2.33 ± 1.21a 1.67 ± 1.03a 0.4372
 Exponent of Shannon Ind. 2.07 ± 0.93a 1.39 ± 0.62a 0.1977
Araneae
 Individuals/sample 8.67 ± 3.27a 4.67 ± 2.42b 0.0325*
 Morphospecies/sample 4.67 ± 1.51a 2.83 ± 1.72a 0.1190
 Exponent of Shannon Ind. 4.39 ± 1.49a 2.58 ± 1.46a 0.0592
Isopoda
 Individuals/sample 3.17 ± 2.14a 1.83 ± 1.17a 0.2965
 Morphospecies/sample 1.00 ± 0.63a 1.00 ± 0.63a >0.9999
 Exponent of Shannon Ind. 0.93 ± 0.51a 1.00 ± 0.63a 0.7772
Coleoptera
 Individuals/sample 1.83 ± 1.41a 2.33 ± 1.26a 0.6667
 Morphospecies/sample 1.50 ± 1.52a 2.00 ± 1.10a 0.5628
 Exponent of Shannon Ind. 1.48 ± 1.51a 1.98 ± 1.10a 0.5264
Julida
 Individuals/sample 1.67 ± 2.25a 2.50 ± 3.33a 0.6688
 Morphospecies/sample 0.67 ± 0.52a 0.83 ± 0.41a >0.9999
 Exponent of Shannon Ind. 0.67 ± 0.52a 0.83 ± 0.41a >0.9999
All groups
 Total individuals 160 115
 Individuals/sample 26.67 ± 9.83a 19.17 ± 7.44a 0.2576
 Total morphospecies 40 30
 Morphospecies/sample 12.33 ± 1.51a 9.50 ± 4.85a 0.4784
 Exponent of Shannon Ind. 10.21 ± 2.15a 7.28 ± 3.43a 0.0962

Different small letters mean statistical differences between treatments (Mann–Whitney t-test for discrete variables and unpaired t-test for continuous variables; p-value <0.05).

After grazing, no significant differences were observed between the chicken treatment and the control regarding the number of individuals per sample, the morphospecies richness, and the exponent of the Shannon index in the dominant orders Hymenoptera, Isopoda, Coleoptera, and Julida (p > 0.05; Table 2). However, the results indicate that the chicken treatment presented significantly fewer spiders per sample than the control (p = 0.0325), suggesting a negative effect of hens regarding these individuals, at the studied animal density (3.5 m2 per hen). Furthermore, also regarding this group, the exponent of the Shannon index was 4.39 (mean value) in the control and approximately half in the chicken treatment (2.58). Although there are no statistically significant differences between the treatment and the control regarding this index (p = 0.0592), we emphasize that the found p-value is very close to the limit that takes into account significant differences, suggesting that the hens can also eventually affect the diversity of this group.

Moreover, the results from comparing the diversity profiles (Hill numbers) between the chicken treatment and the control showed substantially less diversity in the chicken treatment (Figure 5), suggesting that the hens can also negatively affect the general epigeic macrofauna diversity of the system. Although grazing was intermittent, the use of fixed structures, the grazing duration, and the applied density (3.5 m2 per hen) may have contributed to a more aggressive impact on the system’s fauna diversity.

Figure 5 Diversity profiles (Hill numbers) of the chicken treatment and the control, after grazing, at the orchard.
Figure 5

Diversity profiles (Hill numbers) of the chicken treatment and the control, after grazing, at the orchard.

4 Discussion

4.1 Horticultural field

In the horticultural field, our results suggest that the thermal treatment, using flame weeding, may have a slightly negative effect on the diversity of epigeic macrofauna, when compared to the other studied treatments (chicken and mechanical), which presented identical diversity profiles. However, no significant differences were found between treatments in the various analyzed parameters, suggesting that, despite the lower diversity of the thermal treatment, in general, the effects of the studied treatments on soil macrofauna are quite identical.

Regarding the increase in both abundance and diversity in all treatments over time, it is reasonable to consider that this common increase was probably not because of the effects of treatment, but due to external factors common to all treatments. Since soil tillage significantly affects this kind of fauna [22], and since the first sampling was done before treatments and after the tillage which prepared the field for crop production, it is realistic to consider this tillage as a possible factor that contributed to the much lower number of individuals found before the intervention of treatments.

Despite the absence of significant differences between the studied treatments regarding soil epigeic macrofauna, we found a significantly higher earthworm density in the chicken treatment, after grazing. These results disagree with the results of Clark and Gage [8] with foraging chickens but are in agreement with the results found by other authors regarding grazed cattle and grazed sheep [23,24]. Several authors have reported increases in both earthworm density and biomass in organically fertilized fields [25,26]. Nitrogen-rich materials are highly preferred by earthworms [27], which justifies their higher abundance and higher biomass in nitrogen-rich soils, even when the nitrogen source is based on mineral fertilizers [28]. Grazing chickens at the horticultural field for 84 continuous days significantly contributed to an increase in the amounts of both nitric and ammoniacal nitrogen in the grazed soils [5]. This high and significant increase in the amounts of nitrogen in the soil, due to the deposition of dropping, may justify the higher density of earthworms found in the chicken treatment. Although chickens are likely to eat these macrofauna [29], since grazing took place during the dry season, when earthworms are less active, the intake may have been reduced. In these circumstances, the earthworms would have benefited from the accumulation of droppings, without being negatively affected by the scavenging behavior of hens. These results are particularly relevant since earthworms play a key role in soil fertility, contributing to the humification of organic materials and the formation of soil aggregates, which enhances soil stability and water infiltration [30]. However, more research is needed for a better understanding of the scavenging effects of hens on populations of earthworms, especially considering different meteorological conditions.

4.2 Orchard

Grazing chickens at the orchard significantly changed the usual soil macrofauna of this agroecosystem. In this location, the chicken treatment presented significantly fewer spiders per sample than the control treatment (orchard understory vegetation, without treatments). This finding agrees with the results found by Clark and Gage [8], with foraging chickens, reinforcing the negative effects of chickens on these soil organisms. Although the biological control of spiders strongly depends on several factors, such as phenotype, pests, alternative preys, and environmental conditions, spiders are dominant nonvertebrate predators in most terrestrial ecosystems and have high potential as pest control agents [31,32]. Accordingly, the lower number of spiders in the grazed soils requires further attention. This result can arise from the chickens’ intake of these individuals since arachnids have high contents of nitrogen, minerals, and trace elements that can contribute to the nutrition of chickens [33,34]. However, this result can also arise from the habitat disturbance in the grazed plots, due to the presence of the animals. The grazing chickens led to the eradication of vegetation (bare soil) and superficial soil disturbance, due to the scavenging behavior, which may have led to the loss and/or escape of the spiders from the grazed soils.

Furthermore, our results suggest that grazing chickens at the orchard contributed to a significant reduction in the natural epigeic macrofauna diversity of this agroecosystem, according to the found diversity profiles (Hill numbers). Particular attention is needed to this disturbance, since it can compromise the system’s resilience, decreasing its capacity to resist external disturbances. This loss of diversity reinforces the need to practice good grazing management, applying pasture rest periods and/or lower animal outdoor densities. We emphasize that more research into the effects of chickens on soil biology is needed to find a grazing balance that benefits animal production without harming soil biological properties.

4.3 Research limitations

The findings reported herein should be considered in light of some limitations. This work is limited by the use of endangered native breeds in both experiments. The use of such breeds in scientific studies contributes to the conservation of their genetic heritage, in addition to proving their genetic value in systems with outdoor access, such as organic systems. However, the use of these endangered breeds in both experiments and the small number of animals available made it difficult to carry out larger and several experiments, in different locations during the same season. Furthermore, our research could have been improved by identifying organisms at the species level, rather than identifying morphospecies; by increasing the number of samples; and by evaluating earthworms at the orchard, which was not assessed. This work is part of a broad project, which aims to evaluate the integration of laying hens with crops considering several scientific areas, such as soil fertility, pest and weed control, and crop and animal productivities. In this context, it became difficult to collect and analyze more biological samples than those previously mentioned, due to logistical difficulties, such as a high volume of samples from other scientific areas, and short available time and human resources. Moreover, due to the high volume of samples not related to soil macrofauna and the size of each plot (which was conditioned by the low number of available animals), it was particularly difficult to obtain volumes of undisturbed soils for earthworm collection at the orchard, which was not assessed in this location.

5 Conclusions

Soil macrofauna plays a key role in soil fertility. This study demonstrates that chickens can contribute positively or negatively to soil epigeic macrofauna, depending on the agroecosystem. In the horticultural field, where we used chickens as weed control agents and compared their effects to two other weed control treatments (thermal and mechanical), we found that the effects of chickens on soil epigeic macrofauna are quite identical to the other studied treatments. On the other hand, the chicken treatment contributed positively to the density of earthworms in the medium term after grazing, probably due to the accumulation of droppings. At the orchard, the chicken treatment contributed negatively to the spiders’ natural density of that agroecosystem, and it also contributed to a decrease in the general soil epigeic macrofauna diversity, which requires special attention.

Considering the lack of previous research studies on this topic and the importance of soil biology to sustainable soil management, further research is recommended regarding the effects of grazing chickens on soil macrofauna. Future research should address the ways to optimize the management of these animals in the pasture. It is important to identify a combination of animal density and a grazing duration that allows reaching a balance between the chickens’ use of the pasture and the damage caused to soil macrofauna, although this is highly variable and depends on other factors, such as weather conditions and breeds. Chickens can be valuable elements in integrated crop–livestock systems, but more research is recommended regarding their impacts to enhance the sustainability of such agroecosystems.

Acknowledgments

The authors are deeply thankful to Rui Amaro, Daniela Santos, Alexandra Oliveira, Rosinda Leonor Pato, Isabel Costa, Fernando Amaral, Jorge Bandeira, Filipe Melo, Luís Miguel Valério, and Rui Ferreira for their knowledge, and field and laboratory support; to the Azorean Biodiversity Group Members, Paulo Borges, Rosalina Gabriel, and Alejandra Roz Prieto for all the suggestions; to Lúcio Paiva for his field contributions; to Clarinda Paixão from Américo Duarte Paixão Lda for kindly providing the necessary amount of mustard to the extraction of earthworms; to Ana Bela Lopes and Noémia Bárbara for their diligent proofreading and English editing; and to the anonymous reviewers, whose suggestions improved this manuscript.

  1. Funding information: This work received financial support from the Polytechnic Institute of Coimbra within the scope of Regulamento de Apoio à Publicação Científica dos Professores e Investigadores do IPC (Despacho no. 12598/2020). The work was also partially supported by Grant IIA_PDR2020_GMÓVEL_LIC1 and Project Grant PDR2020-101-031353, through the European Regional Development Fund, the PDR 2020 Programs, and FCT Portuguese Foundation for Science and Technology.

  2. Author contributions: Conceptualization, P.R.S., R.G., and A.C.; methodology, P.R.S., R.G., and A.C.; formal analysis, P.R.S.; investigation, P.R.S. and C.G.; resources, P.R.S., R.G., and A.C; writing – original draft preparation, P.R.S.; writing – review and editing, P.R.S., R.G., A.C., and C.G.; supervision, C.G. All authors have read and agreed to the published version of the manuscript.

  3. Conflict of interest: The authors state no conflict of interest.

  4. Data availability statement: All data generated or analyzed during this study are included in this published article.

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Received: 2022-05-18
Revised: 2022-12-30
Accepted: 2023-01-15
Published Online: 2023-03-30

© 2023 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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https://doi.org/10.1515/opag-2022-0172
Keywords for this article
earthworms; insects; laying hens; soil biology; spiders; weed control
Creative Commons
BY 4.0

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  2. The impact of COVID-19 pandemic on business risks and potato commercial model
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  47. Effect of arbuscular mycorrhizal fungi on early growth, root colonization, and chlorophyll content of North Maluku nutmeg cultivars
  48. How intergenerational farmers negotiate their identity in the era of Agriculture 4.0: A multiple-case study in Indonesia
  49. Responses of broiler chickens to incremental levels of water deprivation: Growth performance, carcass characteristics, and relative organ weights
  50. The improvement of horticultural villages sustainability in Central Java Province, Indonesia
  51. Effect of short-term grazing exclusion on herbage species composition, dry matter productivity, and chemical composition of subtropical grasslands
  52. Analysis of beef market integration between consumer and producer regions in Indonesia
  53. Analysing the sustainability of swamp buffalo (Bubalus bubalis carabauesis) farming as a protein source and germplasm
  54. Toxicity of Calophyllum soulattri, Piper aduncum, Sesamum indicum and their potential mixture for control Spodoptera frugiperda
  55. Consumption profile of organic fruits and vegetables by a Portuguese consumer’s sample
  56. Phenotypic characterisation of indigenous chicken in the central zone of Tanzania
  57. Diversity and structure of bacterial communities in saline and non-saline rice fields in Cilacap Regency, Indonesia
  58. Isolation and screening of lactic acid bacteria producing anti-Edwardsiella from the gastrointestinal tract of wild catfish (Clarias gariepinus) for probiotic candidates
  59. Effects of land use and slope position on selected soil physicochemical properties in Tekorsh Sub-Watershed, East Gojjam Zone, Ethiopia
  60. Design of smart farming communication and web interface using MQTT and Node.js
  61. Assessment of bread wheat (Triticum aestivum L.) seed quality accessed through different seed sources in northwest Ethiopia
  62. Estimation of water consumption and productivity for wheat using remote sensing and SEBAL model: A case study from central clay plain Ecosystem in Sudan
  63. Agronomic performance, seed chemical composition, and bioactive components of selected Indonesian soybean genotypes (Glycine max [L.] Merr.)
  64. The role of halal requirements, health-environmental factors, and domestic interest in food miles of apple fruit
  65. Subsidized fertilizer management in the rice production centers of South Sulawesi, Indonesia: Bridging the gap between policy and practice
  66. Factors affecting consumers’ loyalty and purchase decisions on honey products: An emerging market perspective
  67. Inclusive rice seed business: Performance and sustainability
  68. Design guidelines for sustainable utilization of agricultural appropriate technology: Enhancing human factors and user experience
  69. Effect of integrate water shortage and soil conditioners on water productivity, growth, and yield of Red Globe grapevines grown in sandy soil
  70. Synergic effect of Arbuscular mycorrhizal fungi and potassium fertilizer improves biomass-related characteristics of cocoa seedlings to enhance their drought resilience and field survival
  71. Control measure of sweet potato weevil (Cylas formicarius Fab.) (Coleoptera: Curculionidae) in endemic land of entisol type using mulch and entomopathogenic fungus Beauveria bassiana
  72. In vitro and in silico study for plant growth promotion potential of indigenous Ochrobactrum ciceri and Bacillus australimaris
  73. Effects of repeated replanting on yield, dry matter, starch, and protein content in different potato (Solanum tuberosum L.) genotypes
  74. Review Articles
  75. Nutritional and chemical composition of black velvet tamarind (Dialium guineense Willd) and its influence on animal production: A review
  76. Black pepper (Piper nigrum Lam) as a natural feed additive and source of beneficial nutrients and phytochemicals in chicken nutrition
  77. The long-crowing chickens in Indonesia: A review
  78. A transformative poultry feed system: The impact of insects as an alternative and transformative poultry-based diet in sub-Saharan Africa
  79. Short Communication
  80. Profiling of carbonyl compounds in fresh cabbage with chemometric analysis for the development of freshness assessment method
  81. Special Issue of The 4th International Conference on Food Science and Engineering (ICFSE) 2022 - Part I
  82. Non-destructive evaluation of soluble solid content in fruits with various skin thicknesses using visible–shortwave near-infrared spectroscopy
  83. Special Issue on FCEM - International Web Conference on Food Choice & Eating Motivation - Part I
  84. Traditional agri-food products and sustainability – A fruitful relationship for the development of rural areas in Portugal
  85. Consumers’ attitudes toward refrigerated ready-to-eat meat and dairy foods
  86. Breakfast habits and knowledge: Study involving participants from Brazil and Portugal
  87. Food determinants and motivation factors impact on consumer behavior in Lebanon
  88. Comparison of three wine routes’ realities in Central Portugal
  89. Special Issue on Agriculture, Climate Change, Information Technology, Food and Animal (ACIFAS 2020)
  90. Environmentally friendly bioameliorant to increase soil fertility and rice (Oryza sativa) production
  91. Enhancing the ability of rice to adapt and grow under saline stress using selected halotolerant rhizobacterial nitrogen fixer
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