1 Introduction

Feeding the large global population with the increasing scarce of natural resources is a huge challenge for humanity [1]. Although in recent years the production of food has been remarkably improved around the world, mainly due to extensive use of chemical fertilizers, pesticides, machineries and high-yielding varieties for different crops in agriculture [2]. Unfortunately, this intensification of food production leads to environmental concern because of severe loss of biodiversity and soil degradation, which is a big issue for the ensuring welfare of humanity [3, 4]. Sustainable crop production is essential for tackling this issue and it is the system in which maintaining the yield of crops by using low inputs and conserving natural resources [5]. Soil is the fundamental resource for crop production which regulates different processes such as water and nutrient movement, carbon sequestration and maintaining biodiversity from sessile flora to different soil fauna such as ground beetles, earthworms, moles etc. [6, 7].

Soil compaction is a big problem for crop production. About 68 million ha of land is degraded due to soil compaction worldwide [8]. The main cause for soil compaction is the extensive use of agricultural machineries [9]. Bulk density and penetration resistance increased in compacted soil and reduced the soil porosity and pore connectivity at the same time [10, 11]. Therefore, the roots of plants cannot efficiently use natural resources from the deeper soil due to the presence of a compacted layer [11, 12]. Schneider and Don [13] showed that subsoil contains more than half of the water and plant nutrients. Similarly, storage of organic caron is double in subsoil (20–200 cm) compared to topsoil (0–20 cm) [14]. Kautz et al. [15] reported that subsoil contributes around 10–80% of plant nutrients, particularly when topsoil is dry, and nutrients are deficient. Compacted subsoil prevents plant roots from accessing a significant portion of water and nutrients, leading to underutilization of these resources.

There are several ways for improving root growth in compacted soil. Firstly, traditional deep tillage can be used to improve rooting depth in hard soil [16]. However, the impact of deep tillage is short live [17] and this technique requires huge amounts of energy which increases the input cost [18]. On the other hand, soil biopores can be used as a preferential pathway for roots to grow into the deeper soil by providing less mechanical resistance which helps for accessing roots and the utilization of subsoil resources [19].

Biopores are the round shaped pores in soils that are created by the actions of soil living organisms mainly by the plants roots and earthworm’s activities [20]. Biopores are available across the soil profile from the topsoil to several meters depth of soil [20]. Many researchers have claimed that thick and deep roots can penetrate hard soil which after decomposition produced biopores [21, 22] that is also termed as bio-tillage [23]. Islam et al. [24] showed that biopores provide access into the deeper soil for rice roots through the compacted plough pan. Moreover, Colombi et al. [19] reported that biopores improved air permeability in compacted soil. Additionally, biopores improve the water infiltration which reduces the runoff and erosion after heavy rainfall [25].

The wall of biopores created from the decomposition of roots and earthworm’s activities is enriched with nutrient [26]. Dresemann et al. [27] found that uptake of N was greater by the roots of wheat plants grown in microcosms having biopores. Moreover, biopore acts as a hotspot for microbes [28, 29] because of having a higher availability of food and a proper environment in biopores [30]. The bacterial population was greater in the biopores wall than in the soil apart from biopores due to higher availability of carbon in bipores [31]. This improved microbial population is important for crop production because all the biogeochemical processes such as decomposition of organic matter, nutrient cycling, carbon sequestration etc. depend on microbial activities [32]. However, sometimes biopores have a negative influence on root growth particularly when the diameter is larger than the root diameters due to lack of root-soil contact [33, 34] which might reduce the water and nutrients uptake from the soil [35]. Although biopore has some negative impacts in some situations, it has great influence on improving crop productivity particularly in compacted soil. However, the impact of biopores depends on pore characteristics such as size, shape [24], abundance of pores [36], moisture content [37], compaction of soil [38], plant species [24], tillage condition [39, 40] and so on.

The influence of biopore for improving crop productivity can be maximized by using different techniques such as conservation tillage which ensure less disturbance of biopores [35], using perennial [20], tap and deep-rooted plants that have more capacity to create biopores [41], ensuring better crop establishment by timely planting of preceding and succeeding crop [39]. Maintaining reduced tillage is very important for conserving the abundance of biopores from the topsoil to subsoil [40].

Although the impact of biopore-root interaction depends on many factors, there are no comprehensive studies on various variables that influence the impact of biopores on improving crop productivity. This review aims to fill this gap by exploring the various factors affecting biopores influence on root development and crop yield. Additionally, how can we maximise the impact of biopore-root interaction on crop production is not presented in organized ways in the current literatures. Therefore, we also discussed how to maximize the impact of biopore by proper utilization of water and nutrients for sustainable crop production.

2 Methods

Relevant publications were identified using different online search resources such as Google Scholar, Wiley Online, Science Direct, Springer Link, Academia, PubMed, Taylor & Francis Online, and Research Gate platforms. The keywords used for collecting relevant publications were Biopore, Biopores, Macropores, Macropores, Pore, Soil structure, Bio-tillage, Root-soil ineteraction, Cracks, Soil burrowing, Root impacts, Soil structure, Soil pore and Porosity. Out of over 380 articles, 89 articles were found more relevant to tackle the issues mentioned in this review. The results from different field and laboratory studies were included in this review for better understanding of different factors and mechanisms related to root-biopore interactions. Additionally, attempts have been made to depict currently available and possible strategies for maximizing the impact of root-biopore interaction to improve crop productivity in a sustainable way.

3 What is biopore?

Soil pore system is formed by the process of spatial arrangement of soil separates as well as by the actions of biological activities such as growth of roots and activities of soil fauna. Islam et al. [21] noted that previously growing roots can create channels which are utilized by the roots of succeeding plants in subsoil. Additionally, Banfield et al. [28] claimed that soil fauna such as earthworms can create these channels (Fig. 1). Scientists have described that the soil pore which is formed by biological activities is termed as ‘biopore’ [20, 42]. However, biopores that are created and inhabited by earthworms are known as the drilosphere [43]. The drilosphere is not only the pores created by the earthworm’s activities, but it also includes the skin, cast, middens and gut [44]. Biopores are the part of soil macropores and it only consists of 1–10% of total soil volume [28]. On the other hand, Zhang et al. [45] showed that biopores contribute 30.1–58% and 66.3–74.1% of total macroporosity in the subsoil (20–30 cm depth) for rainfed maize and paddy fields, respectively.

Fig. 1
figure 1

Biopore formation processes by the actions of plant roots and earthworms

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The size of the biopores ranging from greater than 30 μm up to 5 mm [26, 46] depending on the factors such as crop type, compaction level, nutrient status of the soil [20]. Strong root systems of preceding crops can grow through compacted soil and after decomposition it produces biopores and this process is called bio-tillage [23]. A field study with sandy loam soil in Denmark conducted by Pulido-Moncada [47] showed that different cover crops such as lucerne and chicory can make many vertically well-connected pores (biopores) in hard subsoil. Moreover, many scientists have shown that different plants can create different types of biopores after decomposition of roots [21, 41]. One of the major alterations in soil structure is the creation of interconnected biopores through plant root degradation [48].

4 Difference between biopore and non-biopore

Soil pore system is crucial for transporting water and air which acts as niches and habitats for soil fauna and plant roots [26, 45]. However, this pore system varies in types such as biopores and non-biopores [49, 50] which are different in functions and morphological features [45]. The main differences between biopores and non-biopores are summarised below in Table 1.

Table 1 Major differences between biopore and non-biopore
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5 Factors affecting biopore-root interaction

There are many factors that affect biopores-root interaction (Fig. 2).

Fig. 2
figure 2

Diagram showing different factors that affect the impact of biopores on plant performance. Up arrow (↑) means impact of biopore is greater and down arrow (↓) means impact of biopore is lower

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5.1 Compactions

Soil bulk density controls the root growth in biopores, which is repeatedly addressed in many studies [12, 38] (Fig. 3). The roots of ryegrass seedlings tended to grow towards artificial biopores when soil strength was greater [56]. In a laboratory study with different bulk densities (1.4, 1.6 and 1.8 g cm−3) De Freitas et al. [57] reported that growth of maize roots was 68.8% of total roots in macropores when the bulk density was at or above 1.6 g cm−3 compared to 1.4 g cm−3 bulk density. On the other hand, growth of wheat roots was only 12.5% in biopores when the bulk density was lower than 1.2 g cm−3 [38]. Similarly, a medium-resolution microscopic analysis study by White and Kirkegaard [58] reported that about only 30–40% of the wheat roots on the inside of macropores in loose topsoil and 85–100% of the roots inside the compacted subsoil. Additionally, a column experiment by Xiong et al. [59] with high resolution X-ray CT image analysis reported that the number of biopores utilized by maize roots was 2.7 times higher in the compacted (1.6 g cm-3) soil than in the noncompacted (1.3 g cm-3) soil [59]. However, the number of biopores crossed by the maize roots was greater in non-compacted soil compared to compacted soil. The presence of biopores in loose soil did not increase the shoot and root biomass of wheat [37]. Therefore, higher bulk density stimulates the growth of roots towards biopores. The bulk density of soil is expressed as penetration resistance. Penetration resistance higher than 2 MPa has been recorded as critical value which reduces the root growth [60]. The growth of roots is prevented at 2.8 MPa penetration resistance in bulk soil then follows root growth in biopores [38].

Fig. 3
figure 3

Picture showing rice roots growing through biopores in compacted plough pan in controlled greenhouse conditions. Image taken by high resolution camera. Source [24]

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5.2 Size, shape and orientation of biopores

The effectiveness of biopores depends on the size of biopores. Landl et al. [36] reported that a biopore with a wider diameter than the root diameter is not effective for water and nutrient uptake by the plant roots due to lack of root-soil contact. Although more than 80% of the roots of maize were in large size (3.2 mm) biopores and depth of root length doubled, the growth of maize plants decreased compared to control without biopores [61]. Additionally, White and Kirkegaurd [58] found that the growth of wheat root has no impact if the biopores size is large. Similarly, Bouke et al. [37] showed that large size biopores limit the water and nutrient uptake due to the presence of large air gaps between the pore walls and plant roots. The length of different types of roots improved according to the size of biopores. In a field study, Han et al. [62] showed that an increased number of fine roots is present in small size biopores. On the other hand, more medium and larger root growth was observed in soil with large biopores. This study suggested that the size of the biopore is important for selection of crops with different root architectures for better utilization of biopores.

In addition to biopore size, orientation of the biopores (vertical or angled) determines the root growth within the biopores as well as re-entering roots into bulk soil. A laboratory study with ryegrass Hirth et al. [56] showed that about 13% of roots grew within the biopores before re-entering into the bulk soil when the biopores are vertically (90°) oriented [56]. On the other hand, this study also reported that 78% roots of ryegrass grew only a few millimetres before re-entering bulk soils when biopores were inclined at 40°. Similarly, a modelling study conducted by Landl et al. [63] found that 83–98% of plant roots remained in the biopores when pores were oriented at 90° and only 18–60% of the roots remained in biopores when the inclination was 40°.

Besides the size and orientation of the biopore, shape is also an important factor for the utilization of biopores for water and nutrient uptake from the deeper soil. A greenhouse study by Islam et al. [24] reported that the root length density of rice plants was 55% greater for elongated biopores compared to round biopores.

Moreover, pore wall roughness and microporosity in the pore wall affect the roots re-entering into the bulk soil. The roots of ryegrass re-enter into the bulk soil from the biopores more efficiently when the roughness and microporosity of the pore wall is greater [56]. A laboratory study using X-ray CT imaging technique showed that the tendency of maize roots to grow into biopores was greater when the wall of biopore is roughened [64].

5.3 Abundance

A column experiment with wheat plants showed that increasing the number of biopores increased root length density but did not increase the root biomass [65]. Therefore, it concluded that roots can be able to explore a greater volume of soil with the same root biomass which will be good for improving water and nutrient uptake from the greater depth of subsoil. This study also suggested that biopore not only increases the root length of plants but there is also a potential for increasing the yield of the plants. Setiawan and Rohmat [66] showed the infiltration of water depends on the number of biopores presence in the grass fields and it reduced the runoff from fields more efficiently when the abundance of biopores was greater [66].

5.4 Management practices/tillage impacts/climatic condition

Formation and maintenance of biopore mainly depend on the management and climatic condition of agricultural land [35]. In the frequently cultivated ecosystems, pore system is disrupted and damaged especially in plough layer [39, 40]. In contrast, bioppores are more stable for soil under natural conditions [39]. The impact of biopores is restricted to the deeper soil in annual cropping systems [67]. Moreover, tillage has great impact on the existence of biopores. Biopores can be continual from surface to subsoil in conservation tillage with perennial cropping systems [40]. The density of biopores is higher in zero or reduced tillage systems compared to conventional tillage practices [40] (Fig. 4) because of an increase in the number of earthworms, which encourages the creation of biopores [20]. Additionally, tillage destroys the opening of biopores, reducing their capacity to facilitate gas exchange with the atmosphere and water infiltration [20]. The utilization of biopores also depends on the climatic conditions of a region. A modelling and real experimental study by Landl et al. [36] showed that the uptake of water by the wheat plant increased during the drought period in the presence of biopores in compacted soil. The impact of biopores varies depending on climatic conditions or locations. The clumping of roots was recorded in biopores and roots were not re-entered into the bulk soil in Australia [33]. However, in Europe, it showed that roots were less clumped in the biopores, and they also observed the re-entry of roots into the bulk soil [26]. This clumping tendency of roots in the biopores differed due to the difference in climatic conditions. In Australia there is dry climatic condition [68] whereas in Germany there is a high precipitation rate. Therefore, the impact of biopores is more prominent in drought prone areas compared to wetland areas.

Fig. 4
figure 4

Adapted from Or et al. [40]

Image showing biopore abundance in different tillage systems. A Zero tillage; B Reduced tillage and C Conventional tillage fields.

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5.5 Plant species

Plant species is also another important factor for getting benefits from the presence of biopores. A controlled greenhouse study by Islam et al. [21] showed that deep rooted rice plant created 20% more biopores compared to shallow rooted rice plants. Additionally, Islam et al. [24] reported that the deep rooted rice genotype produced 81% greater RLD, 30% more root numbers and 103% more branching in the subsoil with the presence of artificial biopores than the shallow rooting rice genotype. Moreover, perennial root systems are much more effective for the creation of more stable and continuous biopores compared to annual root systems [67]. Because the roots of perennial plants are better at penetrating compacted soil due to having thick and deep rooting ability [69]. In general, tap rooted crop species are more effective for drilling the soil than those of fibrous rooted plant species because roots of fibrous rooted plants remain mostly in shallower depth [70]. A field experiment conducted by Huang et al. [71] showed tap rooted precrop chicory increased the number of large sized (5–6 mm) biopores than the fibrous rooted tall fescue. The increased soil macroporosity under the tap rooted crops cultivation is frequently shown by different scientists [72,73,74]. The biopores utilized by the different root systems differently. The tap rooted oilseed rape roots grew in the centre of a biopore with only a few lateral roots attached to the pore wall, whereas fibrous rooted wheat roots grew around the biopore wall which helps for establishing higher root-soil contact [26].

5.6 Soil texture

Soil texture has a great influence on both root decomposition and the quality of biopores. Phalempin et al. [64] reported that maize roots decomposed quickly (> 78 days) in loam soil. However, some biopores were not completely decomposed after 216 days in the sandy soil. The authors also showed the biopores in loam soil were much more stable than biopores in sandy soil.

5.7 Moisture content

Soil moisture content is also a factor for determining the effects of biopores on the growth of plant roots. Because the penetration resistance of soil is modulated by the moisture content and the penetration resistance increases with the reduction of soil moisture. Volkmar [75] investigated that the growth of wheat roots was only observed in dry conditions (Negative water potential). On the other hand, root and shoot growth of spring wheat is reduced in the treatment with biopores in dry conditions compared to without biopores in well irrigated conditions [37]. A laboratory study with artificial macropores by Dresemann et al. [27] showed that the shoot dry weight of winter wheat increased by 66% when grown with the presence of biopores in low water content conditions. On the other hand, shoot dry matter was increased only by 39% when grown with the presence of macropores with high moisture content.

5.8 Depth of soil

Biopores in the deeper soil are more persistent than the biopores in the topsoil [20] because biopore system in the topsoil is frequently destroyed the tillage and machinery activities. On the other hand, biopores in the subsoil are usually intact due to less intervention by tillage activities [20]. In a study, Han et al. [76] concluded that pores size reduced with depth and the authors also claimed that smaller pores (< 0.2 mm) reduced more quickly than larger size pores (0.2–0.1 mm). Therefore, more studies are needed on the dynamics of the creation and utilizations of root-induced biopores in subsoil.

5.9 Nutrient concentration

Apart from different morphological properties and climatic conditions, higher nutrient availability may enhance the root growth in biopores. A study with artificial pores suggested that root growth was 6 times higher in pores with improved nutrient content than in pores filled with sand or empty pores [77]. A rhizotron study with wheat plants Bauke et al. [37] reported that improved water and phosphorous supply enhanced the shoot and root biomass production with the presence of biopores. However, there was no effects of biopores on the shoot and root biomass in water and phosphorous limited conditions.

6 How to improve the effects of biopore?

The improvement of biopore impact is very crucial for sustainable agriculture. The maximization of biopore benefits depends on the various factors such as soil type, crop selection, cropping duration, tillage history etc. A field study with different fodder crops Han et al. [41] showed that soil (Luvisols) with greater silt and clay contents and with bulk density of 1.45 g cm−3 is ideal for creating stable biopores compared to sandy and loose soil. However, soil (Ultisols) with lower bulk density (1.0 g cm−3) is not ideal for stable biopores formation [78] due to having greater shrinkage capacity of loose soil and at the same time, less compacted soil is more susceptible to being deformed after drying [79]. On the other hand, the soils which are extremely compacted (4 MPa) such as Kandosols which contains large amounts of kaolinite that acts as a cementing agent are not good for the creation of biopores by the plant roots and soil fauna because of greater soil strength [58]. Many studies have reported that deep and conventional tillage decreased biopores abundance [40, 42].

Despite the soil types, crop species selection is also playing a vital role in the formation and utilization of biopores. The ability to penetrate the compacted soil is different by the different plant species. Dicotyledonous plants are more effective for penetrating the hard soil compared to monocotyledonous plants [80] because of having greater diameter roots for dicots [81] which can exert greater radial pressure to grow in deeper [82]. A growth chamber study by Stirzaker et al. [81] showed that only larger (< 0.8 mm) roots of barley were able to penetrate the biopore wall which indicates that re-entry of roots from the biopores into the bulk soil depends on the root’s morphologies. Plants with large tap root systems can create more biopores than shallow and fibrous rooted plants [26, 74]. In a field study by Han et al. [41] reported that about 28% more biopores are produced by the tap rooted chicory than fibrous rooted tall fescue.

Cropping duration is another way of increasing the density of biopores. Around 6 times higher biopores density was recorded in the third year compared to the first year for different crops such as lucerne, chicory and tall fescue [41]. Therefore, by cultivating the perennial crops rather than annual crops is better for getting more biopores [20]. Yunusa and Newton [46] suggested that there are four main characteristics for good biopores formation plants: (1) thick and deep roots, (2) rapid growth rate and perennial in nature, (3) rapid decomposition of roots and (4) quick adaptivity to physical constraints.

The continuity of biopore is greater for the fields under no-tillage compared to conventional tillage [35]. Tillage operation destroys the vertical opening of biopores which affects the water and nutrient uptake as well as infiltration and exchange of gas in the biopore networks [20]. Additionally, root growth in subsoil increased in moist conditions than in dry conditions [83]. Timely planting will ensure better root growth [39] which might be helpful for the formation of more biopores by the plant roots. Therefore, maintaining proper moisture and timely planting in the fields are good strategies for getting a good number of biopores. Some other strategies can be adopted for increasing the population of earthworms in the fields by reducing tillage intensity and depth [84].

7 Research gaps and future works

There are many studies that have been recorded on the impacts of biopores on the growth of plants. However, the results are not consistent [19, 26, 33, 37]. Different plants can create different types of biopores in field conditions which vary in their shape, size and orientation due to having different root architectures [85]. Moreover, most of the studies in the literature are focused on how bulk density and penetration resistance affect biopores influences on plant growth [33, 56]. However, very little attempt has been done on how the characteristics of biopores and their pore walls affect the growth of roots in biopores due to opacity of the soils [86, 87]. Additionally, more studies should be conducted with contrasting root architectural genotypes of different crops to get higher benefits from the presence of biopores.

Some studies have reported that biopores abundance affects water infiltration and root growth [65, 66], but more studies need to be done to confirm the critical number of biopores per unit area, which will be good for maintaining water and nutrient dynamics for sustainable crop production.

The management of the field for maximizing the effects of biopores is still elucidated. For instance, Bauke et al. [37] showed that biopore has no impact in phosphorous and water limited conditions on the growth of roots and shoots for spring wheat. On the other hand, root and shoot growth of spring wheat significantly improved under sufficient water and nutrient conditions in the presence of biopores [88]. Therefore, the optimum water and nutrient status needs to be explored for maximizing the impact of biopores on the subsequent crops. However, appropriate water and nutrient status depends on the types of soils and climatic conditions [88] which also need to be further studied.

Changing the cropping pattern such as irrigated to upland for rice cultivation improved biopore production and enhanced the crop performance in upland conditions [21]. This needs more investigations in field conditions for improving the most important cereal crop rice production specially in the water limited environment.

Biopores improve the root length and root biomass for various crops [19, 24]. However, this improvement in root growth may accumulate lots of carbon which might affect the yields of plants. Therefore, more research should be conducted on the calculation of carbon balances for different plants growing with the presence or absence of biopores.

8 Conclusions

Biopores can be utilized by the plant roots as they improve the soil physical, chemical as well as biological properties. Biopores formed by the activities of plant roots and earthworms act as a preferential pathway for growing of roots in deeper soil especially in compacted soil. It also helps for utilization of water and nutrients from the subsoil during a drought period. On the other hand, leaching of nutrients from the topsoil to deeper soil may occur after heavy rainfall through biopores and sometimes roots may be clamped into the biopores, which will negatively affect the production of crops. The impact of biopores depends on many factors such as soil compaction, size of biopore, root characteristics, depth of soil, management practices for crop production and tillage operations. To maximize the effects of biopores, genotypes with deep and thick roots should be cultivated in loamy or clay soil using conservation tillage. Although biopore has great potential for improving crop production in sustainable ways, some research gaps need to be addressed related to optimum abundance of biopores, characteristics of biopores for improving root growth and management practices for maximizing the impact of biopore in real field conditions. This review will improve our understanding of how different factors influence biopore-root interaction ultimately enhances adaptation of various crops to promote higher yield in stressful environmental conditions.