Introduction
Soils are very important and non-renewable resource and a key factor of the
earth system. This is evident from the functions that soil performs. The
important functions of the soils are: (1) it is a habitat for biodiversity,
(2) filters the contaminants in the water (acts as a natural filter), (3)
Support the man-made structures, (4) supports plant for food and nutritional
security, (5) it is an important ally to combat climate change by storing
very high amount of carbon in it, etc. Thus, it offers services, resources
and goods to the human society. Soils play a pivotal role in the
hydrological, biological and geological earth system cycles. But this
natural resource has been experiencing different types of degradation. Among
different degradations processes, soil salinity and sodicity are a one of
the global environmental problems which seriously limit the productivity of
cultivated land (Mao et al., 2014). The salt affected soils occupy
approximately 3 % of the world's total geographical area i.e. 402 and 434
million hectare (Mha) lands are classiffed as saline and sodic, respectively
(Singh, 2015) making them unproductive. The area under salinization in world
has been increasing continually (Drake et al., 2015). Soil salinity is one
of the most important abiotic stresses responsible for reduced crop
production (Plant et al., 2013). In India, about 6.74 Mha of soils are
affected with soil salinity, of which 1.25 Mha is in coastal areas (CSSRI,
2014). Intrusion of saline water either directly through sea or estuaries
indirectly, seepage for the salt water reservoirs and intentional stoppage
for the fish or prawn farming are important reasons for coastal soil
salinity in Goa, India. The area under these soils has been increasing due
to the natural and anthropogenic activities. This has led to development of
a typical characteristic in these soils i.e. presence of salinity and
acidity simultaneously. These soils are locally called as “Khazan” and
occupy nearly 18 000 ha area, of which 12 000 ha is under monoculture of
rice in monsoon season only. These soils are often left fallow in the rabi
(post-monsoon season) because of high salinity levels and no availability of
irrigation water. Farmers have started abandonment of agriculture on such
soils due to low rice productivity (1.5 to 2.0 tha-1). This might be
basically due to excessive soil salinity causing adverse crop growing
conditions and unfavorable biotic and abiotic soil factors (Tripathi et al.,
2007).
Although the effects of salinity and sodicity on soil properties (Qadir et al., 2007) and crop growth has been studied widely but little is known about
their possible effects on soil microbial activities. Rapid and accurate
techniques for salinity and sodicity appraisal has now also being developed
considering the importance of the problem e.g. electromagnetic induction
(EMI) technique (Ganjegunte et al., 2014). They recorded significant
correlation between the EMI measured and laboratory analyzed saturated paste
electrical conductivity and sodium absorption ratio. Development of rapid
salinity and sodicity appraisal techniques indicates the increasing problems
of salinity worldwide. Soil microorganisms are key drivers of organic matter
decomposition (Quails and Raines, 1992), nutrient cycling, energy
transformation (Coleman et al., 1985); and formation of aggregates and
structures. They play a pivotal role in maintaining and improving soil
quality (Egamberdieva et al., 2010). Therefore, understanding of microbial
activities in salt-affected soils is of paramount importance (Singh, 2015)
from crop production point of view. Effect of salinity (electrical
conductivity) and sodicity (exchangeable sodium percentage) has been studied
by several workers and have noted both positive and negative effect on
microbial activity. Thus, reconciliation of the proper mechanism is yet to
be explained properly (Singh, 2015). Changes in soil physical processes
affect water and air movement and available water capacity (Oster and
Jaywardane, 1998), osmotic and matric potential and reduces microbial
activity (Reitz and Haynes, 2003; Sardinha et al., 2003) and inflicts an
adverse effect on plant growth and yield. These could also be due to the
direct toxic effects of salts on microbial communities (Reitz and Haynes,
2003) or vegetation (crop, grass and tree) (Wong et al., 2010), which in
turn, causes the decreased organic matter inputs (crop residue, litter and
fine roots) in the soil and, consequently, reduces the microbial activities
(Singh et al., 2015). At high soil salinity and sodicity, the availability
of organic matter and metabolic energy required for microbial assimilation
is reduced, the microbial cell lysis takes place and soil becomes poor in
microbial activities (Singh, 2015). While the effects of salinity under high
pH soils of arid and semi-arid region (e.g. soil with secondary salinization
or irrigation induced salinity) on soil physical and chemical properties are
very well documented (Keren, 2000), the information on soil biological
activity are limited (Reitz and Haynes, 2003) and less intensively studied
in soils with high salinity and low soil pH (e.g. coastal saline soils). In
the recently reported review by Singh (2015) on effect of soil salinity and
sodicity on microbial activities extensively reviews the saline and sodic
soils of the arid and semi-arid region. The effects of salinity or sodicity
on microbial activities in coastal saline soils of the world is relatively
less investigated and reported. The effects of salinity under low soil pH on
microbial activity in terms of soil microbial biomass (MBC), MBC as
a fraction of soil organic carbon (SOC) (MBC/SOC), basal soil respiration
(BSR), metabolic quotient (qCO2), enzyme activities–dehydrogenase,
acid and alkaline phosphatase and urease are still poorly understood (Iwai
et al., 2012). These parameters also act as a sensitive indicators of soil
quality changes due to management or environmental stress (Powlson et al.,
1987; Reitz and Haynes, 2003; Egamberdieva et al., 2010). Reduced microbial
activities like MBC, soil microbial biomass nitrogen, BSR, fluoroscein
diacetate hydrolyzing and other enzyme activities due in response to
salinity has been reported in literature (Reitz and Haynes, 2003; Tripathi et al., 2006; Shah and Shah, 2011; Iwai et al., 2012). Management studies on
saline soils reveal that organic materials or amendments could improve the
physical, chemical and biological properties of the degraded soils (e.g.
saline soils) with poor soil fertility (Srivastava et al., 2014; Wu et al.,
2014). Over past few centuries, site-specific remediation technologies for
managing salt affected soils have been developed (Mao et al., 2014). These
method include leaching, tillage management, application of organic and
chemical amendments, physical land modifications etc. Novel products like
bio-augmented organic amendments (vermicompost – pre-enriched with plant
growth promoting fungi mixed with pressmud and Azadirechta indica seed cake) found to boost
the wheat yield and soil enzyme activities under sodic soils (Srivastava et al., 2014). Singh et al. (2014) showed that continuous tillage and cropping
on sodic soils is useful to restore them physically and chemically. The
application of chemical amendments like gypsum in loamy sand, sandy loam and
clay loam at 25, 50 and 75 % gypsum requirement rate proved as
cost-effective technique to reduce salinity levels in sodic soils (Ahmad et al., 2015). Oo et al. (2013) observed that application of compost and
vermicompost as a soil conditioner alleviates the salinity stress and
improves the maize productivity. Thus, there are numerous management
strategies to manage salt-affected soils of the world. But, to decide the
location specific remediation strategy, accurate assessment of the salt
affected soils is very important.
Considering the limited research available on the effect of coastal soil
salinity on microbial activities and need of sustainable management of these
soils, the present investigation was carried out to generate primary
information on microbial activities in coastal saline soils. There are no
such reports available with reference to west coast of India. The objective
of the study was to study the effect of salinity in three different seasons–monsoon, post–monsoon and pre–monsoon season on MBC, MBC/SOC, basal soil
respiration (BSR), metabolic quotient (qCO2) and enzyme activities–dehydrogenase, phosphatase and urease. The outcomes of the study would be
useful to develop the countermeasures for sustainable management of these
soils.
Results and discussion
Physico-chemical properties of soil
As already mentioned in the section materials and methods, the soils were
categorized in four groups based on the EC in the rainy season. The EC of
the soils collected ranged from 0.81 to 8.83 dS m-1. The three levels
of salinity exhibited significant (p<0.01) variations in EC in all
three seasons. During monsoon season, strongly saline soils had EC as high
as 5.59 dS m-1 while non-saline soils had 0.81 dS m-1. Salinity of
5.49 dS m-1 in the highest rainfall month (July, Fig. 1a and b) is
a considerable level to limit the crop production. Similar sort of trend of EC
was recorded during the post-monsoon and pre-monsoon season as well. The EC
also varied significantly (p<0.01) among monsoon, post-monsoon and
pre-monsoon and had average values of 2.96, 4.90 and 6.31 dS m-1. Very
high rainfall and low evaporation rate causes washing of salts with
rainwater and reduces the salinity level during monsoon season (Fig. 1a, b). Thus, rainfall and evaporation are two major factors besides salt
water intrusion monitoring the soil salinity in these areas. The variations
in soil pH with different salinity levels and seasons were non-significant.
But, important to note is that, the soil pH was less than 6.11 (ranged from
4.66 to 6.11). The soil reaction exhibited by soils was acidic at all the
sites during all the seasons. The soils originally are lateritic type and
experience salt accumulation due to natural and anthropogenic activities.
Thus, salinity in these soils exists under low pH unlike secondary soil
salinity associated with high soil pH in arid and semi-arid parts of the
country. Existence of salinity under low soil pH or acidic soil reaction is
an interesting and rare situation. Little attention has been given on
investigation on these soils and scanty literature is available. The pattern
of the SOC at different salinity levels and among different seasons was
interesting and significant (p<0.01) (Table 2). In all the seasons,
the highest SOC was recorded in non-saline soils (5.05–16.21 g kg-1),
whereas it was lowest in the strongly saline soils (2.85–5.62 g kg-1).
Highest average SOC was observed in the pre-monsoon (10.27 g kg-1)
followed by post-monsoon (7.20 g kg-1) and it was lowest in monsoon
(3.93 g kg-1). In general, the soil organic carbon decreased with
increasing levels of salinity within the same season. The higher soil
organic carbon in post-monsoon season might be due to the decomposition and
mineralization of the left out residues of rice crop. Decreased
decomposition and mineralization of the crop residues due to submergence in
monsoon could be a probable reason for the lowest soil organic carbon in
monsoon season. Reduced crop growth, C input, gradual dispersion of the soil
aggregates leaving organic matter unprotected and susceptible to degradation
could be the apt reasons for low SOC at high salinity levels (Egamberdieva
et al., 2010). Under salt affected soil conditions the available soil organic
matter is dispersed and not protected physically and undergoes higher
biological mineralization (Abiven et al., 2009; Wiesmier et al., 2012) and
moreover higher accessibility of the free organic matter to microbial decay
further reduces the fertility and physical stability of the soils (Neson and
Oades, 1998; Wong et al., 2010; Fterich et al., 2014). This way the
availability of the organic matter and metabolic energy for microbial
assimilation further reduces and results in to poor microbial activity
(Singh, 2015).
Cationic composition of soils
The cationic composition of the soil depended significantly (p<0.01) on the salinity levels and seasons (Table 3). In general, the
concentration of exchangeable Na was next to Ca and it was higher than that
of exchangeable K and Mg. Concentrations of all the cations studied were
highest during pre-monsoon season followed by post-monsoon and lowest in
monsoon. High concentration of Na in the coastal saline soils of India
causes poor physical and chemical properties, impeded water infiltration and
water availability (Dhanushkodi and Subrahamaniyan, 2012). This causes due
to swelling, slaking, dispersion of clays and degraded soil structure
(Biovin et al., 2004; Tejada and Gonzalez, 2005; Iwai et al., 2012). Thus,
excess of Na in the soils prevailing in all the seasons is a matter of
concern for crop production in these soils.
Microbial activity
The microbial activity in soils can be determined from the soil organic
matter decomposition (Reitz and Haynes, 2003), carbon dioxide emission, soil
microbial biomass and MBC/SOC (Wong et al., 2010; Balota et al., 2013) and
nutrient release or mineralization (Nelson et al., 1998). These are
important parameters to explain various stresses on the microbial activities
(Singh, 2015). The data on the effect of salinity levels and microbial
activity is presented in Table 4. The MBC, MBC/SOC, BSR and qCO2
depended significantly (p<0.01) on the salinity levels and seasons
(Table 5). The MBC, MBC/SOC and BSR reduced significantly with increasing
salinity level in all the seasons, whereas qCO2 showed an increasing
trend. The lowest MBC (21.1 mgkg-1) was recorded in
strongly saline soils during pre–monsoon season, whereas highest was
recorded in non-saline soils during monsoon (112.7 mgkg-1) and
post-monsoon (112.8 mgkg-1). In the present study,
the MBC of weakly, moderately and strongly saline soils were higher in monsoon,
followed by post-monsoon and it was lowest in pre-monsoon season. Low
organic matter and high salinity (e.g. strongly saline soils group in the
present study) creates undesirable environment for the microbial community.
Besides the physical properties of the soil, the biological properties
serves as a better indicator of soil quality and one such biological
properties is MBC (Mahajan et al., 2015). Inverse relationship of the
salinity with MBC, during all the seasons, is in line with those reported by
Tripathi et al. (2006), Iwai et al. (2012), and Mahajan et al. (2015).
The range of the MBC in the present investigation is 21.1 to 112.8 mgkg-1. The MBC reported in by researchers in non-saline soils is
100 to 600 mgkg-1 soil (Powlson et al., 1987; Anderson et al., 2003;
Shah and Shah, 2011) and in saline soils it was as low as 125 mgkg-1
soil (Tripathi et al., 2006), 47.3 mgkg-1 soil (Yuan et al., 2007),
40.5 mgkg-1 soil (Iwai et al., 2012), 158 mgkg-1 (Sardinha
et al., 2003), 147 mgkg-1 (Shah and Shah, 2003), etc. Singh et al. (2012), in the field experiments, observed reduction in the MBC and BSR
in sodic soils with 95 % ESP whereas the substantial reclamation using
afforestation improved the MBC and BSR. The toxic effect of the salinity on
C might be due depressive effect of Na on the microorganisms (Reitz and
Haynes, 2003; Egamberdieva et al., 2010; Ndour et al., 2008). It is not only
the degraded environments like salinity but also mine and forest fires
affected areas and land use changes affect the soil microbial activity
significantly. The forest fires has found to slowdown the recovery of the
soil organic matter related properties, nutrient availability and soil
enzyme activities (Guenon et al., 2013). Under such environments, the
vegetation recovery normalizes the post fire soil microbial processes (Hedo
et al., 2015). Vegetation with the fast growing trees improves the soil
microbial community composition through the improvement in the soil organic
carbon (Wu et al., 2013). Wu et al. (2013) recommended that the soil
microbial community composition should always be considered for the large
scale management of the degraded lands. The soil microbial variables proved
to be strong indicators of soil sustainability (Tejada and Benitez, 2014)
when addition of organic matter (crushed corn straw and waste) was tested to
affect soil microbial activity. Besides the salinity, other degraded
environment also have recorded poor soil microbial activity in low organic
matter content soils. Lower C substrate availability, desiccation due to dry
weather (Van Gestel et al., 1992) and high salinity also attributes to the
reduction in MBC.
In all the seasons, a significant (p<0.01) negative relation
between salinity levels and MBC/SOC was observed. The order of the mean
MBC/SOC in different salinity groups was as: strongly saline
(0.59 %) > moderately saline (0.91 %) > weakly saline
(1.02 %) > non-saline (1.35 %) soils. The mean MBC/SOC of
non-saline soil was 2.28 times higher than that of strongly saline soils.
The order of MBC/SOC was observed as post-monsoon (1.25 %) >
monsoon (0.87 %) > during pre-monsoon (0.79 %) season. The
results clearly indicated the detrimental effect of the salinity on
microbial activities. The significant reduction of MBC/SOC due to high
salinity also recorded by Egamberdieva et al. (2010) and Mahajan et al.
(2015), may be related to microbial stress by higher organic consumption per
unit MBC to maintain the cell integrity and release the Na+.
These both processes consume and require metabolic energy (Utsugi et al.,
1998). The values of MBC/SOC in the strongly saline soils (0.59 %) are
close and in line with those reported by Sardinha et al. (2003) under
strong saline soils (0.50 %). The adverse effect of the soluble salts and
osmotic stress could have caused inhibition of the C assimilation by
microorganisms (Mahajan et al., 2015).
On the contrary to the MBC and MBC/SOC, the qCO2 increased significantly
(p<0.05) with the increasing levels of salinity. The qCO2 index
establishes that MBC becomes more efficient in utilizing the resource
available (Garcia-Orenes et al., 2010). The order of season for qCO2 was
observed as: pre-monsoon (0.43 mgCO2–C day-1g-1MBC)
> post-monsoon (0.43 mgCO2–C day-1g-1MBC)
> monsoon (0.43 mgCO2–C day-1g-1MBC). The
qCO2 of strongly saline soils was 2.4 times higher than that of
non-saline soils. The occurrence of higher qCO2 with high salinity
levels has been reported in literature by researcher (Mahajan et al., 2015; Iwai et al., 2012; Tripathi et al., 2007) and our observations are in
line with them. Chowdhury et al. (2011) and Setia et al. (2011) reported
the decrease in BSR with increasing levels of salinity and this trend was
similar even after addition of organic matter. This explains the magnitude
of the salinity effect on microbial activity. The qCO2 is an indicator
of the environmental stress on the microbial community (Reitz and Haynes,
2003; Rasul et al., 2006; Iwai et al., 2012; Mahajan et al., 2015). The
reduced qCO2 in high salinity levels indicates the lower microbial
functioning efficiency (Anderson and Domsch, 1989) and it also implies that
relatively high C has to be allocated by the microorganisms for maintenance
than growth. The native microbial population could be less able to
incorporate the soil C for their proliferation (Garcia-Orenes et al., 2010).
Physiologically more active population of the microorganisms that used
substrate less efficiently was observed by Wichern et al. (2006) under high
osmotic stress situation. The higher energy requirement of the unit
microbial cell for selective Na exclusion might also reflect the high
qCO2 in the present study (Wichern et al., 2006). Fterich et al.
(2014) reported the high carbon use efficiency in terms of qCO2 values
in different textured soils cultivated with Acacia tortilis. Vegetating the degraded lands
with appropriate crops could be one of the possible solutions to manage
them.
Soil enzyme activities
Soil enzymes are often considered as sensitive indicators of changes in soil
due to different stresses (Schimdt et al., 2011; Nannipieri et al., 2012).
Like MBC, soil enzyme activities significantly (p<0.01) reduced
with increasing levels of salinity (Table 5). In general, the soil enzyme
activities–dehydrogenase and phosphatase decreased as monsoon
> post-monsoon > pre-monsoon, whereas the urease
activity was observed as post-monsoon > monsoon >
pre-monsoon. The dehydrogenase enzyme activity was significantly highest in
non-saline soils, but it varied non-significantly in rest three salinity
levels in all the seasons. The mean dehydrogenase activity in non-saline
soils (26.0 mg TPF kg-1 h-1) was about 4.5 times that in
strongly saline soils (5.73 mg TPF kg-1 h-1). Almost similar
sort of trend was observed for phosphatase enzyme activity. As mentioned
above, the urease activity was higher in the post-monsoon season. This could
be due to the higher availability of the decomposing substrate during the
post-monsoon season. The urease enzyme activity in the monsoon and post-monsoon season was 2.34 and 2.84 times higher than that in the pre-monsoon
season. The results of the present investigation revealed the inhibitory
effect of salinity on soil enzyme activities (Table 5). The magnitude of the
enzyme activity however was lower compared to the one observed in other
soils (Dick et al., 1996; Tripathi et al., 2007). The dehydrogenase activity
reported in the present investigation was found to be lower during the
monsoon season (5.50–78.3 µg TPF g-1 day-1) than those
(213.6–312 µg TPF g-1 day-1) reported by Tripathi et
al. (2007) during similar season in coastal saline region of the Bay of
Bengal, Sundarbans, India. But, the ranges for urease and phosphatase were
found more or less similar. The better dehydrogenase activity in the normal
(e.g. non-saline soils in the present study) could be attributed to higher
organic substrates and MBC. Higher available organic substrate could have
promoted the activity of the indigenous microorganisms and thereby the
dehydrogenase enzyme (Hedo et al., 2015). The dehydrogenase activity is
often considered as a sensitive indicator of the soil quality. Decreasing
soil enzyme activities with increasing salinity might be due to increased
osmotic stress on microorganisms (Frankenberger and Bingham, 1982). This
shows lesser ability of the soils to mineralize essential nutrients and make
them available to plants. Salinity in these soils limits microbial growth,
soil organic matter decomposition and nutrient transformation. To overcome
salinity barriers to restore microbial growth and their activities suitable
ameliorative measure like organic matter addition needs to be developed in
these soils (Tripathi et al., 2007). Increased availability of substrate due
to organic matter addition might counteract the adverse effect of salinity
(Wichern et al., 2006; Mavi and Marschner, 2013). Cultivating degraded soils
with right plants and addition of organic matter has proved to improve the
soil quality indicators like enzyme activities (dehydrogenase, phophphatase,
β-glucosidase, urease, etc.) (Flerich et al., 2014, Hedo et al.,
2015). Hedo et al. (2015) attributed the better soil microbial activity in
recovery of degraded land (fire affected lands) to higher organic matter
concentrations, which can act as energy source to the microorganisms. Soil
salinity affects the soil enzymes by their direct effect on enzyme
production and by making structural changes in enzymes due to anionic
movement and reduced availability of organic matter (Frankenberger and
Bingham, 1982; Amato and Ladd, 1992; Yao et al., 2009; Singh, 2015).
Although the soil enzymes have specific activity with respect to salinity,
all three soil enzymes studied had depressive effect due to salinity.
Based on the results of the present study, the future areas of research or
remediation strategies for management of these soils could be (1) use of the
salinity tolerant microorganisms having plant growth promoting activities,
(2) use of organic and chemical amendments to alleviate the salinity stress,
(3) use of salinity resistant varieties of different crops, (4) use of
integrated nutrient management system to promote plant growth, etc.