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Article

Relative Growth Rate and Specific Absorption Rate of Nutrients in Lactuca sativa L. Under Secondary Paper Sludge Application and Soil Contamination with Lead

by
Elena Ikkonen
* and
Marija Yurkevich
Department of Multidisciplinary Scientific Research, Karelian Research Center, Russian Academy of Sciences, Petrozavodsk 185910, Russia
*
Author to whom correspondence should be addressed.
Agriculture 2025, 15(14), 1541; https://doi.org/10.3390/agriculture15141541
Submission received: 13 May 2025 / Revised: 14 July 2025 / Accepted: 16 July 2025 / Published: 17 July 2025
(This article belongs to the Section Agricultural Soils)
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Abstract

Cost-effective methods for improving soil fertility and mitigating the negative impact of heavy metal contamination in agricultural soils are currently under investigation. This study aimed to evaluate the impact of soil lead (Pb) contamination and the application of secondary pulp and paper mill sludge on the relative growth rate (RGR) and its determinants, as well as the specific absorption rate (SAR) of nutrients of Lactuca sativa L. For the 46-day pot experiment, which was carried out in 2022 under controlled conditions at the Karelian Research Centre of RAS, sandy loam soil was used, to which Pb was added at rates of 0, 50, and 250 mg Pb(NO3)2 kg−1. Secondary sludge was applied with each watering at concentrations of 0%, 20%, and 40%. RGR values varied significantly, primarily due to changes in net assimilation rate (NAR) rather than specific leaf area. Positive relationships were found between RGR and NAR, and RGR and SAR of nitrogen and phosphorus, but not potassium. Sludge applications can stimulate NAR at early stages of plant growth. For plants grown on soil with the highest Pb concentration studied, secondary sludge reduced root lead content by an average of 35%. Soil contamination with lead increased nutrient SAR by 79 and 39% when applied as 20 and 40% sludge, respectively, while 40% sludge increased nitrogen SAR by 51% but did not change phosphorus and potassium SAR. A sludge-mediated reduction in root Pb content and an increase in NAR suggest that secondary paper sludge may contribute to the remediation of Pb-contaminated soils and reduce the toxicity of heavy metals to plants. The results may help in finding new ways to manage soil fertility, especially for contaminated soils.

1. Introduction

To increase crop yields, agricultural soils with low fertility are typically amended with costly commercial fertilizers. Alternative, cost-effective methods to improve soil fertility and reduce production costs are currently under investigation [1,2]. The possibility of using pulp and paper mill sludges in agriculture as an alternative source of soil nutrients is also under discussion [3,4,5]. Secondary sludge is generated through the biological treatment of primary sludge, during which microorganisms break down dissolved organic matter [6]. Nitrogen and phosphorus are added to stimulate microbial activity during treatment, resulting in increased concentrations of these nutrients in the secondary sludge. Secondary sludge also contains more organic matter [7] and has a lower carbon-to-nitrogen (C:N) ratio [8] than primary sludge. The application of secondary sludge has been shown to increase soil pH and the concentrations of carbon (C), nitrogen (N), potassium (K), and phosphorus (P), as well as plant nitrogen uptake, particularly in wheat [9]. The beneficial effects of using of pulp and paper mill sludge have been shown to improve crop growth and yield [9]. A sludge-mediated increase in crop yield can be associated with an enhanced plant physiological state [5], connected with an improvement in soil physical and chemical properties [10,11], including increased nutrient levels [9].
Nutrient availability directly affects plant growth and yield [12], as macronutrients are essential components of biochemical compounds and physiological processes [13,14]. It has been suggested that nutrient status more directly influences plant growth rate than biomass accumulation, which is a result of growth rate over time [15]. For agricultural crops, relative growth rate (RGR) is one of the most important and widely used growth analysis indices closely related to plant productivity [16]. This index is defined as the rate of accumulation of new biomass per unit of existing biomass. A close relationship between RGR and leaf nitrogen content has recently been shown [17], but knowledge about the effect of other macronutrients such as phosphorus and potassium on RGR is limited.
Lettuce (Lactuca sativa L.) is a species widely cultivated throughout the world. Lettuce typically responds to fertilizers [18], and a positive response of the main physiological processes of plants to the secondary sludge application was found [5]. However, limited information is available on how sludge application influences macronutrient accumulation and its relationship with plant growth rate.
Unfortunately, the possibility of contamination of agricultural soils with heavy metal and metalloids including lead exists throughout the world [19,20]. Natural sources, anthropogenic activities, and atmospheric deposition have been identified as potential sources of heavy metal and metalloids, with the primary role of human contribution to soil contamination [21]. Industrial production and agricultural practices such as fertilization, pesticide use, and wastewater irrigation can lead to the accumulation of high concentrations of metals in soils, posing a serious threat to food production and human health [22].
High soil Pb content has a negative impact on the morphological, physiological, and biochemical parameters of plants, causing a decrease in their growth and, consequently, a limitation of productivity and yield [23,24]. Pulp and paper mill sludges can contain up to 50% organic matter [7], which largely controls the mobility of metal ions in soils [25]. Although paper sludge may contain traces of potentially toxic elements, their concentrations are generally low and similar to those in organic fertilizers [8]. It was therefore concluded that the application of paper sludge to soil at rates consistent with agricultural practice does not pose a significant risk of heavy metal accumulation in plants [8]. The positive effects of pulp and paper sludges as a rich source of organic substrates on soil properties have been shown [12,26,27]. Moreover, a number of studies have shown that the use of paper sludge in agriculture increases the availability of nutrients to plants and the activity of microorganisms and reduces the mobility of toxic elements [6,7,28]. Secondary sludge may act as an effective biosorbent for heavy metal and metalloids, potentially reducing their uptake by plants. Consequently, sludge application might alleviate the growth-limiting effects of heavy metal contamination. Thus, it can be assumed that sludge applications can reduce the limiting effect of heavy metal and metalloids on plant growth processes. This study aimed to evaluate the effect of secondary sludge on growth rate, nutrient accumulation in L. sativa, as well as the relation between these parameters. Furthermore, the novelty of this study was in the evaluation of the effect of soil lead content on plant growth rate and the associated net uptake rate to understand whether the application of secondary sludge affects the response of lettuce to heavy metals. The results can be useful for finding new ways to manage the fertility of soils with low nutrient content and contaminated with heavy metals, as they aim to increase crop yields and reduce production costs.

2. Materials and Methods

2.1. Soil Preparation and Plant Treatment

Sandy loam soil with low natural fertility was used for the pot experiment. The nitrogen content in the soil was 0.39%, phosphorus and potassium—0.16%, which indicates its low fertility. The content of Mg and Ca was 0.20 and 1.95 g kg−1 accordingly, and the natural Pb content was 0.13 mg kg−1 [29]. The humus content of the collected soil was 0.7%, and pH was 5.46. The soil was collected from a field site of the research station of the Karelian Scientific Centre of the Russian Academy of Sciences (61°84′71.23″ N, 33°21′12.28″ W) in 2022. The soil was air-dried and sifted through a sieve with a mesh size of 2 mm, and nitrogen, phosphorus, and potassium were added at a concentration of 150 mg kg−1. The soil was then amended with Pb(NO3)2 at concentrations of 0, 50, or 250 mg kg−1, designed as 0 Pb, 50 Pb, or 250 Pb, respectively. The concentrations studied were selected in a preliminary experiment. The soil substrates were incubated for 14 days and placed in 0.8 L plastic pots to achieve a soil density of 1.4 g cm−3.
Seeds of Lactuca sativa L. (var. Medvezhie ushko) were sown in pots (one seed per pot) with prepared soil. The seedlings were grown under controlled conditions of a day/night temperature of 23/20 °C, a PPFD of 250 µmol m−2 s−1, and a 16 h photoperiod. The pots were watered every two days with 0, 20, and 40% solutions of secondary mill sludge, referred to as the 0%, 20%, and 40% treatments, respectively. The sludge was collected from a pulp and paper mill located in the northwestern region of Russia. The secondary sludge used in this study contained 238, 9, and 64 mg L−1 of N, K, and P, respectively, and 47, 233, and 22 mg L−1 of Na, Ca, and Mg, respectively. The content of lead, cadmium, mercury, and arsenic in the sludge under study was 0.4, 0.02, 0.002, and 0.06 mg L−1, respectively. The carbon content of the sludge was 56.7%, and pH was 7.16. Thus, the randomized study design included three soil Pb levels (0, 50, or 250 mg Pb(NO3)2 kg−1) and three treatments with sludge. Each treatment included 16 pots. The experiment lasted for 46 days, during which 0, 139, or 278 mL of sludge was added to 1 L of soil for treatments of 0%, 20%, or 40%, respectively.

2.2. Plant Growth Measurement

Four plants of each treatment were collected at 17, 21, 34, and 46 days of age; washed; separated into shoots and roots; dried at 70 °C; and weighed. The leaf area of plants was measured by scanning the leaves and using AreaS software (AreaS software, v. 2.1, SGU, Samara, Russia).
The absolute growth rate (AGR) of roots and shoots was calculated as AGR = (W2 − W1)/(t2 − t1), where W1 and W2 are the dry biomass at times t2 and t1. The relative growth rate (RGR) was expressed as RGR = (lnW2 − lnW1)/(t2 − t1). The net assimilation rate (NAR) of intact plants was defined as NAR = AGR (lnA2 − lnA1)/(A2 − A1), where A2 and A1 are leaf area at times t2 and t1. The value of specific leaf area (SLA) was determined by dividing the leaf area by the leaf mass.

2.3. Chemical Analyses

The mass-based Pb content was determined by spectrophotometric atomic absorption (Shimadzu AA-7000, Kyoto, Japan). Spectrophotometric atomic absorption (Shimadzu AA-7000, Kyoto, Japan) was used to determine the Pb content in the plant shoots and roots. Mineralization was carried out with an acid mixture in a Berghof Speedwave system (MWS four digestion system, Enningen unter Achalm, Germany). To determine the content of N and P, spectrophotometric and flame photometric methods were used (SF 2000 OKB Spectrum, St. Petersburg, Russia). Potassium content was determined using a flame atomic absorption spectrophotometer (Shimadzu AA-6800, Kyoto, Japan). The chemical analyses were carried out in the analytical laboratory of the Forest Institute of KRC of RAS.
According to [30], the specific absorption rate (SAR) was defined as the amount of nutrients absorbed by a unit of root biomass.

2.4. Statistical Analysis

The data are shown as mean ± SE with four replicates for the plant biomass and three replicates for chemical parameters. To assess significant differences between mean values, the LSD test was used at p < 0.05 level (Statistica software, v. 8.0.550.0, StatSoft, Inc., Tulsa, OK, USA). The two-way ANOVA test was used to determine the effect of sludge application and soil Pb, as well as their interaction on plant parameters. A linear function was used to describe the relation between the parameters.

3. Results

3.1. Plant Growth Parameters

No significant effect (p > 0.05) of soil Pb on the accumulation of dry mass of shoots and roots of L. sativa was found on the 17th and 21st days after sowing (Table 1). For the 34-day-old plants grown without sludge treatment, an increase in soil Pb content caused a decrease in both shoot and root biomass, but this trend was not significant for 46-day-old plants. For untreated 21- and 34-day-old plants, the leaf area values tended to decrease with increasing soil lead content. The ANOVA test did not reveal a significant effect (p > 0.05) of soil lead on the leaf area of 46-day-old plants.
Regardless of Pb content, no significant differences were found in the shoot dry weight between secondary sludge treatments in 17- and 21-day-old plants, as well as in the root dry weight in 21-day-old plants (Table 1). With one exception, sludge application increased shoot dry mass accumulation in 21-, 34-, and 46-day plants, but not in 17-day-old plants. On the 17th day after sowing, sludge application increased the accumulation of root mass of L. sativa grown under 0 and 250 mg Pb(NO3)2 content in the soil. The sludge application resulted in increased root biomass accumulation regardless of soil lead content, but not all increases were confirmed by statistical testing. No strong and clear effect of sludge treatment on leaf area values was observed in this study. The 17-day-old plants had the highest SLA values regardless of soil Pb content and sludge dose (Table 1). For the 46-day-old plants, sludge application decreased SLA under soil Pb contents of 0 and 250 mg Pb(NO3)2 kg−1.

3.2. Growth Rate Parameters

During the initial period of development (17–21 days after sowing), L. sativa had the lowest AGR, with the values did not exceeding 0.01 g d−1 for both shoots and roots (Figure 1). However, as the seedlings evolved, AGR increased significantly. Among the plants untreated with sludge, soil contamination with Pb resulted in decreased AGR (p ˂ 0.05). If in the period of 21–34 days after sowing, the sludge application initiated an increase in the AGR values both in shoots and roots, regardless of the Pb content in the soil, then in the period of 34–46 days after sowing, this effect was observed only for the shoots of plants growing in Pb-free soil (Figure 1a,b).
Table 1. Shoot and root dry weight, leaf area, and specific leaf area (SLA) in L. sativa plants grown on the soil containing 0, 50, or 250 mg Pb(NO3)2 kg−1 and watered with 0, 20, or 40% secondary pulp and paper mill sludge at 17, 21, 34, and 46 days after sowing.
Table 1. Shoot and root dry weight, leaf area, and specific leaf area (SLA) in L. sativa plants grown on the soil containing 0, 50, or 250 mg Pb(NO3)2 kg−1 and watered with 0, 20, or 40% secondary pulp and paper mill sludge at 17, 21, 34, and 46 days after sowing.
Parameter0 mg Pb(NO3)2 kg−150 mg Pb(NO3)2 kg−1250 mg Pb(NO3)2 kg−1
0%20%40%0%20%40%0%20%40%
Shoot dry weight, g
17 days after sowing0.01 ± 0.00 a0.01 ± 0.00 a0.03 ± 0.01 a0.02 ± 0.01 a0.02 ± 0.01 a0.02 ± 0.00 a0.01 ± 0.00 a0.03 ± 0.01 a0.03 ± 0.01 a
21 days after sowing0.03 ± 0.01 b0.03 ± 0.02 ab0.06 ± 0.02 a0.03 ± 0.01 b0.06 ± 0.02 a0.03 ± 0.00 b0.03 ± 0.01 b0.05 ± 0.02 a0.05 ± 0.02 a
34 days after sowing0.56 ± 0.06 b1.04 ± 0.19 a0.83 ± 0.1 a0.29 ± 0.03 c0.52 ± 0.06 b0.71 ± 0.09 a0.34 ± 0.06 c0.41 ± 0.04 bc0.66 ± 0.09 ab
46 days after sowing0.97 ± 0.24 b1.33 ± 0.15 ab1.62 ± 0.11 a1.46 ± 0.24 a1.47 ± 0.07 a1.37 ± 0.08 a1.06 ± 0.06 b1.11 ± 0.16 b1.59 ± 0.18 a
Root dry weight, g
17 days after sowing0.002 ± 0.000 b0.003 ± 0.001 ab0.004 ± 0.001 a0.003 ± 0.002 ab0.003 ± 0.002 a0.002 ± 0.000 a0.002 ± 0.000 b0.003 ± 0.001 ab0.004 ± 0.001 a
21 days after sowing0.006 ± 0.001 a0.007 ± 0.003 a0.011 ± 0.003 a0.008 ± 0.005 a0.011 ± 0.005 a0.007 ± 0.010 a0.010 ± 0.002 a0.012 ± 0.005 a0.010 ± 0.003 a
34 days after sowing0.192 ± 0.027 b0.306 ± 0.130 a0.280 ± 0.045 a0.058 ± 0.014 c0.147 ± 0.029 b0.167 ± 0.023 b0.071 ± 0.021 c0.114 ± 0.014 b0.163 ± 0.027 b
46 days after sowing0.510 ± 0.131 bcd0.606 ± 0.066 ab0.676 ± 0.065 a0.447 ± 0.035 cd0.524 ± 0.086 b0.502 ± 0.001 c0.405 ± 0.154 c0.410 ± 0.057 d0.515 ± 0.077 bc
Leaf area, cm2
21 days after sowing53 ± 19 a23 ± 11 ab29 ± 9 ab18 ± 4 b26 ± 10 ab21 ± 3 ab18 ± 3 b26 ± 10 ab27 ± 6 ab
34 days after sowing114 ± 7 bc124 ± 37 ab136 ± 20 ab110 ± 48 abc113 ± 25 b87 ± 8 cd78 ± 18 d81 ± 12 d152 ± 8 a
46 days after sowing288 ± 39 ab302 ± 20 ab320 ± 13 a345 ± 37 a335 ± 11 a300 ± 16 ab267 ± 24 b419 ± 120 a323 ± 40 ab
SLA, m2 kg−1
21 days after sowing81 ± 5 a68 ± 7 b52 ± 6 c52 ± 4 c44 ± 2 d64 ± 5 b52 ± 4 c53 ± 3 c55 ± 4 bc
34 days after sowing20 ± 4 c22 ± 3 c26 ± 4 bc39 ± 4 a21 ± 3 c26 ± 2 b23 ± 3 bc20 ± 2 c23 ± 1 bc
46 days after sowing28 ± 3 a23 ± 3 bc20 ± 1 c24 ± 2 bc23 ± 3 bc22 ± 1 c25 ± 2 ab21 ± 2 c20 ± 1 c
Different letters indicate significant differences between the means.
In contrast to AGR, the RGR values significantly (p ˂ 0.05) decreased with increasing plant age, which was particularly noticeable for the roots (Figure 1c,d). For plants not treated with sludge, soil contamination with Pb significantly (p ˂ 0.05) affected the RGR of roots in both periods of 17–21 and 21–34 days, but this trend was not expressed for plant shoots. The effect of secondary sludge application on the RGR of shoots or roots varied significantly depending on plant age and soil heavy metal content. A significant (p ˂ 0.05) positive effect of sludge application on the RGR values was found only for 50 Pb 17–34-day-old plants; in other cases, the effect was negative or neutral.

3.3. Calculated Net Assimilation Rate

Significant differences in NAR were observed between plants of different ages, with NAR values being higher at earlier growth stages (Figure 2). On average, over the 21–46-day period for all sludge treatments, NAR values did not differ between 0 Pb and 50 PB plants (5.4 ± 0.6 and 5.6 ± 0.7 g m−2 d−1, respectively) but were higher than for 250 PB ones (4.7 ± 0.5 g m−2 d−1). A significant positive effect of sludge application on NAR was revealed only for 0 Pb and 50 PB plants during 21–34 days after sowing.

3.4. Pb Content in Shoots and Roots of Seedling

Regardless of the Pb rate used in this study, the Pb content in the roots was significantly higher than in the shoots (Table 2). Pb content increased in both the shoots and roots, following the increase in Pb content in the soil. The use of sludge significantly reduced the Pb content only in the shoots of 50 Pb seedlings 46 days after sowing and in the roots of 250 Pb plants in both measurement periods.

3.5. Macroelement Content in Shoots and Roots of L. sativa Seedling

Regarding the N content in both shoots and roots, no significant effect of soil Pb content (p ˃ 0.05) was found for L. sativa without sludge treatment (Figure 3a). The application of sludge at a dose of 20% significantly increased the nitrogen content in both shoots and roots of 250 Pb plants, as well as in the roots of 0 Pb ones when plants were treated with 40% sludge solution.
For the plant shoots, no significant differences in the P content were found between the secondary sludge treatments and the Pb dose used in this study (Figure 3b). The phosphorus concentration in the roots of 50 Pb plants grown without sludge treatments was significantly higher than that of 0 Pb and 250 Pb plants. No significant differences in the P content were observed among all sludge treatments at different soil Pb contents.
In both shoots and roots, K concentration tended to increase following increases in soil Pb content (Figure 3c). Sludge application resulted in a decrease in the potassium content in the shoots of both 50 Pb and 250 Pb plants, as well as in the roots of 250 Pb ones.

3.6. Relationship Between NAR and Macronutrient Content

For seedling shoots, the NAR values were positively associated with N and P content (Figure 4). No strong association was found between K content and NAR.

3.7. Specific Absorption Rate of Nitrogen, Phosphorus, and Potassium

For untreated L. sativa, soil Pb contamination increased the SAR of nitrogen in 50 Pb and 250 Pb plants, the SAR of phosphorus in 250 Pb plants, and the SAR of potassium in 50 Pb plants (Figure 5). Among the plants grown on Pb-free soil, sludge application increased the SAR of N but had no effect on the SAR of P and K. Sludge application caused an increase in the SAR of N in 0 Pb and 250 Pb plants and a decrease in the SAR of P in 250 Pb plants and the SAR of K in 50 Pb plants.

3.8. Relationship Between Relative Growth Rate (RGR) and Specific Leaf Area (SLA), Net Assimilation Rate (NAR), and Specific Absorption Rate (SAR)

Across all treatments, RGR showed no significant relationship with SLA; however, RGR showed a strong positive relationship with NAR (Figure 6). RGR was positively associated with the SAR of nitrogen and phosphorus, but not potassium.

4. Discussion

Relative growth rate is considered an important indicator of plant productivity strategy, with an important effect of RGR on plant growth and development, as well as reproduction [31]. So, knowledge of RGR is of primary importance in plant ecology and agronomy [32]. As RGR is the most used method for measuring and comparing species growth, potential assessments allow us to analyze the impact of environment and nutrition on plant growth [33]. In our study, we aimed to understand how secondary sludge application to nutrient-poor soils affects plant growth and nutrient uptake. Therefore, we quantified the effects of soil Pb on growth rate and nutrient uptake rate to understand whether plant responses to sludge are affected by soil heavy metal contamination. This study revealed a high degree of variability in RGR (Figure 1), which is consistent with results showing differences in relative growth rate between plant species from contrasting environments [34,35,36]. The temporal variability in RGR of lettuce leaves and roots found in this study confirms age-mediated changes in relative growth rate that have been well documented [16,37]. The observed decrease in RGR as the plants aged can be explained by ontogenetic changes and higher allocation to low-efficiency tissues [16,38], or temporal variation in NAR [39].
On average, for all sludge treatments, soil contamination with Pb negatively affected the RGR of L. sativa during about the first month of growth. Subsequently, plants grown on Pb-rich soil increased RGR compared to their counterparts grown on Pb-free soil. This could be due to certain acclimatization adjustments that occurred during growth under stressful conditions of exposure to the heavy metal. Secondary sludge application affected RGR more in leaves than in roots, but there was no general pattern of sludge-mediated changes in RGR for the plants grown on the soils with different contents of Pb (Figure 1). While secondary sludge did not affect the relative growth rate in the leaves of Pb-free soil plants, it increased the RGR in 50 Pb plants and decreased the RGR in 250 Pb plants.
RGR variability is closely related to the physiological and morphological characteristics of plant [40]. To increase productivity and potential RGR, plants need to adjust their morphological and physiological traits in response to changing environments. A number of studies highlight the important role of such morphological characteristics as specific leaf area (SLA) in enhancing plant performance [34,35,37,41]. Other studies point to the priority of physiological components such as net assimilation rate (NAR) [16,42]. However, it has been shown that the predominant role of SLA or NAR in modifying growth rate may depend on plant growth conditions such as temperature [33] and light [32,43]. Our study revealed the high variability of both SLA and NAR of lettuce plants depending on plant age, soil Pb content, and sludge application (Table 1 and Figure 2), but unlike SLA, NAR showed a highly positive relationship with RGR (Figure 6). While NAR reflects the physiological traits of plants, SLA reflects their morphological features [38]. NAR is closely linked to physiological processes such as photosynthesis and respiration [44], which respond to environmental changes more rapidly than structural changes. Therefore, NAR has a greater plasticity index than SLA, which may explain the greater dependence of RGR on NAR than on SLA in lettuce grown under conditions soil pollution and sludge application.
On average for all sludge treatments, Pb accumulation in the roots and shoots of L. sativa was found to decrease NAR at early growth stage (Figure 2). Secondary sludge application contributed to enhanced NAR, but only for plants grown on lead-free soil and on the soil with low Pb content. NAR largely reflects the relationship between photosynthesis and respiration [34] relating to net whole-plant carbon fixation. Respiration and photosynthesis were shown to be sensitive to both soil Pb contamination and sludge application [5]. Sludge-mediated stabilization of the ratio of respiration to photosynthesis can be responsible for the enhanced NAR in lettuce plants. Moreover, since NAR was positively related to plant nitrogen content (Figure 4), the increase in leaf nitrogen content may be one of the factors causing the increase in NAR and providing its positive relationship with RGR (Figure 6).
A deficiency of nitrogen, phosphorus, and potassium limits plant growth [45]. Secondary sludge applications resulted in an increase in root P content (Figure 3b), which may be related to the increase in phosphorus content in soil caused by sludge [10,12] due to the addition of phosphorus to activate the biological treatment of paper sludge [8]. Nunes et al. [9] also showed increased levels of some macronutrients, including phosphorus, in agricultural soils when secondary sludge was used. Increased soil phosphorus content may partially contribute to the restoration of the intensity of photosynthesis and stabilization of the balance between respiration and photosynthesis and, consequently, NAR of lettuce plants. Paper sludge application can also be responsible for the changes in the physical properties of soils [11]. Butilkina and Ikkonen [11] showed an increase in aeration pore volume, heat transfer, and water-holding capacity of the soil under conditions of sludge addition, which could have a positive effect on the physiological characteristics of the plants. The results of our study displayed a sludge-mediated decrease in Pb levels in the roots and leaves of L. sativa (Table 2), which may be associated with an increase in organic matter content and a decrease in Pb mobility in the soil due to the formation of organo-mineral complexes [46]. Moreover, increasing soil phosphate levels may also reduce lead phytoavailability [47]. Both organic matter and additional phosphorus may be responsible for decreased Pb accumulation by plants, thereby helping to reduce Pb load on plants.
While a positive relationship between leaf nitrogen content and seedling RGR was found in some studies [48], other studies showed no relationship [49] or showed a negative relationship [50] between these parameters. No significant effect of phosphorus addition into soils on RGR was found in a line of studies [51,52]. For lettuce plants, our study did not reveal any significant connection between the studied nutrients and RGR, but a positive relationship was found between the specific adsorption rate (SAR) of N or P, defined as the amount of nutrients per unit of root mass, and RGR (Figure 6). For N and P but not for K, soil contamination with Pb caused an increase in SAR (Figure 5), which may be related to the need for additional uptake due to certain adjustments aimed at maintaining plant viability when grown in soil with heavy metal. This adaptive response allows plants to maintain high growth rates under a wide range of environmental conditions [41], including stressful ones, which this study showed. Secondary sludge application increased SAR[N] for 0 Pb and 250 Pb plants, which can be related to the sludge-mediated increases in root biomass or nutrient demand increase and can be the reason for the increased nitrogen accumulation by plants. For the lettuce plants considered in this study, differences in SAR may also be largely related to variations in root morphology, but this point should be explored in future studies. The close links between SAR and RGR found in our study and reported earlier suggest a strong role of SAR in determining RGR [50,53].

5. Conclusions

In this study, the relative growth rate (RGR) index was used as an important indicator of plant productivity strategy to analyze the impact of lead contamination of agricultural soils on L. sativa and evaluate the role of secondary sludge application in mitigating the negative impact of soil lead on plants. High variability in the RGR of the plants was found depending on the time scale and treatments. Differences in the RGR between treatments appear to be explained primarily by plant physiological traits, reflected in the net assimilation rate (NAR), rather than structural features, reflected in the specific leaf area (SLA). During the early growth stage, sludge application stimulated the NAR in plants grown on lead-free or low-Pb soil. For plants cultivated on soil with the highest Pb concentration studied, secondary sludge reduced root lead content. This study found that soil contamination with lead can increase the specific uptake rate (SAR) of nitrogen, phosphorus, and potassium by plants and that sludge addition increases the SAR of N but not P and K. Both the NAR and SAR of nitrogen and phosphorus were positively associated with RGR and can be considered the main determinants of RGR in L. sativa plants. However, the long-term impacts of using paper mill sludges in agriculture and the potential risk of the accumulation of pollutants and heavy metals in soils with long-term sludge application deserve further study.

Author Contributions

Conceptualization, M.Y.; methodology, E.I.; validation, E.I.; investigation, E.I.; resources, M.Y.; writing—original draft preparation, E.I.; writing—review and editing, M.Y.; project administration, M.Y.; funding acquisition, M.Y. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Ministry of Science and Higher Education of the Russian Federation, grant number 2022-0013.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The raw data supporting the conclusions of this article will be made available by the authors on request.

Acknowledgments

The experimental facilities for this study were offered by the Core Facility of the Karelian Research Centre of the Russian Academy of Sciences.

Conflicts of Interest

The authors declare no conflicts of interest.

Abbreviations

The following abbreviations are used in this manuscript:
AGRAbsolute growth rate
RGRRelative growth rate
NARNet assimilation rate
SLASpecific leaf area
SARSpecific absorption rate

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Agriculture 15 01541 g001
Figure 1. Absolut growth rate (AGR, (a,b)) and relative growth rate (RGR, (c,d)) of shoot (a,c) and root (b,d) of L. sativa shoots grown in the soil containing 0, 50, or 250 mg Pb(NO3)2 kg−1 (0 Pb, 50 Pb, or 250 Pb, respectively) and watered with 0, 20, or 40% secondary pulp and paper mill sludge during 17–21, 21–34, and 34–46 days after sowing. Different letters indicate significant differences between the means. For the 17–21-day-old plants, we used lowercase letters; for the 21–34-day-old plants, uppercase letters; and for the 34–46-day-old plants, lowercase letters with apostrophes.
Figure 1. Absolut growth rate (AGR, (a,b)) and relative growth rate (RGR, (c,d)) of shoot (a,c) and root (b,d) of L. sativa shoots grown in the soil containing 0, 50, or 250 mg Pb(NO3)2 kg−1 (0 Pb, 50 Pb, or 250 Pb, respectively) and watered with 0, 20, or 40% secondary pulp and paper mill sludge during 17–21, 21–34, and 34–46 days after sowing. Different letters indicate significant differences between the means. For the 17–21-day-old plants, we used lowercase letters; for the 21–34-day-old plants, uppercase letters; and for the 34–46-day-old plants, lowercase letters with apostrophes.
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Figure 2. Net assimilation rate of L. sativa grown on the soil containing 0, 50, or 250 mg Pb(NO3)2 kg−1 (0 Pb, 50 Pb, or 250 Pb, respectively) and watered with 0, 20, or 40% secondary pulp and paper mill sludge during 21–34 and 34–46 days after sowing. Different letters indicate significant differences between the means. For the 21–34-day-old plants, we used uppercase letters, and for the 34–46-day-old plants, we used lowercase letters with apostrophes.
Figure 2. Net assimilation rate of L. sativa grown on the soil containing 0, 50, or 250 mg Pb(NO3)2 kg−1 (0 Pb, 50 Pb, or 250 Pb, respectively) and watered with 0, 20, or 40% secondary pulp and paper mill sludge during 21–34 and 34–46 days after sowing. Different letters indicate significant differences between the means. For the 21–34-day-old plants, we used uppercase letters, and for the 34–46-day-old plants, we used lowercase letters with apostrophes.
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Agriculture 15 01541 g003
Figure 3. Nitrogen (a), phosphorus (b), and potassium (c) content in shoots and roots of L. sativa grown on the soil containing 0, 50, or 250 mg Pb(NO3)2 kg−1 (0 Pb, 50 Pb, or 250 Pb, respectively) and watered with 0, 20, or 40% secondary pulp and paper mill sludge at 46 days after sowing. Different letters indicate significant differences between the means.
Figure 3. Nitrogen (a), phosphorus (b), and potassium (c) content in shoots and roots of L. sativa grown on the soil containing 0, 50, or 250 mg Pb(NO3)2 kg−1 (0 Pb, 50 Pb, or 250 Pb, respectively) and watered with 0, 20, or 40% secondary pulp and paper mill sludge at 46 days after sowing. Different letters indicate significant differences between the means.
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Figure 4. Relationships between net assimilation rate (NAR) and nitrogen content (a), NAR and phosphorus content (b), and NAR and potassium content (c) in the shoots of L. sativa grown on the soil containing 0, 50, or 250 mg Pb(NO3)2 kg−1 and watered with 0, 20, or 40% secondary pulp and paper mill sludge. NAR values were means for the interval 21–46 days after sowing.
Figure 4. Relationships between net assimilation rate (NAR) and nitrogen content (a), NAR and phosphorus content (b), and NAR and potassium content (c) in the shoots of L. sativa grown on the soil containing 0, 50, or 250 mg Pb(NO3)2 kg−1 and watered with 0, 20, or 40% secondary pulp and paper mill sludge. NAR values were means for the interval 21–46 days after sowing.
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Figure 5. Specific absorption rate of nitrogen (SAR[N], (a)), phosphorus (SAR[P], (b)), and potassium (SAR[K], (c)) of L. sativa plants grown on the soil containing 0, 50, or 250 mg Pb(NO3)2 kg−1 (0 Pb, 50 Pb, or 250 Pb, respectively) and watered with 0, 20, or 40% secondary pulp and paper mill sludge at 46 days after sowing. Different letters indicate significant differences between the means.
Figure 5. Specific absorption rate of nitrogen (SAR[N], (a)), phosphorus (SAR[P], (b)), and potassium (SAR[K], (c)) of L. sativa plants grown on the soil containing 0, 50, or 250 mg Pb(NO3)2 kg−1 (0 Pb, 50 Pb, or 250 Pb, respectively) and watered with 0, 20, or 40% secondary pulp and paper mill sludge at 46 days after sowing. Different letters indicate significant differences between the means.
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Figure 6. Relationships between relative growth rate (RGR) and specific leaf area (SLA, (a)), RGR and net assimilation rate (NAR, (b)), RGR and specific absorption rate of nitrogen (SAR[N], (c)), phosphorus (SAR[P], (d)), and potassium (SAR[P], (e)) of L. sativa grown on the soil containing 0, 50, or 250 mg Pb(NO3)2 kg−1 (0 Pb, 50 Pb, or 250 Pb, respectively) and watered with 0, 20, or 40% secondary pulp and paper mill sludge at 46 days after sowing.
Figure 6. Relationships between relative growth rate (RGR) and specific leaf area (SLA, (a)), RGR and net assimilation rate (NAR, (b)), RGR and specific absorption rate of nitrogen (SAR[N], (c)), phosphorus (SAR[P], (d)), and potassium (SAR[P], (e)) of L. sativa grown on the soil containing 0, 50, or 250 mg Pb(NO3)2 kg−1 (0 Pb, 50 Pb, or 250 Pb, respectively) and watered with 0, 20, or 40% secondary pulp and paper mill sludge at 46 days after sowing.
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Table 2. Lead content in roots and shoots of L. sativa grown on the soil containing 0, 50, or 250 mg Pb(NO3)2 kg−1 and watered with 0, 20, or 40% secondary pulp and paper mill sludge at 34 and 46 days after sowing.
Table 2. Lead content in roots and shoots of L. sativa grown on the soil containing 0, 50, or 250 mg Pb(NO3)2 kg−1 and watered with 0, 20, or 40% secondary pulp and paper mill sludge at 34 and 46 days after sowing.
Parameter0 mg Pb(NO3)2 kg−150 mg Pb(NO3)2 kg−1250 mg Pb(NO3)2 kg−1
0%20%40%0%20%40%0%20%40%
Pb content, g kg−1
In shoosts
34 days after sowing0.8 ± 0.0 c0.7 ± 0.0 c0.5 ± 0.0 c1.5 ± 0.1 b1.4 ± 0.2 b1.3 ± 0.3 b2.5 ± 0.4 a3.4 ± 1.0 a1.9 ± 0.5 ab
46 days after sowing0.4 ± 0.1 d0.8 ± 0.1 dc0.5 ± 0.1 d2.6 ± 0.3 b0.9 ± 0.2 c1.2 ± 0.2 c4.7 ± 1.2 a5.1 ± 0.5 a4.0 ± 0.6 a
In roots
34 days after sowing1.7 ± 0.6 d1.4 ± 0.3 d0.9 ± 0.2 d6.2 ± 1.0 c5.6 ± 0.8 c5.7 ± 0.5 c83.8 ± 10.1 a62.3 ± 4.8 b65.8 ± 4.8 b
46 days after sowing1.2 ± 0.0 d0.9 ± 0.1 d1.1 ± 0.3 d9.6 ± 0.6 c8.4 ± 2.6 c8.2 ± 6.9 c55.7 ± 11.5 a38.4 ± 1.7 b34.9 ± 9.5 b
Different letters indicate significant differences between the means.
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Ikkonen, E.; Yurkevich, M. Relative Growth Rate and Specific Absorption Rate of Nutrients in Lactuca sativa L. Under Secondary Paper Sludge Application and Soil Contamination with Lead. Agriculture 2025, 15, 1541. https://doi.org/10.3390/agriculture15141541

AMA Style

Ikkonen E, Yurkevich M. Relative Growth Rate and Specific Absorption Rate of Nutrients in Lactuca sativa L. Under Secondary Paper Sludge Application and Soil Contamination with Lead. Agriculture. 2025; 15(14):1541. https://doi.org/10.3390/agriculture15141541

Chicago/Turabian Style

Ikkonen, Elena, and Marija Yurkevich. 2025. "Relative Growth Rate and Specific Absorption Rate of Nutrients in Lactuca sativa L. Under Secondary Paper Sludge Application and Soil Contamination with Lead" Agriculture 15, no. 14: 1541. https://doi.org/10.3390/agriculture15141541

APA Style

Ikkonen, E., & Yurkevich, M. (2025). Relative Growth Rate and Specific Absorption Rate of Nutrients in Lactuca sativa L. Under Secondary Paper Sludge Application and Soil Contamination with Lead. Agriculture, 15(14), 1541. https://doi.org/10.3390/agriculture15141541

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