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Article

Seasonal Evaluation and Effects of Poultry Litter-Based Organic Fertilization on Sustainable Production and Secondary Metabolism of Cuphea carthagenensis (Jacq.) J. F. Macbr

by
Joice Karina Otênio Ribeiro
1,
Mariana Moraes Pinc
1,
Rosselyn Gimenes Baisch
2,
Marina Pereira da Silva Bocchio Barbosa
2,
Jaqueline Hoscheid
1,2,
Maiara Kawana Aparecida Rezende
1,
Paula Derksen Macruz
3,
Eduardo Jorge Pilau
3,
Ezilda Jacomassi
2 and
Odair Alberton
1,2,*
1
Postgraduate Program in Biotechnology Applied to Agriculture, Universidade Paranaense (UNIPAR), Umuarama 87502-210, Paraná, Brazil
2
Postgraduate Program in Medicinal Plants and Herbal Medicines in Basic Health Care, Universidade Paranaense (UNIPAR), Umuarama 87502-210, Paraná, Brazil
3
Laboratory of Biomolecules and Mass Spectrometry, Department of Chemistry, State University of Maringá, Maringá 87020-080, Paraná, Brazil
*
Author to whom correspondence should be addressed.
Sustainability 2025, 17(23), 10801; https://doi.org/10.3390/su172310801
Submission received: 22 October 2025 / Revised: 27 November 2025 / Accepted: 29 November 2025 / Published: 2 December 2025
(This article belongs to the Special Issue Soil Pollution, Soil Ecology and Sustainable Land Use)
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Abstract

To ensure the quality and efficient access of the population to plant-derived resources, research on the sustainable cultivation of medicinal species is of great importance, and the present study aimed to evaluate the influence of poultry litter-based organic fertilization and seasonality on plant growth, soil health (quality), and secondary metabolism of Cuphea carthagenensis. Plants were cultivated during the summer and autumn/winter seasons in a randomized design with five poultry litter application rates (0, 10, 20, 30, and 40 t ha−1) and three replications per plot field (1 × 2 m). The parameters evaluated included soil health, plant biomass, nutrient content, extract yield from the aerial parts, and chemical composition. In the summer, soil bioindicators (microbial biomass carbon and basal respiration) increased with the addition of poultry litter, although plant biomass was not affected by the season. Plant nutrient levels, particularly N and P, increased under poultry litter application rates of 30 t ha−1 and higher. Under these conditions, the highest extract yield from the aerial parts was obtained at a rate of 40 t ha−1. During autumn/winter, poultry litter increased significantly soil microbial biomass carbon, plant biomass, and N and P contents, resulting in an 11.07% increase in extract yield at a rate of 20 t ha−1. Phytochemical analysis of the extracts identified 29 compounds, predominantly quercetin derivatives. Overall, the findings demonstrate that the sustainable cultivation of C. carthagenensis under organic fertilization enhances soil health, plant biomass, and extract yield. These findings highlight the potential of organic nutrient management as a promising strategy for advancing sustainable medicinal plant production and meeting societal demands for natural bioactive resources.

1. Introduction

Agronomic studies have been conducted on several Cuphea species to assess their potential for large-scale agricultural production and sustainability [1,2,3,4,5,6]. Among the Cuphea species, Cuphea carthagenensis (Jacq.) J. F. Macbr., commonly known as “sete-sangrias” or waxweed, stands out for its frequent use in Brazilian folk medicine and is traditionally used as a diaphoretic, diuretic, laxative, and in the treatment of arterial hypertension [7].
Pharmacological studies have demonstrated that C. carthagenensis exhibits vasodilatory [8,9], angiotensin-converting enzyme (ACE) inhibitory [10,11], hypotensive [12], antibacterial [13], antimicrobial [14], antistaphylococcal [15], antiviral [16], antioxidant [17,18,19,20,21], anti-inflammatory [22], hypolipidemic, antiatherogenic [23], and hypocholesterolemic activities [24], in addition to renal and cardiovascular protective effects [25]. Phytochemical studies on this species have identified several bioactive compounds in the aerial parts responsible for its biological activities, including flavonoids [13,20], triterpenes [8], tannins, and proanthocyanidins [8,9,18].
These compounds are synthesized through the secondary metabolism of plants, and their production can be influenced by various factors [26,27], such as application of organic fertilizers and environmental conditions—such as climatic variations, seasonal nutrient availability, water supply, and stress periods like drought—play a significant role [27,28,29]. Such factors reflect the adaptive capacity of plants and should be carefully considered when optimizing the production of bioactive compounds [30]. The use of organic fertilizers helps reduce the reliance on chemical fertilizers, which can have adverse effects on human health and the environment. Additionally, organic fertilizers provide an adequate supply of nutrients to plants and contribute to maintaining ecosystem balance and sustainability [27].
Poultry litter, a by-product of poultry farming, has increasing agronomic and environmental relevance, particularly in Brazil, one of the world’s largest chicken producers [31]. As an organic fertilizer, it improves soil chemical properties due to its richness in nutrients, enhances water retention, benefits soil microorganisms, enhances crop productivity, supports soil health, and strengthens the local economy by providing an accessible resource for local poultry producers [32,33,34,35].
Therefore, considering the agronomic and environmental benefits of poultry litter, as well as the widespread traditional use and scientific relevance of C. carthagenensis in treating various conditions, this study aimed to evaluate the seasonality of its cultivation under different rates of a poultry litter-based organic fertilizer. Specifically, the research assessed the effects on soil biological and chemical properties, plant production, and the yield and phytochemical composition of extracts from the plant aerial parts cultivated during the summer and autumn/winter seasons.

2. Materials and Methods

2.1. Experimental Design

The study was conducted at the Medicinal Garden of Universidade Paranaense (UNIPAR) in Umuarama, Paraná, Brazil, located at 23°47′55″ S and 53°18′48″ W, at an altitude of 430 m above sea level. C. carthagenensis is cataloged in the UNIPAR Herbarium under accession number 2401.
The experiment was conducted using a completely randomized design with five treatments corresponding to different rates of the organic fertilizer poultry litter, applied at 0, 10, 20, 30, and 40 t ha−1, in three field subdivided plots of 1 × 2 m each. Poultry litter (with 4.71% of N, 3.42% of P, 2.53% of K, 34% of C, C/N of 7.2, and a pH of 7.3) obtained from a local poultry producer, after composting and maturation, was applied and mixed to a 10 cm layer on the soil surface of each plot. Seedlings of C. carthagenensis were propagated from the mother bed at the UNIPAR Medicinal Garden and transplanted into all experimental field plots, with 70 seedlings per plot. The experiment was conducted twice: first during the summer and subsequently during the autumn/winter season of 2020. Irrigation was applied once daily using conventional sprinklers, and manual weed control was performed. The cultivation period concluded upon the plants’ flowering, which ranged from 100 to 120 days.

2.2. Chemical Characterization of the Soil

Soil samples were collected at a depth of 10 cm at three locations per field plot before poultry litter application rates. Additional soil samples were collected at the end of the cultivation period in the summer and autumn/winter seasons for each poultry litter rate application. All soil samples were submitted for chemical characterization at the Solo Fértil Laboratory in Umuarama, Paraná, Brazil.

2.3. Spore Density and Colonization by Arbuscular Mycorrhizal Fungi (AMF)

Soil samples were collected at the end of plant cultivation to determine AMF spore density. AMF spores were extracted from 10 g soil subsamples for each treatment rate using the wet sieving technique with 0.710 mm and 0.053 mm meshes, following the method of Gerdemann and Nicolson [36]. The samples were centrifuged in water at 3000 rpm for 3 min and in a 50% sucrose solution at 2000 rpm for 2 min, and the resulting supernatant was passed through a 0.053 mm sieve again. For counting, spores were transferred to Petri dishes and examined under a stereomicroscope (40×).
Root samples collected at the end of cultivation during both the summer and autumn/winter seasons were washed under running water and cut into approximately 3 cm segments. The roots were cleared in 10% KOH at 90 °C for 1 h, washed, and acidified with 5% HCl at 90 °C for 30 min, followed by a final rinse in water. They were then stained with 0.05% trypan blue in a water bath at 90 °C for 30 min and preserved in lactoglycerol until slide mounting [37]. To assess root colonization, three root segments were mounted on slides with coverslips, and approximately 100 segments per sample were examined under a stereomicroscope at 40–100× magnification to identify colonization sites by AMFs.

2.4. Determination of Soil Microbial Biomass Carbon, Basal Respiration, and Metabolic Quotient

Microbial biomass carbon (MBC) was determined using the fumigation–extraction method described by Vance et al. [38] and Tate et al. [39], with modifications according to Lermen et al. [40], using 10 g soil subsamples from each treatment and cultivation period.
Basal soil respiration (BSR) was measured following the procedure proposed by Jenkinson and Powlson [41] and described by Silva et al. [42], using 30 g of soil, and the metabolic quotient (qCO2), representing the amount of CO2 released per unit of microbial biomass over a given period, as the ratio between BSR and MBC, according to Anderson and Domsch [43] and Silva et al. [44].

2.5. Determination of Plants’ Fresh and Dry Biomass

At the plants’ flowering, entire plants, including aerial parts and roots, were harvested for analysis. The fresh mass of both aerial parts and roots was determined using a semi-analytical balance, and samples were then oven-dried at 45 °C for 48 h under forced air circulation. Subsequently, the dry mass of aerial parts and roots was determined using a semi-analytical balance.

2.6. Determination of Phosphorus and Nitrogen Content in Plants

Plant P content was determined colorimetrically using the ammonium molybdate–ascorbic acid method with a spectrophotometer equipped with a red filter at a wavelength of 660 nm, following the procedure described by Silva [45], and N content was determined by sulfuric acid digestion at 450 °C, followed by distillation using the Kjeldahl method, according to the procedure described by Silva [45].

2.7. Preparation and Yield of Extracts

Extracts were prepared following the procedure described by Barboza et al. [23], with modifications. One liter of boiling water was added to 60 g of powdered aerial parts, and the mixture was sealed and allowed to stand until reaching room temperature (approximately 6 h). After infusion, three volumes of analytical-grade ethanol were added to induce protein precipitation and obtain the ethanol-soluble fraction, which was subsequently filtered.
The ethanol-soluble fraction was concentrated using rotary evaporation to remove alcohol, followed by lyophilization to eliminate water. The resulting lyophilized extract was stored at −20 °C until phytochemical characterization. The extract yield was calculated as the ratio of the lyophilized extract mass to the initial plant mass (%, m/m).

2.8. Identification of Constituents in the Aerial Parts of C. carthagenensis

Phytochemical analysis of the extracts was performed using an ultra-high-performance liquid chromatograph (UHPLC; Shimadzu Nexera X2, Kyoto, Japan) coupled to a quadrupole time-of-flight mass spectrometer (Q-TOF Impact II, Bruker Daltonik, Bremen, Germany). A solution of 1000 µg mL−1 was prepared in methanol–water (1:1, v/v), filtered through PTFE filters (Millex, 0.22 µm × 13 mm, Millipore, Sigma, Billerica, MA, USA), and 2 µL was injected for analysis.
The UHPLC was equipped with a UPLC® CSH C18 column (1.7 µm, 2.1 × 100 mm, Waters Corp, Milford, MA, USA). The mobile phase consisted of solvent A (water with 0.1% formic acid, v/v) and solvent B (acetonitrile with 0.1% formic acid, v/v), with a flow rate of 0.25 mL min−1. The gradient program was as follows: 3% B (0–1 min), 50% B (1–10 min), 95% B (10–15 min), 95% B (15–19 min), 3% B (19–21 min), and maintained at 3% B (21–25 min) at 40 °C. The final 4 min was used for column re-equilibration. The same solvent system was employed for both positive and negative ionization modes.
Mass spectrometry was performed using a Q-TOF Impact II equipped with an electrospray ionization (ESI) source in AutoMS/MS acquisition mode (Bruker Daltonik, Germany). Data were acquired at a rate of 5 Hz (MS and MS/MS) over an m/z range of 120–1200. Mass spectra were recorded in both positive and negative ionization modes, with a capillary voltage of 3.50 kV, a source temperature of 200 °C, and a desolation gas flow rate of 9 L min−1 [46].

2.9. Statistical Analysis

The means and the standard error of the mean were calculated. The variables for the treatments (Poultry litter and season) were submitted to a two-way analysis of variance (ANOVA) using a general linear model with mixed effects. Before the ANOVA, Levene’s test for equality of variances (homogeneity) was performed, and treatment means were compared using Duncan’s multiple range test at a significance level of p ≤ 0.05. All statistical analyses were performed using IBM SPSS Statistics® version 22 (SPSS Inc., Chicago, IL, USA). The heatmap and principal component analyses (PCAs) were performed using SRplot [47].

3. Results and Discussion

3.1. Chemical Characterization of the Soil

At a poultry litter rate of 40 t ha−1, soil pH increased from 5.44 to 6.17 during the summer and from 5.40 to 6.80 during the autumn/winter season (Table 1).
These results are consistent with the study by Masocha and Dikinya [49], in which poultry litter applied at rates of 0, 15, 30, 60, and 120 g kg−1 significantly affected soil pH, ranging from 7.67 to 8.24. The observed increase in soil pH may be attributed to ion exchange reactions induced by the application of poultry litter at high rates [50].
Poultry litter rates increased soil P, with values exceeding the reference range of 16–24 mg dm−3. A notable increase was observed at 20 t ha−1 in both seasons and at 40 t ha−1 during the autumn/winter season. Before the experiment, soil P at 20 t ha−1 was 11.48 mg dm−3 (below the reference value [48]), increasing to 64.89 mg dm−3 in summer and 30.78 mg dm−3 in autumn/winter after poultry litter application. At a 40 t ha−1 rate without fertilizer, soil P was 33.18 mg dm−3, increasing to 33.48 mg dm−3 in summer and 85.68 mg dm−3 in autumn/winter (Table 1). These results are consistent with those of Chakraborty et al. [51], who reported that poultry litter significantly enhances soil P availability.
Phosphorus is essential for plants, playing a central role in virtually all major metabolic processes, including photosynthesis and respiration [52,53]. Adequate P availability in the soil promotes root growth, facilitates the transfer of nutrients and energy to plant cells, and influences flower and fruit development and overall productivity. Furthermore, P availability can modulate and enhance the concentration of bioactive compounds [54,55].
During the autumn/winter season, the rate of 40 t ha−1 exhibited significantly higher values than the other treatments for soil pH, organic C, Ca, SB, CEC, and V (Table 1). These results indicate that the highest poultry litter rate substantially influenced soil chemical composition, even under lower light and temperature conditions, thereby creating an optimal soil environment for plant growth and enhancing nutrient availability, as well as soil health and quality.

3.2. Arbuscular Mycorrhizal Fungi and Soil Health (Quality)

In this study, soil microbiological activity was evaluated through AMF spore density and root colonization, as well as MBC, BSR, and qCO2 (Table 2 and Table 3). Poultry litter significantly influenced AMF spore density, MBC, qCO2, root biomass, extract yield, and N and P content in the plant (Table 2).
Season alone significantly affected AMF spore density and root colonization, MBC, qCO2, root biomass, total fresh mass, and extract yield. Additionally, the interaction between poultry litter application and season significantly influenced AMF spore density, MBC, root dry mass, and extract yield (Table 2 and Table 3).
During summer cultivation, AMF spore density in the soil was significant at 10 t ha−1 (4.16 spores g−1 of dry soil) and 20 t ha−1 (4.18 spores g−1 of dry soil). However, no significant difference was observed for AMF root colonization during this season.
During the autumn/winter season, neither AMF spore density nor root colonization exhibited significant differences (Table 3). Nevertheless, these results indicate that seasonality had a considerable influence on AMF colonization, with higher values observed in the summer and lower values in the autumn/winter season. This seasonal variation is likely related to climatic factors, such as temperature and humidity, which affect root growth and the AMF response [56].
Spores are reproductive structures of AMF and can persist in the soil for extended periods, awaiting favorable conditions to germinate and colonize plant roots [57]. AMF colonization establishes a symbiotic association, in which the fungi penetrate plant roots and form specialized structures called arbuscules, facilitating the exchange of nutrients and water between the fungus and the host plant [58]. Normally, soils with low P content promote AMF colonization and sporulation, whereas high P levels inhibit both processes, with the magnitude of this effect varying among plant species [59].
During summer cultivation, poultry litter rates of 30 and 40 t ha−1 increased MBC and BSR significantly, consequently, reducing qCO2 values. However, significant qCO2 values were also observed at lower poultry litter rates of 10 t ha−1 and in the control (Table 3). The observed increase in MBC, along with the decrease in qCO2, indicates that C is being retained in the soil rather than released into the atmosphere. This process promotes sustainability and enhances soil health (quality) by improving C sequestration, soil fertility, and the retention of nutrients and water [60,61].
During autumn/winter cultivation, significant increases in MBC were observed at rates of 20 t ha−1 and 40 t ha−1 compared to the control (Table 3). However, no significant differences were found for BSR or qCO2 during this season. These results can be attributed to environmental changes in the autumn/winter, such as lower temperatures, which reduce microbial activity compared with warmer seasons [62]. Such seasonal variations also affect the availability of organic C and other essential nutrients for plant growth [63].
Regression analysis revealed significant relationships for MBC, BSR, and qCO2 during the summer, whereas in autumn/winter, significant effects were observed for AMF root colonization and MBC (Table S1).

3.3. Plants’ Biomass, Phosphorus, and Nitrogen Content

Poultry litter application did not significantly affect the fresh or dry mass of shoots and roots during the summer. In contrast, during autumn/winter, a significant increase in shoot fresh mass (SFM) was observed at 40 t ha−1 (2.83 g plant−1), although no significant effect was detected for shoot dry mass (SDM), and root fresh mass (RFM) was significantly higher at 10 t ha−1 (0.79 g plant−1) and 30 t ha−1 (0.75 g plant−1), while at 10 t ha−1, both root dry mass (RDM) and total dry mass (TDM) also increased significantly (Table 4 and Table S2). Total fresh mass (TFM) was affected significantly at rates of 10, 30, and 40 t ha−1. However, no significant correlation or linear regression was observed between poultry litter rates and season for overall plant biomass (Table S2).
During summer, shoot nitrogen (SN) did not differ significantly among treatments. However, root nitrogen (RN) was significantly higher at 30 t ha−1 (21.50 mg g−1) (Table 5). Shoot phosphorus (SP) content was significantly higher at 30 t ha−1 (1.69 mg g−1) and 40 t ha−1 (1.71 mg g−1) compared with the control treatment without poultry litter addition (1.52 mg g−1) (Table 5). Root phosphorus (RP) also increased significantly at 10, 30, and 40 t ha−1, with values of 1.58, 1.62, and 1.48 mg g−1, respectively (Table 5).
During the autumn/winter season, SN content increased at 40 t ha−1 (26.17 mg g−1) compared with the control (21.33 mg g−1). RN was also significantly higher at 30 and 40 t ha−1, reaching 21.00 and 21.33 mg g−1, respectively. The SP content was significantly higher at 30 t ha−1 (1.70 mg g−1) and 40 t ha−1 (1.64 mg g−1), whereas no significant differences were observed in RP content (Table 5).
Regression analysis showed that, during summer, RN and SP were significantly affected by poultry litter applications. In autumn/winter, SN, RN, and SP of C. carthagenensis increased significantly with higher poultry litter rates (Table S3).
Low soil pH reduces microbial activity, leading to the accumulation of organic matter. In contrast, soils with near-neutral pH have a greater potential for carbon storage and enhanced microbial growth efficiency, which accelerates organic matter decomposition [64]. This explains why, in autumn/winter, a 40 t ha−1 rate showed a pH of 6.80—approaching alkalinity—along with an increase in MBC to 154.96 µg CO2 g−1. These conditions favored higher shoot nitrogen (26.17 mg g−1) and root nitrogen (21.33 mg g−1) contents in C. carthagenensis, resulting in greater shoot and root biomass.
The heat map combined with hierarchical clustering revealed distinct treatment profiles based on soil quality parameters, AMF spore density and root colonization, plant biomass production, shoot and root N and P content, and plant extract yield. During summer cultivation, treatments without poultry litter and 10 t ha−1 formed one distinct cluster, while treatments from 20 t ha−1 formed another cluster (Figure 1A). In autumn/winter, the control (0 t ha−1) formed an isolated cluster, distinct from all litter-amended treatments (Figure 1B). The variable most influencing extract yield was qCO2 during summer, whereas spore density and AMF root colonization were the most influential factors during winter (Figure 1A and Figure 1B, respectively).
During the summer, the rates of 0 and 10 t ha−1 exhibited similar behavior, likely due to limited nutrient availability and reduced stimulation of mycorrhizal activity. In contrast, poultry litter rate of 20 t ha−1 and above produced a distinct pattern, characterized by higher N and P contents and increased plant biomass (Figure 1A). In autumn/winter, the heatmap indicated that the rate of 0 t ha−1 formed a separate cluster from all litter-amended rates, suggesting that the absence of organic fertilization accentuated differences among rates. This finding aligns with the results of Agbede [65], who reported that poultry litter applications up to 10 t ha−1 induced responses distinct from those at higher doses, reflecting significant differences in soil properties and plant productivity.
Among the analyzed parameters (Figure 1A), qCO2 was the most influential factor affecting extract yield. Lower qCO2 values indicate greater microbial efficiency, which is directly associated with improved plant performance—a pattern observed at the rate of 40 t ha−1. Li et al. [66] emphasized that efficient utilization of available C, reflected by reduced qCO2, is linked to a more active and effective microbial community, resulting in enhanced nutrient availability for plants and, consequently, higher biomass accumulation and increased production of bioactive compounds.
The dendrogram for autumn/winter cultivation (Figure 1B) indicated that AMF spore density and root colonization were the parameters most strongly influencing extract yield, highlighting the importance of mycorrhizal symbiosis under conditions of reduced soil nutrient availability [67]. During this season, organic fertilization played an even more crucial role in supporting plant performance by improving soil health and quality and increasing extract yield. The rate of 20 t ha−1 poultry litter produced the highest extract yield, AMF root colonization, and spore density, even in the absence of AMF inoculation. Lower application rates may have limited nutrient availability [68], whereas higher doses could have decreased mycorrhizal colonization efficiency due to nutrient excess or shifts in microbial community dynamics [69].
Furthermore, elevated soil microbial activity may be associated with enhanced plant productivity, improved nutrient availability, and increased accumulation of bioactive compounds [70]. Therefore, obtaining plant extracts and performing phytochemical characterization under this cultivation model were essential to assess the effectiveness of poultry litter application for the cultivation of this species.

3.4. Yield of Extracts and Identification of Constituents in the Aerial Parts of C. carthagenensis

Overall, the interaction between season and poultry litter application rate significantly influenced the extract yield (EY) of the aerial parts of C. carthagenensis. During summer cultivation, the highest EY was observed at 40 t ha−1 (10.91%), followed by 10 t ha−1 (10.62%) and 20 t ha−1 (10.17%), whereas the lowest yield occurred at 30 t ha−1 (8.46%). The control (0 t ha−1) presented an EY of 10.87%. In the autumn/winter season, the highest yield was recorded at 20 t ha−1 (11.07%), followed by the control (10.81%), 30 t ha−1 (10.49%), and 10 t ha−1 (10.31%), while the lowest yield occurred at 40 t ha−1 (9.81%). All EYs differed significantly among treatments (Table 2).
In the EY, a total of 29 compounds were identified in the phytochemical profiles (positive and negative ionization modes) of the aerial parts of C. carthagenensis cultivated during summer and autumn/winter under poultry litter application rates of 0, 10, 20, 30, and 40 t ha−1 (Table 6 and Table 7).
In the positive ion mode during the summer, the major chemical compound identified was the glycosylated flavonoid quercetin 3-O-glucuronide, accounting for 37.49% in the treatment without poultry litter and 34.59% in the rate of 10 t ha−1. At higher poultry litter rates (20, 30, and 40 t ha−1), free quercetin was the predominant compound, representing 33.22%, 37.28%, and 36.62%, respectively (Table 6). In autumn/winter, quercetin 3-O-glucuronide was predominant in the treatment without poultry litter (35.50%) and at 20 t ha−1 (36.59%), whereas free quercetin was dominant at 10, 30, and 40 t ha−1, representing 40.96%, 40.29%, and 40.50%, respectively (Table 6). Thus, higher poultry litter rates favored the predominance of free quercetin.
In the negative ion mode, quercetin 3-O-glucuronide was also the major compound across all poultry litter rates in both summer and autumn/winter (Table 7). Additionally, during the summer, the relative abundance of free quercetin increased with poultry litter application: the treatment without poultry litter accounted for 11.54%, while the 10, 20, 30, and 40 t ha−1 treatments showed 14.05%, 15.50%, 18.57%, and 16.94%, respectively (Table 7). A similar pattern was observed in autumn/winter, with the control (no poultry litter) showing 12.31% free quercetin, and the 10, 20, 30, and 40 t ha−1 treatments showing 19.25%, 14.62%, 19.26%, and 17.77%, respectively (Table 6 and Table 7).
The heatmap combined with hierarchical clustering revealed distinct treatment profiles based on the three major compounds—quercetin 3-O-glucuronide, quercetin, and quercetin 3-α-L-arabinofuranoside—in the positive ion mode during summer (Figure 2A) and autumn/winter (Figure 2B). In summer, the rates 30 and 40 t ha−1 formed a distinct cluster and showed increased quercetin production (Table 6 and Figure 2A), whereas in autumn/winter, a similar pattern was observed for the rates 10, 30, and 40 t ha−1 (Table 6 and Figure 2B).
Principal component analysis (PCA) explained 99.2% of the total variance in summer (PC1 = 92.5%, PC2 = 6.7%), clearly distinguishing the treatments according to their major compound profiles, with positive associations at 30 and 40 t ha−1 (Figure 2C). In autumn/winter, PCA explained 98.7% of the total variance (PC1 = 73.3%, PC2 = 25.4%), again clearly differentiating the treatments based on their major compound profiles, with positive associations observed at 10, 30, and 40 t ha−1 (Figure 2D).
These results indicate that increasing poultry litter rates stimulated flavonoid biosynthesis under both seasonal conditions. This effect may be associated with improvements in soil chemical and biological properties induced by the organic amendment, which enhance nutrient availability and microbial activity [27,71]. Therefore, poultry litter likely promoted metabolic pathways leading to the formation of both free and glycosylated quercetin.
Additionally, the positive effect may be partially attributed to the interaction between seasonal and physiological factors. During summer, higher light intensity and temperature likely intensified oxidative stress in plants, thereby stimulating the production of antioxidant metabolites such as quercetin [71]. Higher poultry litter rates may have mitigated nutritional stress, enabling plants to allocate more metabolic energy toward secondary metabolite production [72]. In autumn/winter, even under lower light intensity, both lower and higher rates continued to favor quercetin synthesis, indicating that the organic amendment exerts a modulatory effect independent of season [27].
Table 6. Compounds (%) identified by ultra-high-performance liquid chromatography coupled to mass spectrometry (UHPLC–MS/MS) in positive ion mode from aerial part extracts of Cuphea carthagenensis cultivated during summer and autumn/winter seasons under poultry litter application rates of 0, 10, 20, 30, and 40 t ha−1.
Table 6. Compounds (%) identified by ultra-high-performance liquid chromatography coupled to mass spectrometry (UHPLC–MS/MS) in positive ion mode from aerial part extracts of Cuphea carthagenensis cultivated during summer and autumn/winter seasons under poultry litter application rates of 0, 10, 20, 30, and 40 t ha−1.
CompoundMSRT
(min)		Summer–Poultry Litter Doses (t ha−1)Autumn/Winter–Poultry Litter Doses (t ha−1)Reference
010203040010203040
Quercetin 3-O-glucuronide479.0825.5637.49 *34.5932.1131.5229.2835.5031.4536.5931.4032.36[73]
Quercetin303.0507.2627.9232.3933.2237.2836.6231.6440.9633.1340.2940.50[74]
Quercetin 3-α-L-arabinofuranoside435.0925.699.118.458.807.647.748.147.988.138.207.46[75]
Quercetin 3-O-glucoside465.1035.405.504.715.335.014.814.804.754.274.804.26[76]
Kaempferol 3-O-beta-sophoroside611.1615.124.594.384.614.244.403.302.612.572.612.84[77]
Quercetin 3-O-galactoside465.1035.064.503.514.223.303.823.022.923.272.862.48[78]
Kaempferol 3-O-rutinoside595.1665.534.445.144.904.935.133.734.274.374.424.76[79]
Kaempferol 3-O-glucoside449.1085.762.072.042.112.262.202.292.352.192.682.71[79]
Vicenin 2595.1664.411.732.351.661.722.151.401.021.010.960.97[80]
Kaempferol 3-glucuronide463.0875.901.160.941.020.970.941.071.041.161.111.13[81]
Myricetin 3-galactoside481.0984.981.010.951.010.670.920.50-0.54--[82]
2′-O-galloylhyperin617.1145.200.500.540.620.450.560.620.640.640.680.52[83]
Catechin291.0864.16----1.041.34-1.31--[84]
Epigallocatechin307.0813.33-----0.83-0.83--[85]
Apigenin 7-glucuronide447.0925.99-----1.03----[86]
Leucoside581.1505.46--0.40-0.40-----[87]
Rosmarinic acid361.0926.11-----0.82----[88]
Glycosylated flavonoids:72.0867.6166.7862.7262.3465.3759.0464.7459.7159.50
Free flavonoids:27.9232.3933.2237.2837.6633.8140.9635.2640.2940.50
Phenolic acids:-----0.82----
* Relative percentages were calculated based on the total area of identified compounds. (-) Not detected. RT: retention time. MS: molecular mass.
Table 7. Compounds (%) identified by ultra-high-performance liquid chromatography coupled to mass spectrometry (UHPLC–MS/MS) in negative ion mode from aerial part extracts of Cuphea carthagenensis cultivated during summer and autumn/winter seasons under poultry litter application rates of 0, 10, 20, 30, and 40 t ha−1.
Table 7. Compounds (%) identified by ultra-high-performance liquid chromatography coupled to mass spectrometry (UHPLC–MS/MS) in negative ion mode from aerial part extracts of Cuphea carthagenensis cultivated during summer and autumn/winter seasons under poultry litter application rates of 0, 10, 20, 30, and 40 t ha−1.
CompoundMSRT (min)Summer–Poultry Litter Doses (t ha−1)Autumn/Winter–Poultry Litter Doses (t ha−1)Reference
010203040010203040
Quercetin 3-O-glucuronide477.0665.6028.01 *25.6523.2325.0621.8121.4724.2524.4023.5122.68[89]
Quercetin301.0347.2611.5414.0515.5018.5716.9412.3119.2514.6219.2617.77[90]
Quercetin 3-α-L-arabinofuranoside433.0775.7110.7910.7110.189.169.308.5710.3610.2511.019.31[89]
Gallic acid169.0132.489.8211.1913.529.9514.917.319.079.628.799.92[91]
Turanose341.1081.009.439.677.349.036.517.389.149.227.927.77[92]
D-Mannitol227.0761.016.237.934.996.936.335.087.558.947.488.35[91]
Quercetin 3-O-glucoside463.0875.424.634.384.804.144.303.604.373.794.563.66[93]
Kaempferol 3-O-rutinoside593.1505.513.854.544.374.544.732.733.943.984.414.52[94]
Quercetin 3-O-galactoside463.0875.053.442.923.552.883.142.232.662.592.612.09[89]
Kaempferol 3-O-glucoside447.0925.782.122.262.402.322.441.992.792.563.223.03[95]
Matairesinoside519.1865.981.38-1.221.091.011.441.791.912.281.88[96]
Kaempferol 3-O-beta-sophoroside609.1455.141.301.041.210.921.120.300.330.390.380.39[77]
Kaempferol 3-glucuronide461.0715.901.111.030.991.030.931.001.111.191.281.11[81]
Chebuloside II711.3956.211.100.831.300.841.260.370.39-0.410.34[97]
Rosmarinic acid359.0766.111.04----9.990.381.50-2.83[98]
Vicenin 2593.1504.390.951.620.651.290.770.910.831.050.760.82[99]
Myricetin 3-galactoside479.0824.970.770.720.960.560.820.37-0.42-0.32[82]
Myricetin-3-O-xyloside449.0715.270.73-0.870.490.810.43----[100]
Chicoric acid473.0716.590.64----6.59-0.53-0.92[101]
1-O-Feruloylglucose355.1024.090.630.270.600.740.430.430.530.610.840.77[102]
2′-O-galloylhyperin615.0985.220.520.550.650.480.600.560.660.660.710.56[103]
3-methoxybenzoic acid465.1036.04--0.46-0.40-----[104]
Apigenin 7-glucuronide445.0776.03-----0.37----[105]
Catechin289.0714.19-0.670.54-0.660.70-0.82--[90]
Epigallocatechin305.0663.35----0.340.75-0.96--[90]
1.6-Digalloyl-beta-D-glucopyranose483.0773.89--0.41-0.460.510.58-0.59-[106]
Abscisic acid263.1286.85--0.26-------[107]
Carnosol329.17510.74-----2.64---0.97[108]
Glycosylated flavonoids:58.2055.4153.8752.8650.7744.5151.3251.2752.4548.48
Free flavonoids:11.5414.7116.0418.5717.9413.7619.2516.4019.2617.77
Carboxylic acids:9.8211.1913.519.9514.917.319.079.628.789.92
Glycosides:9.439.677.349.036.517.389.149.227.927.77
Lignans:6.237.934.996.926.335.087.558.947.488.35
Saccharides:2.010.271.811.831.441.862.322.523.112.65
Terpenoids:1.100.831.560.841.263.010.39-0.401.30
Cinnamic acids:1.04----9.990.381.50-2.83
Phenolic acids:0.64-0.46-0.406.59-0.53-0.92
Tannins:-0.460.510.58-0.59--0.460.51
* Relative percentages were calculated based on the total area of identified compounds. (-) Not detected. RT: retention time. MS: molecular mass.
Free quercetin was also abundant in the aerial parts of C. carthagenensis in the study by Prando et al. [20]. The conjugated flavonoid quercetin 3-sulfate was identified as the major compound in this species in studies by Santos et al. [109] and Krepsky et al. [9]. Similarly, quercetin 3-O-glucuronide was reported as the predominant compound in aerial extracts by Barboza et al. [23], which is consistent with the findings of the present study.
Conjugated quercetin is the most common form in plants, serving as the transport and storage form, whereas free quercetin exhibits higher in vitro biological activity [110]. Barboza et al. [23] and Santos et al. [109] reported the predominance of quercetin, myricetin, and kaempferol derivatives in aerial extracts of C. carthagenensis. These compounds were also detected in the present study.
Notably, under the cultivation conditions described here, poultry litter influenced the phytochemical profile of C. carthagenensis, leading to increased free quercetin production. The enhanced accumulation of free quercetin may reflect the plant’s response to poultry litter, with organic fertilization inducing metabolic stress that triggers a higher release of this active form as a defense mechanism. Among the therapeutic properties of quercetin, its antioxidant activity is widely reported [111,112,113,114,115,116]. Additionally, quercetin exhibits anticancer [117], antidiabetic [118], anti-inflammatory [119], antimicrobial [117], antiviral [120], cardiovascular [121], and neuroprotective [122] effects.
Although isolated compounds such as quercetin exhibit well-recognized pharmacological activity, their use may be associated with adverse effects. In contrast, the whole plant functions as a phytocomplex, in which the synergy of multiple secondary metabolites can enhance therapeutic efficacy while minimizing side effects [109]. Therefore, recognizing and valuing the use of the whole plant is essential for maintaining both effectiveness and safety, highlighting the importance of phytotherapeutics in integrative medicine and the development of new natural products.

4. Conclusions

During summer, soil bioindicators—including spore density, microbial biomass carbon (MBC), basal soil respiration, and the metabolic quotient—showed significant responses to poultry litter application at rates above 20 t ha−1. Although the soil properties were affected, no significant differences were observed in plant biomass yield. Although plant nutrients, such as P and N, were influenced during the same season, with significant effects observed at poultry litter rates of 30 t ha−1 and 40 t ha−1. Under these cultivation conditions, the highest extract yield of the aerial part was obtained at 40 t ha−1. Analyses also revealed that poultry litter affected the major bioactive compounds, with higher free quercetin at rates of 30 and 40 t ha−1.
During the autumn/winter season, significant effects on soil health were observed only for MBC at rates of 20 t ha−1 and higher. Consequently, plant biomass (total dry mass) yield increased significantly at rates starting from 10 t ha−1. N and P levels also increased from 10 t ha−1 onward. Furthermore, heatmap analysis indicated that AMF root colonization and soil spore density influenced the extract yield of the aerial part, with the greatest effect observed at a rate of 20 t ha−1. Regarding free quercetin, the major bioactive compounds, poultry litter rates of 10, 30, and 40 t ha−1 increased its production.
It is noteworthy that, although the autumn/winter season generally presents lower soil quality and health for plant growth, the application of poultry litter at low rates produced significant positive effects on the cultivation of the medicinal species C. carthagenensis in this season.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/su172310801/s1, Table S1: Correlation and linear regression of AMF spore density, root colonization (%), microbial biomass carbon (MBC, µg CO2 g−1), basal soil respiration (BSR, µg C-CO2 g−1 h−1), and metabolic quotient (qCO2, µg CO2 µg−1 microbial C h−1) in Cuphea carthagenensis cultivated in summer and autumn/winter seasons under different poultry litter rates (0, 10, 20, 30, and 40 t ha−1). Table S2: Correlation and linear regression of shoot fresh mass (SFM—g plant−1), shoot dry mass (SDM—g plant−1), root fresh mass (RFM—g plant−1), root dry mass (RDM—g plant−1), total fresh mass (TFM—g plant−1), and total dry mass in Cuphea carthagenensis cultivated in summer and autumn/winter seasons under different poultry litter rates (0, 10, 20, 30, and 40 t ha−1). Table S3: Nitrogen in aerial parts and roots (SN mg g−1 and RN mg g−1), phosphorus in aerial parts and roots (SP mg g−1 and RP mg g−1) of Cuphea carthagenensis cultivated in summer and autumn/winter seasons under different poultry litter rates (0, 10, 20, 30, and 40 t ha−1).

Author Contributions

Conceptualization, J.K.O.R. and O.A.; Methodology, J.K.O.R., M.M.P., R.G.B., M.P.d.S.B.B., J.H., P.D.M., E.J.P., E.J. and O.A.; Software, P.D.M. and E.J.P.; Formal analysis, J.K.O.R., M.M.P., J.H., P.D.M., E.J.P. and O.A.; Investigation, M.M.P., R.G.B., M.P.d.S.B.B., J.H., P.D.M., E.J.P., E.J. and O.A.; Resources, O.A.; Data curation, J.H., M.K.A.R., P.D.M., E.J.P. and O.A.; Writing—original draft, J.K.O.R., M.M.P., M.K.A.R. and O.A.; Writing—review & editing, O.A.; Visualization, O.A.; Supervision, O.A.; Project administration, O.A.; Funding acquisition, O.A. All authors have read and agreed to the published version of the manuscript.

Funding

The authors acknowledge Universidade Paranaense (UNIPAR) for financial support. Joice K.O. Ribeiro thanks PROSUP/CAPES for the scholarship. Mariana M. Pinc thanks CAPES/PDPG Emergencial de Consolidação Estratégica dos Programas de Pós-Graduação for the scholarship. Odair Alberton acknowledges a research fellowship from CNPq (grant number 310981/2023-9).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data will be made available on request.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Heatmap combined with hierarchical clustering showing distinct treatment profiles based on soil quality parameters, AMF spore density and root colonization, plant biomass production, shoot and root N and P contents, and extract yield (EY) (based on Table 2) of Cuphea carthagenensis cultivated during summer (A) and autumn/winter (B) seasons under poultry litter application rates of 0, 10, 20, 30, and 40 t ha−1.
Figure 1. Heatmap combined with hierarchical clustering showing distinct treatment profiles based on soil quality parameters, AMF spore density and root colonization, plant biomass production, shoot and root N and P contents, and extract yield (EY) (based on Table 2) of Cuphea carthagenensis cultivated during summer (A) and autumn/winter (B) seasons under poultry litter application rates of 0, 10, 20, 30, and 40 t ha−1.
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Figure 2. Heatmap combined with hierarchical clustering showing distinct treatment profiles based on the three major compounds (quercetin 3-O-glucuronide, quercetin, and quercetin 3-α-L-arabinofuranoside) in the positive ion mode of the extract during summer (A) and autumn/winter (B), and Principal Component Analysis (PCA) of the same compounds in Cuphea carthagenensis plants cultivated in summer (C) and autumn/winter (D) seasons under different poultry litter rates of 0, 10, 20, 30, and 40 t ha−1.
Figure 2. Heatmap combined with hierarchical clustering showing distinct treatment profiles based on the three major compounds (quercetin 3-O-glucuronide, quercetin, and quercetin 3-α-L-arabinofuranoside) in the positive ion mode of the extract during summer (A) and autumn/winter (B), and Principal Component Analysis (PCA) of the same compounds in Cuphea carthagenensis plants cultivated in summer (C) and autumn/winter (D) seasons under different poultry litter rates of 0, 10, 20, 30, and 40 t ha−1.
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Table 1. Chemical properties of the soil cultivated with Cuphea carthagenensis cultivated in summer and autumn/winter seasons under different poultry litter rates (0, 10, 20, 30, and 40 t ha−1).
Table 1. Chemical properties of the soil cultivated with Cuphea carthagenensis cultivated in summer and autumn/winter seasons under different poultry litter rates (0, 10, 20, 30, and 40 t ha−1).
Rates *pH (CaCl2)PCAl3+H+ + Al3+Ca2+Mg2+K+SBCECV
mg dm−3g dm−3Cmol dm−3%
Before the experiment
05.1213.026.4302.742.501.250.264.016.7559.39
105.2629.547.4002.952.881.750.364.987.9362.82
205.2111.486.2302.542.501.500.234.236.7762.49
305.3339.907.0102.542.881.750.385.017.5566.36
405.4433.187.6002.743.001.750.415.167.9065.32
After summer cultivation
06.0416.456.2302.032.631.500.364.486.5168.84
106.1324.748.3802.193.251.750.385.387.5771.09
206.1664.895.6502.033.001.500.334.836.8670.42
305.9458.596.4302.192.751.630.214.586.7767.65
406.1733.487.2102.033.502.000.265.767.7973.93
After autumn/winter cultivation
06.0717.506.2302.032.751.500.384.636.6669.54
106.3427.546.8201.893.251.750.515.517.4074.47
206.5730.787.0101.753.131.750.385.267.0175.03
306.5835.287.9901.753.752.000.366.117.8677.73
406.8085.6810.5201.624.632.750.447.819.4382.82
Ref 13.8–6.616–240.8–15.9-0.6–5.00.3–7.20.3–3.30.1–0.7-2.2–12.5-
* Methods: Phosphorus (P) and potassium (K) were extracted using Mehlich-I; calcium (Ca), magnesium (Mg), and aluminum (Al) were extracted with 1 mol L−1 potassium chloride (KCl); carbon (C) was determined by dichromate/colorimetric method; CEC = cation exchange capacity; SB = sum of bases; V = base saturation. 1 Source: Sambatti et al. [48].
Table 2. Phosphorus (P) values in two-way ANOVA for various soil parameters of Cuphea carthagenensis cultivated in summer and autumn/winter seasons under different poultry litter rates (0, 10, 20, 30, and 40 t ha−1).
Table 2. Phosphorus (P) values in two-way ANOVA for various soil parameters of Cuphea carthagenensis cultivated in summer and autumn/winter seasons under different poultry litter rates (0, 10, 20, 30, and 40 t ha−1).
ParametersPoultry Litter (PL) Season (S)PL × S
Spores (number of spores g−1 of dry soil)<0.001<0.0010.010
Root colonization by AMF (%)0.377<0.0010.338
Microbial biomass carbon (µg CO2 g−1)<0.001<0.0010.005
Soil basal respiration (µg C-CO2 g−1 h−1)0.1300.1460.479
Metabolic quotient (qCO2, µg CO2 µg−1 microbial C h−1)0.017<0.0010.564
Shoot fresh mass (g)0.1200.0910.686
Shoot dry mass (g)0.2220.3920.818
Root fresh mass (g)0.025<0.0010.602
Root dry mass (g)0.031<0.0010.001
Total fresh mass (g)0.0900.0230.812
Total dry mass (g)0.1800.1540.642
Extract yield (%) in the shoot<0.001<0.001<0.001
Shoot nitrogen content (mg kg−1)0.1230.1780.853
Root nitrogen content (mg kg−1)0.0030.6160.764
Shoot phosphorus content (mg kg−1)0.0020.1020.763
Root phosphorus content (mg kg−1)0.0440.1740.427
Table 3. AMF Spore density, root colonization (%), microbial biomass carbon (MBC, µg CO2 g−1), basal soil respiration (BSR, µg C-CO2 g−1 h−1), and metabolic quotient (qCO2, µg CO2 µg−1 microbial C h−1) of Cuphea carthagenensis cultivated in summer and autumn/winter seasons under different poultry litter rates (0, 10, 20, 30, and 40 t ha−1).
Table 3. AMF Spore density, root colonization (%), microbial biomass carbon (MBC, µg CO2 g−1), basal soil respiration (BSR, µg C-CO2 g−1 h−1), and metabolic quotient (qCO2, µg CO2 µg−1 microbial C h−1) of Cuphea carthagenensis cultivated in summer and autumn/winter seasons under different poultry litter rates (0, 10, 20, 30, and 40 t ha−1).
RatesSporeColonizationMBCBSRqCO2
After summer cultivation
01.48 ± 0.18 b85.67 ± 6.23132.15 ± 9.77 c1.01 ± 0.06 b7.69 ± 0.23 ab
104.16 ± 0.29 a87.37 ± 2.28146.36 ± 11.83 c1.27 ± 0.13 ab8.66 ± 0.54 a
204,18 ± 0.41 a86.15 ± 3.69202.27 ± 8.25 b1.30 ± 0.07 ab6.45 ± 0.30 bc
302.33 ± 0.08 b91.30 ± 0.81262.55 ± 28.00 a1.32 ± 0.01 a5.16 ± 0.58 c
402.18 ± 0.77 b84.26 ± 2.07246.91 ± 19.83 ab1.51 ± 0.12 a6.27 ± 1.01 bc
Sig.0.0030.6900.0010.0360.017
After autumn/winter cultivation
01.10 ± 0.1828.33 ± 1.67113.73 ± 3.22 c1.29 ± 0.1811.24 ± 1.39
101.70 ± 0.4020.11 ± 4.91119.44 ± 3.34 bc1.43 ± 0.1412.03 ± 1.37
201.93 ± 0.2224.11 ± 9.63150.50 ± 12.59 a1.38 ± 0.129.27 ± 1.01
301.41 ± 0.1117.56 ± 2.41141.02 ± 11.58 ab1.48 ± 0.0810.52 ± 0.27
401.31 ± 0.0412.22 ± 2.42154.96 ± 4.91 a1.38 ± 0.108.95 ± 0.92
Sig.0.3350.2900.0170.8690.282
Mean ± standard error (n = 3). Means within each column followed by different letters are significantly different according to Duncan’s multiple range test (p ≤ 0.05).
Table 4. Shoot fresh mass (SFM—g plant−1), root fresh mass (RFM—g plant−1), total fresh mass (TFM—g plant−1), shoot dry mass (SDM—g plant−1), root dry mass (RDM—g plant−1), and total dry mass (TDM—g plant−1) of Cuphea carthagenensis cultivated in summer and autumn/winter seasons under different poultry litter rates (0, 10, 20, 30, and 40 t ha−1).
Table 4. Shoot fresh mass (SFM—g plant−1), root fresh mass (RFM—g plant−1), total fresh mass (TFM—g plant−1), shoot dry mass (SDM—g plant−1), root dry mass (RDM—g plant−1), and total dry mass (TDM—g plant−1) of Cuphea carthagenensis cultivated in summer and autumn/winter seasons under different poultry litter rates (0, 10, 20, 30, and 40 t ha−1).
RatesSFMRFMTFMSDMRDMTDM
After summer cultivation
01.42 ± 0.310.31 ± 0.041.73 ± 0.350.41 ± 0.090.06 ± 0.010.47± 0.10
101.66 ± 0.480.57 ± 0.202.22 ± 0.690.50 ± 0.120.05 ± 0.010.55 ± 0.12
201.93 ± 0.530.30 ± 0.102.23 ± 0.620.56 ± 0.160.07 ± 0.010.63 ± 0.16
302.37 ± 0.300.40 ± 0.022.77 ± 0.310.67 ± 0.110.08 ± 0.010.74 ± 0.12
402.16 ± 0.490.31 ± 0.012.47 ± 0.490.62 ± 0.160.08 ± 0.010.69 ± 0.17
Sig.0.5720.3700.7020.6700.3730.662
After autumn/winter cultivation
01.60 ± 0.26 b0.42 ± 0.04 b2.02 ± 0.26 b0.43 ± 0.050.08 ± 0.01 b0.51 ± 0.05 b
102.73 ± 0.43 ab0.79 ± 0.07 a3.52 ± 0.50 a0.74 ± 0.110.16 ± 0.02 a0.90 ± 0.13 a
201.97 ± 0.28 ab0.68 ± 0.10 ab2.65 ± 0.36 ab0.57 ± 0.080.12 ± 0.01 b0.69 ± 0.08 ab
302.64 ± 0.47 ab0.75 ± 0.09 a3.39 ± 0.44 a0.71 ± 0.120.12 ± 0.01 b0.83 ± 0.11 ab
402.83 ± 0.25 a0.51 ± 0.10 ab3.34 ± 0.26 a0.61 ± 0.100.11 ± 0.01 b0.72 ± 0.09 ab
Sig.0.0470.0480.0470.2310.0040.048
Mean ± standard error (n = 3). Means within each column followed by different letters are significantly different according to Duncan’s multiple range test (p ≤ 0.05).
Table 5. Shoot nitrogen (SN, mg g−1) and roots (RN, mg g−1) content and shoot phosphorus (SP, mg g−1) and roots (RP, mg g−1) content in Cuphea carthagenensis cultivated in summer and autumn/winter seasons under different poultry litter rates (0, 10, 20, 30, and 40 t ha−1).
Table 5. Shoot nitrogen (SN, mg g−1) and roots (RN, mg g−1) content and shoot phosphorus (SP, mg g−1) and roots (RP, mg g−1) content in Cuphea carthagenensis cultivated in summer and autumn/winter seasons under different poultry litter rates (0, 10, 20, 30, and 40 t ha−1).
RatesSNRNSPRP
After summer cultivation
022.17 ± 0.9317.33 ± 0.44 b1.52 ±0.01 b1.15 ± 0.07 b
1026.50 ± 2.7820.17 ± 1.17 ab1.56 ± 0.06 b1.58 ± 0.02 a
2027.67 ± 3.6119.50 ± 1.04 ab1.61 ± 0.03 ab1.42 ± 0.15 ab
3025.17 ± 0.3321.50 ± 0.76 a1.69 ± 0.03 a1.62 ± 0.05 a
4026.00 ± 1.0020.17 ± 1.17 ab1.71 ± 0.03 a1.48 ± 0.07 a
Sig.0.4780.0410.0140.022
After autumn/winter cultivation
021.33 ± 1.45 b17.17 ± 0.73 b1.40 ± 0.04 b1.28 ± 0.06
1024.17 ± 0.88 ab19.17 ± 0.33 ab1.54 ± 0.05 ab1.41 ± 0.11
2024.17 ± 0.93 ab18.50 ± 1.00 ab1.50 ± 0.05 ab1.31 ± 0.07
3024.00 ± 1.53 ab21.00 ± 1.00 a1.70 ± 0.10 a1.38 ± 0.06
4026.17 ± 1.17 a21.33 ± 1.20 a1.65 ± 0.09 a1.42 ± 0.18
Sig.0.0470.0420.0480.844
Mean ± standard error (n = 3). Means within each column followed by different letters are significantly different according to Duncan’s multiple range test (p ≤ 0.05).
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MDPI and ACS Style

Ribeiro, J.K.O.; Pinc, M.M.; Baisch, R.G.; Barbosa, M.P.d.S.B.; Hoscheid, J.; Rezende, M.K.A.; Macruz, P.D.; Pilau, E.J.; Jacomassi, E.; Alberton, O. Seasonal Evaluation and Effects of Poultry Litter-Based Organic Fertilization on Sustainable Production and Secondary Metabolism of Cuphea carthagenensis (Jacq.) J. F. Macbr. Sustainability 2025, 17, 10801. https://doi.org/10.3390/su172310801

AMA Style

Ribeiro JKO, Pinc MM, Baisch RG, Barbosa MPdSB, Hoscheid J, Rezende MKA, Macruz PD, Pilau EJ, Jacomassi E, Alberton O. Seasonal Evaluation and Effects of Poultry Litter-Based Organic Fertilization on Sustainable Production and Secondary Metabolism of Cuphea carthagenensis (Jacq.) J. F. Macbr. Sustainability. 2025; 17(23):10801. https://doi.org/10.3390/su172310801

Chicago/Turabian Style

Ribeiro, Joice Karina Otênio, Mariana Moraes Pinc, Rosselyn Gimenes Baisch, Marina Pereira da Silva Bocchio Barbosa, Jaqueline Hoscheid, Maiara Kawana Aparecida Rezende, Paula Derksen Macruz, Eduardo Jorge Pilau, Ezilda Jacomassi, and Odair Alberton. 2025. "Seasonal Evaluation and Effects of Poultry Litter-Based Organic Fertilization on Sustainable Production and Secondary Metabolism of Cuphea carthagenensis (Jacq.) J. F. Macbr" Sustainability 17, no. 23: 10801. https://doi.org/10.3390/su172310801

APA Style

Ribeiro, J. K. O., Pinc, M. M., Baisch, R. G., Barbosa, M. P. d. S. B., Hoscheid, J., Rezende, M. K. A., Macruz, P. D., Pilau, E. J., Jacomassi, E., & Alberton, O. (2025). Seasonal Evaluation and Effects of Poultry Litter-Based Organic Fertilization on Sustainable Production and Secondary Metabolism of Cuphea carthagenensis (Jacq.) J. F. Macbr. Sustainability, 17(23), 10801. https://doi.org/10.3390/su172310801

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