Next Article in Journal
Mycobiota of Mexican Maize Landraces with Auxin-Producing Yeasts That Improve Plant Growth and Root Development
Next Article in Special Issue
Silicon Induces Heat and Salinity Tolerance in Wheat by Increasing Antioxidant Activities, Photosynthetic Activity, Nutrient Homeostasis, and Osmo-Protectant Synthesis
Previous Article in Journal
Reduction in Nitrogen Rate and Improvement of Nitrogen Use Efficiency without Loss of Peanut Yield by Regional Mean Optimal Rate of Chemical Fertilizer Based on a Multi-Site Field Experiment in the North China Plain
Previous Article in Special Issue
Medicago sativa L. Plant Response against Possible Eustressors (Fe, Ag, Cu)-TiO2: Evaluation of Physiological Parameters, Total Phenol Content, and Flavonoid Quantification
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Plants
Volume 12
Issue 6
10.3390/plants12061327
plants-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Biostimulant and Elicitor Responses to Cricket Frass (Acheta domesticus) in Tomato (Solanum lycopersicum L.) under Protected Conditions

by
Ema Alejandra Ferruzca-Campos
1,
Amanda Kim Rico-Chavez
1,
Ramón Gerardo Guevara-González
1,
Miguel Urrestarazu
2,
Tatiana Pagan Loeiro Cunha-Chiamolera
2,
Rosalía Reynoso-Camacho
3 and
Rosario Guzmán-Cruz
4,*
1
Centro de Investigaciones Aplicadas en Biosistemas (CIAB), Facultad de Ingeniería, Campus Amazcala, Universidad Autónoma de Querétaro, Carr. Chichimequillas-Amazcala Km 1 S/N, Amazcala, Querétaro 76265, Mexico
2
Centro de Investigación en Agrosistemas Intensivos Mediterraneos y Biotecnología Agroalimentaria (CIAIMBITAL), Universidad de Almería, 04120 Almería, Spain
3
Facultad de Química, Universidad Autónoma Querétaro, Cerro de las Campanas S/N, Querétaro 76010, Mexico
4
Cuerpo Académico de Bioingeniería Básica y Aplicada, Facultad de Ingeniería, Campus Amazcala, Universidad Autónoma de Querétaro, Carr. Chichimequillas-Amazcala Km 1 S/N, Amazcala, Querétaro 76265, Mexico
*
Author to whom correspondence should be addressed.
Plants 2023, 12(6), 1327; https://doi.org/10.3390/plants12061327
Submission received: 22 February 2023 / Revised: 4 March 2023 / Accepted: 9 March 2023 / Published: 15 March 2023
(This article belongs to the Special Issue Eustressors to Enhance Plant Performance)
Browse Figures
Review Reports Versions Notes

Abstract

:
Agriculture in the current century is seeking sustainable tools in order to generate plant production systems with minimal negative environmental impact. In recent years it has been shown that the use of insect frass is an option to be used for this purpose. The present work studied the effect of low doses (0.1, 0.5, and 1.0% w/w) of cricket frass (Acheta domesticus) in the substrate during the cultivation of tomatos under greenhouse conditions. Plant performance and antioxidant enzymatic activities were measured in the study as explicative variables related to plant stress responses in order to determine possible biostimulant or elicitor effects of cricket frass treatments during tomato cultivation under greenhouse conditions. The main findings of this study indicated that tomato plants responded in a dose dependent manner to cricket frass treatments, recalling the hormesis phenomenon. On the one hand, a 0.1% (w/w) cricket frass treatment showed typical biostimulant features, while on the other hand, 0.5 and 1.0% treatments displayed elicitor effects in tomato plants under evaluated conditions in the present study. These results support the possibility that low doses of cricket frass might be used in tomato cultivation (and perhaps in other crops) for biostimulant/elicitor input into sustainable production systems.

1. Introduction

Current agriculture demands plant production systems that mainly use inputs that are not toxic to the environment or to living beings, and that increase crop stress tolerance and their nutritional quality [1]. Any input supporting the abovementioned should be welcomed and included in current agricultural production systems. In the last decade in Europe and for the last five years in the United States of America, a series of natural products derived from cellular components of plants, animals, or microorganisms have been successfully used, known as biostimulants or elicitors. These products, depending on the dose, significantly improve the physiology of the plants for growth and development (biostimulant) and strengthen their immune systems (elicitor) in such a way that the plants display an eustressic behavior. Such biostimulants are viable without having to apply them in the quantities usually used of toxic synthetic agrochemicals, thus producing results with minimal levels of toxicity or even without detected toxicity to the environment or living beings [1]. Biostimulant and elicitor agents that have been used in agriculture are cell extracts (microalgae, plants, etc.), microorganisms that promote plant growth, chemical substances of natural origin such as jasmonic acid, salicylic acid, hydrogen peroxide, fragmented DNA, chitin, and chitosan, among others [1,2,3]. These substances have shown the mentioned effects when applied via foliar or irrigation during cultivation in commercially important species such as chili and tomato [3,4].
The use of biostimulants and elicitors can help to obtain high-quality seedlings [1,2,3,4]. Effects of the application of biostimulants were evaluated—with and without inoculation of Trichoderma harzianum—on growth in passion fruit seedlings, where the number of leaves (NH), plant height (AP), chlorophyll index (CI), root length (LR), dry weight of the aerial part (PSPA) and the root part (PSPR) were considered. This study concluded that the application of biostimulants positively affected the biometric NH and PSPR variables in comparison to control [5]. Other studies investigated the effects of the seaweed concentrate ‘Kelpak’ on the growth and mineral nutrition of lettuce plants grown under conditions of varying nutrient supply. Kelpak significantly increased the yield, concentration, and amounts of Ca, K, and Mg in the leaves of lettuce, achieving an adequate supply of nutrients [6].
Thus, bioproducts containing live microorganisms or natural compounds derived from organisms, such as bacteria, fungi, and algae, improve plant growth and restore soil fertility [7]. Another alternative is to evaluate formulations derived from chitin (and other carriers of microorganisms beneficial to plant growth) that are also used as biostimulants in agriculture [8]. Chitin is obtained by recycling exoskeleton waste from crustacean shrimp, crabs, and crickets [9]. The most widely used derivative in agriculture is chitosan, the N-deacetylation of chitin obtained under alkaline conditions [10,11]. The beneficial effects of chitosan have been previously reported to promote plant growth and increase tolerance to biotic and abiotic stress [12]. In recent years, the use of insects as food has led to an increase in the number of private companies dedicated to the production of insect-derived products [13]. An essential part of the mass-rearing process is the production of frass (insect excreta) by insects, which supposes an important end product within the system that might be considered an organic fertilizer and food for livestock farms; although under-exploited, such frass is has possibilities for use as agricultural input [14,15].
The present research aimed to evaluate the biostimulant and elicitor potential of frass derived from the intensive cultivation of crickets (Acheta domesticus) in a substrate for the production of tomato (Solanum lycopersicum) under protected conditions. Some morphological characteristics such as plant height, basal stem diameter, and leaf number, as well as some antioxidant enzyme producers such as superoxide dismutase (SOD), catalase (CAT), and phenylalanine ammonium lyase (PAL), all related to plant stress responses, were evaluated as plant immunity markers. Our results displayed that depending on the dose, the cricket frass amendment in the substrate displayed a hormetic curve behavior in the evaluated variables. Treatment 0.1% (w/w) showed biostimulant features, while 0.5 and 1.0% treatments displayed elicitor effects in tomato plants under evaluated conditions. The results suggested the possibility of proposing a new product for sustainable production agriculture based on cricket frass and give value to a residue from the production of crickets for human consumption.

2. Results

2.1. Effect of Cricket Frass on Plant Morphological Variables in Tomato

The results obtained from the morphological variables for each treatment and control is shown in Figure 1. As observed, it demonstrated a linear growth of the morphological variables during the crop development evaluated. On the one hand, it can be seen that the treatment in which the substrate is composed of 99.9% sand and 0.1% frass displayed a biostimulant effect. The former asseveration was based on the results of the tomato plants in morphological variables related to an eustressic plant performance, with significantly higher height, basal diameter, and number of leaves compared to the control. On the other hand, the treatments where the percentage of frass was 0.5% and 1%, showed a likely elicitor effect since the plants reached a significantly lower height, basal diameter, and number of leaves, thus trending to a distressic behavior compared to the control (Figure 1); however, no apparent visual symptoms of toxicity were observed.
The Analysis of Variance for the morphological variables of the plants reaffirmed observations regarding differences in treatment among plants in terms of their heights, the basal diameter of their stems, and the number of their leaves. Therefore, the Tukey Test was performed to compare all possible combinations of pairs of means, and it was found that there were statistically significant differences among the treatments that these means represent (Table 1).
The effects on morphological characteristics of tomato plants shown by cricket frass applications evaluated suggest that depending on the dose, the effect might be that of a biostimulant (0.1% frass), displaying a higher behavior in the three morphological variables evaluated as shown in the regression study displayed in Figure 1 and Table 1. Moreover, frass doses of 0.5 and 1% showed decreased behavior in the same analysis compared to the control, likely suggesting that instead of plant biomass production, the plant is allocating energy for immunity to cope with stress conditions (elicitation), although not significantly affecting plant performance.

2.2. Effect of Cricket Frass on Plant Antioxidant Enzymatic Immunity Markers

In order to characterize in more detail the response of tomato plants to different cricket frass doses, the Analysis of Variance determined that commonly evaluated antioxidant enzymes be considered plant immunity markers. All data are presented as the mean ± SD (Figure 2). The evaluated enzymes related to stress response were phenylalanine ammonia lyase (PAL), catalase (CAT) and superoxide dismutase (SOD), the former being a key enzyme in the phenylpropanoids (PPDs) synthesis, while CAT and SOD participate in the scavenging of reactive oxygen species (ROS) during plant stress responses [16]. The results shown in Figure 2 display, on the one hand, that in comparison to control, treatment with 0.1% frass displayed a significant decrease for PAL activity, as well as a significant increase in CAT activity; SOD activity was not different in comparison to control. On the other hand, the treatment with 1% frass showed the highest decrease and increase for PAL and CAT activities, respectively, with no difference in SOD in comparison to the control (Figure 2). These results together suggest that treatments with 0.5% and 1% frass caused a decrease in phenylpropanoids production. The resources saved in this task are probably being used for plant growth in the case of the biostimulant treatment (0.1% frass), and preferentially to produce another type of secondary metabolite different from PPDs (i.e., terpenes, alkaloids) related to defense instead of to plant growth in the case of elicitor treatment (1% frass).
Moreover, in the present research, it was found that the use of cricket frass in low doses (0.1–1%) within the substrate displayed a hormetic effect such as biostimulant or elicitor behavior in the tomato plant’s morphological and biochemical variables related to the plant stress response being evaluated (Figure 3).

3. Discussion

Although the abovementioned results showed that cricket frass improved plant performance and, probably, the elicitation features in the tomato plants evaluated, this behavior depended on the week of the measurement (Figure 1 and Table 1). Changes in morphological characteristics displayed a trend to behave like control plants. Similar results were obtained in applying elicitation to chili peppers, a phenomenon in which the plant’s developmental stage might be explained regarding the response to external stress factors applied to the plants during cultivation [16].
Taken together, the effects on morphological characteristics and antioxidant enzyme activities of tomato plants shown by the evaluated cricket frass applications suggested that depending on the dose, the plants might lean toward eustressic or distressic behavior. This indicates the possibility that the hormetic phenomenon is participating in the experimental model evaluated. Biostimulant frass (0.1%) displayed improved behavior in the morphological variables evaluated. On the other hand, frass doses of 0.5 and 1% showed worsened behavior in the same analysis compared to the control, likely suggesting that instead of plant biomass production, the plant is allocating energy for immunity to cope with stress conditions (elicitation), although this does not significantly affect plant performance (Figure 4).
Both biostimulation and elicitation are positive plant responses that, based on the hormesis phenomenon, can be defined as part of the eustress zone in the biphasic hormetic curve [1,17]. The case of elicitation is interesting to highlight because if it is excessive, the plant will be in distress, thus showing symptoms of toxicity as suggested above [1,18]. It is likely that the level of nutrients (or possibly another component not analyzed in the frass, i.e., levels of chitin residues) that cricket frass contains (Table 2) provides a type of “alert cue” in the plants that also participate in inducing the plant stress response observed at morphological levels.
As the results suggest, the treatments with 0.5% and 1% of cricket frass in the substrate caused a decrease in the production of phenylpropanoids. Probably the resources saved in this task are being used for plant growth, as occurs in the case of the 0.1% frass treatment (biostimulant), and preferably to produce other types of secondary metabolites different from PPDs related to defense instead of to growth in the treatment of 1% frass (elicitor). The latter asseveration suggests that depending on the dose, the cricket frass is causing the trade-off commonly reported in the application of stress factors to plants, provoking hormesis [16]. The CAT activity results with both frass treatments also support the abovementioned, because the treatment with the highest CAT activity (1% frass) suggests high H2O2 (ROS) detoxification activity that is provoking elicitation in such a way that the hormetic behavior is related to the distress zone; while for treatment with 0.1% frass, although significantly higher in comparison to control, is likely generating an H2O2 level in the range of the eustress zone in a hormetic curve related to biostimulation [19]. The fact that SOD activity was not different from control in both frass treatments suggests that the H2O2 (ROS) production as stress response caused by frass in the tomato plants evaluated in this work, is perhaps mainly caused by other enzymes, such as plasma membrane NADPH oxidases, peroxisonal oxidases, type III peroxidases, and other apoplastic oxidases [20].
Recent studies by other authors using insect frass (HexafrassTM) showed that depending on the plant variable evaluated, a hormetic effect was observed; even a dose of 6 g per pot of chicory and ribwort showed high toxicity on shoot growth and yield [21]. Although our study lasted a short time (60 days) in relation to the complete cultivation cycle of tomatos, the results showed that based on the hormetic responses observed, it would be possible to evaluate in future work the possibility that this frass residue could be evaluated in complete cultivation cycles to determine its effects on fruit yield and quality, as well as on plant protection against pest and diseases—and even as a fertilizer source, based on its composition shown in Table 2. These future studies should consider the fact that insect frass might also have a positive effect on plants because it is a vector of beneficial microorganisms (not evaluated in the present work). Ref [22] conducted a study using mealworm frass, which found an increase in tolerance to biotic and abiotic stress of seedlings against drought, floods, and salinity, due to the sterilization of excrement, identifying numerous bacterial and fungal isolates capable of fixing atmospheric nitrogen, solubilizing phosphates and potassium, and producing siderophores, auxins, and 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase. Ref. [23] found that the excreta of different herbivorous insects were capable of activating the defensive responses of the plant mediated by salicylic acid and jasmonic acid. Ref. [24] found that the microorganisms present in insect droppings can activate the defensive responses of the S. frugiperda corn plant, since the bacterium Pantoea ananatis was isolated and identified in insect droppings, demonstrating its ability to increase the expression in the plant of the gene that codes for the inhibitor of the proteinase of maize induced by herbivores (mpi), which causes a decrease in attacks of the insect.

4. Materials and Methods

4.1. Plant Growth Conditions and Fertigation

The experiment was carried out in controlled growth under a greenhouse of 30 m2 located in Amazcala, Querétaro (Mexico). On 15 April 2022, seedlings were transplanted into individual 500-mL containers filled with coconut fiber substrate, whose physicochemical characteristics were described by [25]. The experiment ended on 15 June 2022. During the experimentation within the greenhouse, the temperature was 25 to 18 °C/18 to 16 °C (day/night, respectively) with a relative humidity of 80 to 85%. The nutrient solution was based on a standard nutrient solution of [26]. The pH of the nutrient solutions was always maintained at 5.8 with the addition of nitric acid; the amount of nitric acid required always increased nitrate to a negligible extent. New fertigation was applied when the water in the crop unit reached 10% of the easily available water [27,28,29].

4.2. Frass Nutrient Characteristics

The levels of macro and micronutrients and the levels of secondary elements were determined in a commercial laboratory (Fertilab-Celaya, México) using standard methods for each chemical element. The results and the method that the commercial laboratory uses to measure each chemical element are shown in Table 2.

4.3. Treatments

For the study, treatments corresponding to mixtures of inert substrate (sand): frass (w/w) in the proportions 99:1, 99.5:0.5, and 99.9:0.1 were carried out; as the control, 100% sand was evaluated. Twenty-four seedlings of the Saladette type tomato were transplanted in triplicate on these mixtures with 6–8 true leaves per each treatment (n = 24). Plants were located within bags with 3 kg of each treatment, and the study used a planting density of 2 plants m2 distributed in a random block design in the greenhouse (8 plants per block). The plants were grown in the greenhouse. Watering with a nutrient solution irrigated the substrate every 2 d with 300 mL of nutrient solution. The nutrient solution was prepared using highly soluble fertilizer salts to obtain the next ion concentration: 12 meq L−1 of NO3−; 1 meq L−1 of H2PO4−; 7 meq·L−1 of SO4−2; 7 meq L−1 of K+; 9 meq L−1 of Ca+2; and 4 meq L−1 of Mg+2. The pH of the nutrient solution was kept at 6 ± 0.2, and the electrical conductivity was kept between 1.6 and 1.8 dS mL−1. The production system lasted two months in the greenhouse.

4.4. Determination of Plant Morphological Characteristics

Morphometric measurements of height, basal stem diameter, and leaf number in the plants were taken weekly. The plant height was measured using a ruler from the base to the tip of the shoot, the basal stem diameter was measured with a digital vernier, and the numbers of leaves were counted according to [30].

4.5. Antioxidant Enzyme Activities

4.5.1. Superoxide Dismutase (SOD) Enzyme Activity

Samples consisting of 9 leaves from 3 different plants from each block were taken to perform biochemical antioxidant enzyme activity analyses for each treatment. SOD activity was determined by a modified method according to [31]. The plant material was thoroughly ground with liquid nitrogen; then 0.3 g of plant powder was separately homogenized in 2 mL of 50 mM phosphate buffer (pH 7.8) at 4 °C. The homogenate was vortexed for 2 min and then centrifuged for 15 min at 12,000 rpm min−1 at 4 °C. The supernatant was the enzyme extract used to determine the enzyme activity. Test tubes were added, each containing: 1.5 mL of phosphate buffer (pH 7.8), 0.3 mL of 0.1 mM EDTA-Na2, 0.3 mL of 0.13 M methionine, 0.3 mL of 0.02 riboflavin, 0.3 mL of 0.75 mM nitroblue tetrazolium (NBT), and 0.25 mL distilled water. The reaction was initiated by adding 0.05 mL enzyme extract to each tube and incubating for 30 min at 25 °C under white light exposure. Finally, each absorbance was recorded at 560 nm against a blank. One unit of SOD was expressed as the amount of protein that caused a 50% reduction of NBT in the reaction, and the enzyme activity was expressed as unit mg−1 protein.

4.5.2. Catalase (CAT) Enzyme Activity

Catalase activity was determined according to the method reported by [32] with some modifications. The basis was the decrease in absorbance at 240 nm caused by the decomposition of H2O2 by the catalase enzyme. The enzyme extract was obtained by homogenizing 0.3 g of frozen plant material in 2 mL of a 100 mM Tris-HCl buffer (pH 8) containing 30 mM 2-mercaptoethanol and 20% (v/v) glycerol at 4 °C. The homogenate was vortexed for 2 min and centrifuged for 15 min at 12,000 rpm at 4 °C. The supernatant was the enzyme extract used for the activity test. For measuring CAT activity, 0.1 mL of the enzyme extract was added to test tubes containing 2 mL of 50 mM phosphate buffer and 0.2 mL of 100 mM H2O2. The change in absorbance of the reaction mixture was determined by measuring the absorbance every minute for 6 min. The CAT activity was calculated as the H2O2 extinction coefficient of 0.0392 mM cm−1 and expressed as mmol H2O2 mg−1 protein.

4.5.3. Phenylalanine Ammonium Lyase (PAL) Activity

PAL activity was determined by the method reported by [33] with some modifications. First, 0.3 g of each frozen sample was homogenized in 2 mL of 0.1 M sodium borate buffer containing 0.1% 2-mercaptoethanol (pH 8.8) at 4 °C. The extract was vortexed for 2 min and then centrifuged at 12,000 rpm for 15 min at 4 °C. The supernatant was the enzyme extract for the activity test. PAL activity was analyzed as the ratio of conversion of L-phenylalanine to trans-cinnamic acid at 290 nm in a UV–Vis spectrophotometer. Samples containing 0.2 mL of the enzyme extract were added to 2.3 mL of sodium borate buffer (pH 8.8) containing 10 mM L-phenylalanine. The reaction mixture was incubated at 40 °C for 60 min. After the incubation time, the reaction was forced to stop by adding 0.5 mL of 1 N HCl and left for 10 min. The absorbance was measured at 290 nm, and the values were compared to a 7-point trans-cinnamic acid calibration curve.

4.6. Statistical Analysis

For the statistical analysis, the Analysis of Variance (ANOVA) was performed. With the ANOVA, each of the morphological and biochemical variables were measured in various groups of tomato plants, each of which receives a different dose of cricket frass: 0% (control), 0.1%, 0.5%, and 1%. The Tukey’s HDS post hoc test was performed for each experiment to determine statistical differences using the software STATGRAPHICS XV. A p ˂ 0.05 was considered significant.

5. Conclusions

Taken together, our results suggest that cricket frass under the evaluated conditions in the present work, when less than 1% is used in the substrate, displayed either a biostimulant (0.1%) or elicitor (0.5 and 1.0%) effect on tomato crops. Both the biostimulant or elicitor effects were reflected in the morphology and antioxidant enzyme activities evaluated, showing improved features in relation to the control. Future research studying insect frass, in addition to increasing insight into using it as a biostimulant/elicitor in other crops as sustainable agricultural input, should also include research into the possibility of the frass being used as fertilizer, based on the essential chemical elements composition it displays.

Author Contributions

Conceptualization and methodology, R.G.G.-G., R.R.-C. and R.G.-C.; experimentation and data collection, E.A.F.-C.; validation, M.U. and T.P.L.C.-C.; formal analysis, investigation, A.K.R.-C. and R.G.-C.; writing—review and editing, A.K.R.-C., R.G.G.-G. and R.G.-C.; funding acquisition, R.G.-C. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Faculty of Engineering for funding this research through of the Call for Attention to National Problems, grant number FIN202105.

Data Availability Statement

Not applicable.

Acknowledgments

To Agroinsects S.A. of C.V. for the donation of cricket frass to this research.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Vázquez-Hernández, M.C.; Parola-Contreras, I.; Montoya-Gómez, L.M.; Torres-Pacheco, I.; Schwarz, D.; Guevara-González, R.G. Eustressors: Chemical and physical stress factors used to enhance vegetables production. Sci. Hortic. 2019, 250, 223–229. [Google Scholar] [CrossRef]
  2. Vargas-Hernandez, M.; MAcias-Bobadilla, I.; Guevara-Gonzalez, R.G.; de Romero-Gomez, S.J.; Rico-Garcia, E.; Ocampo-Velazquez, R.V.; de Alvarez-Arquieta, L.L.; Torres-Pacheco, I. Plant hormesis management with biostimulants of biotic origin in agriculture. Front. Plant Sci. 2017, 8, 1762. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. Solano-Alvarez, N.; Valencia-Hernández, J.A.; Rico-García, E.; Torres-Pacheco, I.; Ocampo-Velázquez, R.V.; Escamilla-Silva, E.M.; Romero-García, A.L.; Alpuche-Solís, Á.G.; Guevara-González, R.G. A novel isolate of bacillus cereus promotes growth in tomato and inhibits clavibacter michiganensis infection under greenhouse conditions. Plants 2021, 10, 506. [Google Scholar] [CrossRef] [PubMed]
  4. Mejía-Teniente, L.; Durán-Flores, B.A.; Torres-Pacheco, I.; González-Chavira, M.M.; Rivera-Bustamante, R.F.; Feregrino-Perez, A.A.; Pérez-Ramírez, I.; Rocha-Guzmán, N.E.; Reynoso-Camacho, R.; Guevara-González, R.G. Hydrogen peroxide protects pepper (Capsicum annuum L.) against pepper golden mosaic geminivirus (PepGMV) infections. Physiol. Mol. Plant Pathol. 2019, 106, 23–29. [Google Scholar] [CrossRef]
  5. Díaz, G.; Rodríguez, G.; Montana, L.; Miranda, T.; Basso, C.; Arcia, M. Efecto de la aplicación de bioestimulantes y Trichoderma sobre el crecimiento en plántulas de maracuyá (Passiflora edulis Sims) en vivero. Bioagro 2020, 32, 195–204. [Google Scholar]
  6. Crouch, I.J.; Beckett, R.P.; van Staden, J. Effect of seaweed concentrate on the growth and mineral nutrition of nutrient-stressed lettuce. J. Appl. Phycol. 1990, 2, 269–272. [Google Scholar] [CrossRef]
  7. Sadiqi, S.; Hamza, M.; Ali, F.; Alam, S.; Shakeela, Q.; Ahmed, S.; Ayaz, A.; Ali, S.; Saqib, S.; Ullah, F.; et al. Molecular Characterization of Bacterial Isolates from Soil Samples and Evaluation of their Antibacterial Potential against MDRS. Molecules 2022, 27, 6281. [Google Scholar] [CrossRef]
  8. Pereira, J.F.; Oliveira, A.L.M.; Sartori, D.; Yamashita, F.; Mali, S. Perspectives on the Use of Biopolymeric Matrices as Carriers for Plant-Growth Promoting Bacteria in Agricultural Systems. Microorganisms 2023, 11, 467. [Google Scholar] [CrossRef]
  9. El Amerany, F.; Meddich, A.; Wahbi, S.; Porzel, A.; Taourirte, M.; Rhazi, M.; Hause, B. Foliar application of chitosan increases tomato growth and influences mycorrhization and expression of endochitinase-encoding genes. Int. J. Mol. Sci. 2020, 21, 535. [Google Scholar] [CrossRef] [Green Version]
  10. Kumar, R.M.N.V. A review of chitin and chitosan applications. React. Funct. Polym. 2000, 46, 1–27. [Google Scholar] [CrossRef]
  11. Antony, R.; Arun, T.; Manickam, S.T.D. A review on applications of chitosan-based Schiff bases. Int. J. Biol. Macromol. 2019, 129, 615–633. [Google Scholar] [CrossRef] [PubMed]
  12. Saqib, S.; Zaman, W.; Ayaz, A.; Habib, S.; Bahadur, S.; Hussain, S.; Muhammad, S.; Ullah, F. Postharvest disease inhibition in fruit by synthesis and characterization of chitosan iron oxide nanoparticles. Biocatal. Agric. Biotechnol. 2020, 28, 101729. [Google Scholar] [CrossRef]
  13. Van Huis, A. Insects as food and feed, a new emerging agricultural sector: A review. J. Insects Food Feed 2020, 6, 27–44. [Google Scholar] [CrossRef] [Green Version]
  14. Cortes Ortiz, J.A.; Ruiz, A.; Morales-Ramos, J.; Thomas, M.; Rojas, M.G.; Tomberlin, J.K.; Yi, L.; Han, R.; Giroud, L.; Jullien, R.L. Chapter 6—Insect Mass Production Technologies. In Insects as Sustainable Food Ingredients: Production, Processing and Food Applications; Dossey, A.T., Morales-Ramos, J.A., Rojas, M.G.B.T., Eds.; Academic Press: San Diego, CA, USA, 2016; pp. 153–201. [Google Scholar] [CrossRef]
  15. Wang, H.; Rehman, K.; Liu, X.; Yang, Q.; Zheng, L.; Li, W.; Cai, M.; Li, Q.; Zhang, J.; Yu, Z. Biotechnology for Biofuels Insect biorefinery: A green approach for conversion of crop residues into biodiesel and protein. Biotechnol. Biofuels 2017, 10, 304. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  16. Carbajal-Valenzuela, I.A.; Guzmán-Cruz, R.; González-Chavira, M.M.; Medina-Ramos, G.; Serrano-Jamaica, L.M.; Torres-Pacheco, I.; Vázquez, L.; Feregrino-Pérez, A.A.; Rico-García, E.; Guevara-González, R.G. Response of Plant Immunity Markers to Early and Late Application of Extracellular DNA from Different Sources in Tomato (Solanum lycopersicum). Agriculture 2022, 12, 1587. [Google Scholar] [CrossRef]
  17. Ferrusquía-Jiménez, N.I.; González-Arias, B.; Rosales, A.; Esquivel, K.; Escamilla-Silva, E.M.; Ortega-Torres, A.E.; Guevara-González, R.G. Elicitation of Bacillus cereus-Amazcala (B.c-A) with SiO2 Nanoparticles Improves Its Role as a Plant Growth-Promoting Bacteria (PGPB) in Chili Pepper Plants. Plants 2022, 11, 3445. [Google Scholar] [CrossRef]
  18. Magaña-López, E.; Palos-Barba, V.; Zuverza-Mena, N.; Vázquez-Hernández, M.C.; White, J.; Nava-Mendoza, R.; Feregrino-Pérez, A.A.; Torres-Pacheco, I.; Guevara-González, R.G. Nanostructured mesoporous silica materials induce hormesis on chili pepper (Capsicum annuum L.) under greenhouse conditions. Heliyon 2022, 8, e09049. [Google Scholar] [CrossRef]
  19. Vargas-Hernandez, M.; Ferrusquia-Jimenez, N.I. Introducción a la teoría del estrés e inmunología vegetal. In Manejo del Estrés Vegetal como una Estrategia para una Agricultura Sostenible; Guevara-González, R.G., Torres-Pacheco, I., Eds.; Editorial Universidad de Almería: Almería, Spain, 2022; pp. 53–101. [Google Scholar]
  20. Smirnoff, N.; Arnaud, D. Hydrogen peroxide metabolism and functions in plants. New Phytol. 2019, 221, 1197–1214. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  21. Hodge, S.; Conway, J. The Effects of Insect Frass Fertilizer and Biochar on the Shoot Growth of Chicory and Plantain, Two Forage Herbs Commonly Used in Multispecies Swards. Agronomy 2022, 12, 2459. [Google Scholar] [CrossRef]
  22. Poveda, J.; Jiménez-Gómez, A.; Saati-Santamaría, Z.; Usategui-Martín, R.; Rivas, R.; García-Fraile, P. Mealworm frass as a potential biofertilizer and abiotic stress tolerance-inductor in plants. Appl. Soil Ecol. 2019, 142, 110–122. [Google Scholar] [CrossRef]
  23. Ray, S.; Alves, P.C.M.S.; Ahmad, I.; Gaffoor, I.; Acevedo, F.E.; Peiffer, M.; Jin, S.; Han, Y.; Shakee, S.; Felton, G.W.; et al. Turnabout is fair play: Herbivory-induced plant chitinases excreted in fall armyworm frass suppress herbivore defenses in maize. Plant Physiol. 2016, 171, 694–706. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Acevedo, F.E.; Peiffer, M.; Tan, C.W.; Stanley, B.A.; Stanley, A.; Wang, J.; Jones, A.G.; Hoover, K.; Rosa, C.; Luthe, D.; et al. Fall armyworm-associated gut bacteria modulate plant defense responses. Mol. Plant-Microbe Interact. 2017, 30, 127–137. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Pozo, J.; Juan, E.A.; Morales, I.; Requena, J.; La Malfa, T. A New Local Sustainable Inorganic Material for Soilless Culture in Spain: Granulated Volcanic Rock. HortScience 2014, 49, 1537–1541. [Google Scholar] [CrossRef]
  26. Sonneveld, C.; Straver, N. Nutrient solutions for vegetables and flowers grown in water or substrates. Voedingsoploss. Glastuinb 1994, 10, 45. Available online: http://edepot.wur.nl/237302%0Ahttps://agris.fao.org/agris-search/search.do?recordID=NL8901262 (accessed on 1 April 2022).
  27. Da Cunha-Chiamolera, T.P.L.; Urrestarazu, M.; Filho, A.B.C.; Morales, I. Agronomic and economic feasibility of tomato and lettuce intercropping in a soilless system as a function of the electrical conductivity of the nutrient solution. HortScience 2017, 52, 1195–1200. [Google Scholar] [CrossRef] [Green Version]
  28. Rodríguez, D.; Reca, J.; Martínez, J.; Lao, M.T.; Urrestarazu, M. Effect of controlling the leaching fraction on the fertigation and production of a tomato crop under soilless culture. Sci. Hortic. 2014, 179, 153–157. [Google Scholar] [CrossRef]
  29. Urrestarazu, M.; Gallegos, V.; Álvaro, J.E. The Use of Thermography Images in the Description of the Humidification Bulb in Soilless Culture. Commun. Soil Sci. Plant Anal. 2017, 48, 1595–1602. [Google Scholar] [CrossRef] [Green Version]
  30. Sáenz-de la, O.D.; Morales, L.O.; Strid, Å.; Torres-Pacheco, I.; Guevara-González, R.G. Ultraviolet-B exposure and exogenous hydrogen peroxide application lead to cross-tolerance toward drought in Nicotiana tabacum L. Physiol. Plants 2021, 173, 666–679. [Google Scholar] [CrossRef] [PubMed]
  31. Hayat, S.; Ahmad, H.; Ali, M.; Ren, K.; Cheng, Z. Aqueous garlic extract stimulates growth and antioxidant enzymes activity of tomato (Solanum lycopersicum). Sci. Hortic. 2018, 240, 139–146. [Google Scholar] [CrossRef]
  32. Afiyanti, M.; Chen, H.J. Catalase activity is modulated by calcium and calmodulin in detached mature leaves of sweet potato. J. Plant Physiol. 2014, 171, 35–47. [Google Scholar] [CrossRef]
  33. Toscano, S.; Ferrante, A.; Leonardi, C.; Romano, D. PAL activities in asparagus spears during storage after ammonium sulfate treatments. Postharvest. Biol. Technol. 2018, 140, 34–41. [Google Scholar] [CrossRef]
Plants 12 01327 g001 550
Figure 1. Dispersion diagram of morphological variables (a) height, (b) basal stem diameter, and (c) the number of leaves.
Figure 1. Dispersion diagram of morphological variables (a) height, (b) basal stem diameter, and (c) the number of leaves.
Plants 12 01327 g001
Plants 12 01327 g002 550
Figure 2. Effect of cricket frass on the (a) PAL, (b) SOD and (c) CAT enzyme activities in tomato plants. Different letters in each histogram for each enzyme indicate a statistically significant difference after two-way ANOVA (p < 0.05) and Tukey’s HDS test for multiple comparisons (95%). Error bars represent the standard deviation of the mean.
Figure 2. Effect of cricket frass on the (a) PAL, (b) SOD and (c) CAT enzyme activities in tomato plants. Different letters in each histogram for each enzyme indicate a statistically significant difference after two-way ANOVA (p < 0.05) and Tukey’s HDS test for multiple comparisons (95%). Error bars represent the standard deviation of the mean.
Plants 12 01327 g002
Plants 12 01327 g003 550
Figure 3. Dispersion diagram of morphological variables (a) height, (b) basal stem diameter, and (c) the number of leaves; and biochemical enzyme activities variables (d) PAL, (e) SOD and (f) CAT.
Figure 3. Dispersion diagram of morphological variables (a) height, (b) basal stem diameter, and (c) the number of leaves; and biochemical enzyme activities variables (d) PAL, (e) SOD and (f) CAT.
Plants 12 01327 g003
Plants 12 01327 g004 550
Figure 4. Graphical representation of the hormetic effect observed in tomato treated with frass in the substrate in the present study.
Figure 4. Graphical representation of the hormetic effect observed in tomato treated with frass in the substrate in the present study.
Plants 12 01327 g004
Table
Table 1. Morphological response of tomato plants to the addition of cricket Frass to the cultivation substrate.
Table 1. Morphological response of tomato plants to the addition of cricket Frass to the cultivation substrate.
Morphologic VariablesWeekControl0.1% Frass0.5% Frass1% Frass
Height114 a15 a14 a15 a
219 a20 a19 a20 a
326 a29 a24 a26 a
434 a,b41 a32 b32 b
540 a,b46 a38 a,b37 b
644 a,b51 a42 b42 b
758 a60 a51 a53 a
866 a68 a60 a62 a
Stem diameter13.24 a3.64 a3.33 a3.45 a
23.29 a3.69 a3.38 a3.50 a
33.33 a3.73 a3.42 a3.54 a
44.16 a,b4.58 a4.02 b4.11 b
54.22 a,b4.64 a4.07 b4.18 ab
65.02 a5.23 a4.82 a4.82 a
75.12 a5.33 a4.92 a4.92 a
85.25 a5.46 a5.05 a5.05 a
Number of leaves13 a4 a3 a3 a
23 a4 a3 a3 a
34 a5 a4 a4 a
47 a,b8 a6 b6 b
59 a,b10 a8 b8 b
67 a8 a6 a6 a
710 a11 a9 a9 a
812 a13 a11 a11 a
Different letters in each row (week of each treatment) indicate a statistically significant difference after a two-way ANOVA (p < 0.05) and a Tukey’s HDS test for multiple comparisons (95%).
Table
Table 2. Nutrient analysis of the cricket frass used in the study.
Table 2. Nutrient analysis of the cricket frass used in the study.
NutrientsElementUnitsResultsMethod
MacronutrientsTotal nitrogen%4.035MicroKjeldahl
Total Phosphorus (P2O5)%1.560Spectrophotometric
Potassium (K2O)%1.820Atomic absorption
Secondary elementsCalcium%1.340Atomic absorption
Magnesium%0.510Atomic absorption
Sulfur%0.699Turbidimetric
Sodium%0.620Atomic absorption
MicronutrientsIronppm334.040Atomic absorption
Cooperppm47.770Atomic absorption
Manganeseppm154.350Atomic absorption
Zincppm195.680Atomic absorption
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Ferruzca-Campos, E.A.; Rico-Chavez, A.K.; Guevara-González, R.G.; Urrestarazu, M.; Cunha-Chiamolera, T.P.L.; Reynoso-Camacho, R.; Guzmán-Cruz, R. Biostimulant and Elicitor Responses to Cricket Frass (Acheta domesticus) in Tomato (Solanum lycopersicum L.) under Protected Conditions. Plants 2023, 12, 1327. https://doi.org/10.3390/plants12061327

AMA Style

Ferruzca-Campos EA, Rico-Chavez AK, Guevara-González RG, Urrestarazu M, Cunha-Chiamolera TPL, Reynoso-Camacho R, Guzmán-Cruz R. Biostimulant and Elicitor Responses to Cricket Frass (Acheta domesticus) in Tomato (Solanum lycopersicum L.) under Protected Conditions. Plants. 2023; 12(6):1327. https://doi.org/10.3390/plants12061327

Chicago/Turabian Style

Ferruzca-Campos, Ema Alejandra, Amanda Kim Rico-Chavez, Ramón Gerardo Guevara-González, Miguel Urrestarazu, Tatiana Pagan Loeiro Cunha-Chiamolera, Rosalía Reynoso-Camacho, and Rosario Guzmán-Cruz. 2023. "Biostimulant and Elicitor Responses to Cricket Frass (Acheta domesticus) in Tomato (Solanum lycopersicum L.) under Protected Conditions" Plants 12, no. 6: 1327. https://doi.org/10.3390/plants12061327

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop