The objective of this study was to evaluate the effect of polyphenol reduction in a food formulated with Eisenia arborea and its effect on the feeding preference of the abalone Haliotis fulgens through multiple selection tests. Two foods were formulated: one without polyphenol reduction (EA01) and one with polyphenol reduction (EA02). Rehydrated E. arborea (ER03) was used as the control food. The polyphenol content was quantified in EA01 and EA02, and the stability and hardness of all three foods were measured at 24 h. Food preference was evaluated through attraction and consumption tests on day 1, 6, and 12. The polyphenol concentration was reduced by 41% in EA02 (13.9 mg GAE/g) compared to that of EA01 (33.3 mg GAE/g). Both formulated foods showed 88% stability and hardness values > 680 g cm− 2, which were greater than those of the control (ER03, 66% and 285 g cm− 2, respectively). Abalone were more attracted to EA02 and ER03 on day 1, 6, and 12 than to ER03 on the same days. A similar trend was observed with consumption. EA02 and ER03 were the most consumed foods (> 6 g/day) throughout the experiment, and no significant differences in consumption were observed between these foods. On the other hand, juvenile H. fulgens showed a greater attraction to and consumption of EA02 (reduced polyphenol content) than EA01 (no reduction in polyphenol content). This allows us to conclude that EA02 can replace rehydrated algae as a suitable food source for juvenile H. fulgens.
Research Article
Formulated algae-based food with low polyphenol content and its effect on the feeding preference of juvenile blue abalone Haliotis fulgens
https://doi.org/10.21203/rs.3.rs-2692970/v1
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brown algae
abalone
feeding preference
attraction
consumption
multiple selection test
Brown algae, , produce secondary metabolites to defend against biotic stressors, such as herbivory and epiphytism, and abiotic stressors such as excess of light and temperature. The production of polyphenolic compounds (e.g., phlorotannins) holds particular interest when evaluating this defense mechanism in the context of herbivory (Pavia & Toth 2000; Pereira et al. 2002; Lattanzio 2013; Abdala-Díaz et al. 2014). Polyphenolic compounds participate in various functions that include protecting organisms from detrimental light and oxygen exposure and defending against herbivory (Mekinić et al. 2019). In macroalgae, the production of defense compounds like polyphenols is constantly changing because algae respond to stimuli in multiple ways. For example, polyphenolic compounds, such as phlorotannins, are constantly produced by brown algae and are present in concentrations that vary between 5–30% of the dry weight of the seaweed (Singh & Sidana 2013; Venkatesan et al. 2018; Mekinić et al. 2019). However, when macroalgae are exposed to air or sunlight, the concentrations of these compounds have been found to significantly increase (Abdala-Díaz et al. 2014; Lemesheva & Tarakhovskaya 2018). A similar phenomenon has been observed when algae are subject to herbivory. For example, algae of the Fucus, Sargassum, and Ascophyllum genera have been observed to increase phlorotannin production in response to stress from herbivory (Jormalainen & Ramsay 2009; Singh & Sidana 2013; Kurr & Davies 2019).
Despite the anti-herbivory role that polyphenolic compounds play in macroalgae and their high concentrations in these seaweeds, brown algae are fundamental components of the diets of various gastropod mollusks such as abalone. Haliotis abalone pass through various developmental stages in which they feed on microalgae and then on green, red, and brown macroalgae (Viana 2000; Mazariegos-Villarreal et al. 2012). However, some Haliotis species are characterized by selective feeding behaviors, which are primarily associated with the polyphenol concentrations present in algae food sources (Conrwall et al. 2009; Angell et al. 2012). For example, in food preference evaluations using fresh algae, Haliotis midae Linnaeus 1758 (Stepto & Cook 1996), H. rubra Leach 1814 (Fleming 1995), H. asinina Linnaeus 1758 (Angell et al. 2012), and H. squamata Reeve 1846 (Yusup et al. 2020) have shown a greater preference for consuming red or green algae over brown algae. In contrast, H. tuberculata Linnaeus 1758 and H. iris Gmelin 1791 have shown a broad preference for red and brown algae over green algae, which suggests that the consumption of brown algae could depend on their degree of chemical defense (Conrwall et al. 2009; Roussel et al. 2020). Although studies have documented the consumption of brown algae by H. fulgens Philippi 1845 (Guzmán del Proo et al. 2003; Mazariegos-Villarreal et al. 2012), no information is currently available on the feeding preferences of this species based on the polyphenol content of the algae food source.
The green abalone, H. fulgens, is an important fisheries resource in northwestern Mexico, and products derived from this resource are considered to be of high quality. However, despite its commercial importance, the information available for H. fulgens remains limited. Indeed, no food preference studies have yet been conducted that evaluate the effect of reducing polyphenol content in formulated foods for H. fulgens, with previous studies employing fresh or rehydrated algae (e.g., Yusup et al. 2020; Roussel et al. 2020) with unaltered polyphenol content.
The consumption of brown algae by H. fulgens is notable, and it is quite possible that the polyphenol content of brown algae could influence the feeding behaviors of H. fulgens. The objective of this study was to evaluate the effect of polyphenol reduction in a food formulated with brown macroalgae and its effect on the feeding preference of juvenile H. fulgens through multiple selection tests that evaluated attraction and consumption. Ultimately, this study provides evidence that a new formulated food with reduced polyphenol content may be used in culture systems as an alternative to natural macroalgae food sources, which are not always available year-round. The formulated food, which meets specific nutritional requirements, resolves this issue, and may be employed during months when algae are in short supply.
Seaweed flour production and ethanol treatment
Eisenia arborea Areschough 1876, a brown macroalga, was collected from La Bocana in Baja California Sur (BCS), Mexico (26°, 46.411´ N; 113° 42.639´ W). The collected algae were cleaned to remove epiphytes, washed with fresh water to remove excess salt, and left to dry in the sun. Once dry, a portion of the collected algae was used to produce seaweed flour (4 kg) while the rest was used as a rehydrated food source (4 kg).
The production of seaweed flour involved grinding the dried E. arborea in a hammer mill and subsequently pulverizing (Pulvex 2000, Pulvex SA. de CV., Mexico City, Mexico) and sieving it (250 µ). To reduce the concentration of polyphenols, a portion (2 Kg) of the algae flour was treated with ethanol (EtOH). The treatment consisted of three 24-h ethanol washes at room temperature at an algae:ethanol ratio of 1:3.
Extraction and quantification of polyphenols from Eisenia arborea
Polyphenols were extracted from the ethanol-treated flour following the method of Kuda et al. (2007). Ethanol (80%) was used as the solvent at an algae:ethanol ratio of 1:20 and 75 °C. The solution remained under constant agitation for 20 min and was subsequently vacuum filtered. The filtrate was centrifuged at 1200 x g for 20 min (CENTU00370 Prolab Centrifuge, Centurion Scientific Ltd., Chichester, UK). The supernatant was decanted and concentrated under reduced pressure using a Rotovapor R II (Buchi, Flawil, Switzerland) at 45 °C. The resulting extract was stored at 4 °C until further use to determine the polyphenol content.
Polyphenol content was determined in triplicate with the Folin-Denis method based on the work of Hwang & Thi (2014). Each extract was diluted with 0.4 mL of Folin-Ciocalteu phenol reagent (2 N at 10%) and left to react for 3 min at room temperature. Then, 0.8 mL of 10% sodium carbonate was added, and the mixture was agitated and incubated in the dark for 1 h. Absorbance at 750 nm was measured using a 10s UV-Vis spectrophotometer (Genesys, Menlo Park, USA). The results are expressed as mg of gallic acid equivalent (GAE)/g of dry weight.
Diet development and formulation
Rationmix software v. 0.1 (2020) was used to formulate two foods from the E. arborea flour: EA01 and EA02 (Table 1). EA01 was made with untreated E. arborea flour, whereas EA02 was made with the ethanol-treated E. arborea flour with reduced polyphenol content. The nutritional content of EA01 and EA02 (Table 1) was adjusted based on the recommendation of Fleming et al. (1996). The proximate chemical composition of EA01 and EA02 was analyzed in triplicate following the official methods of the Association of Official Analytical Chemists (AOAC) utilizing the services of the University Center for Biological and Agricultural Sciences (CUCBA) in Jalisco, Mexico (Table 1). A third food consisting of rehydrated E. arborea (ER03) was used as the control. All foods were vacuum-packed until use.
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Table 1. Formulation and proximal chemical compositions of the three foods used in this study: a formulated food made with Eisenia arborea flour without reduced polyphenol content (EA01), a formulated food made with E. arborea flour with reduced polyphenol content (EA02), and a control consisting of rehydrated E. arborea (ER03). |
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|
Treatment |
|
|
|
|
EA01 |
EA02 |
ER03 |
|
|
Ingredients (g Kg-1) |
|
|
|
|
|
|
Natural flour E.a. |
666.9 |
--- |
--- |
|
|
Treated flour E.a |
--- |
666.9 |
--- |
|
|
Soy flour a |
133.0 |
133.0 |
--- |
|
|
Fish flour b |
150.0 |
150.0 |
--- |
|
|
PMC c |
50 |
50 |
--- |
|
Proximate chemical composition (%) |
|
|
||
|
|
Protein |
25.9 ± 0.8 |
25.6 ± 0.7 |
12.0 ± 0.6 |
|
|
Lipids |
5.4 ± 0.4 |
5.3 ± 0.5 |
3.4 ± 0.8 |
|
|
ELN |
38.8 ± 0.6 |
38.2 ± 0.3 |
50.3 ± 0.5 |
|
|
Fiber |
6.6 ± 0.6 |
6.1 ± 0.9 |
6.6 ± 0.8 |
|
|
Ash |
18.3 ± 0.5 |
18.7 ± 0.3 |
21.1 ± 0.6 |
Food stability and hardness
The stability and hardness of EA01, EA02, and ER03 were determined in triplicate. To determine stability, foods were immersed in water for 24 h and subsequently dried in a convection oven at 70 °C for 48 h. After which, the foods were weighed (g). The stability value was obtained using Eq. (1) based on the work of Pérez-Estrada (2006):
where Ar is the weight (g) of the recovered food and Ap is the weight (g) of the food provided. Hardness (g cm-2) was determined using a TA.XTplus digital texture analyzer (Stable Micro Systems Ltd., Godalming, UK) after the foods had been immersed for 24 h prior to oven drying.
Study organisms
A total of 450 juvenile blue abalone (37.82 ± 7.30 mm length, 7.30 ± 1.88 g) were donated by the fishing cooperative Sociedad Cooperativa Progreso de Producción Pesquera S.C. de R.L., which is located in La Bocana, BCS. The organisms were maintained under laboratory culture conditions (temperature: 20.5 ± 0.4 °C, salinity: 34 ± 0.6 PSU, pH: 8.1 ± 0.2, oxygen: 7.1 ± 0.8 mg L-1, and photoperiod: 24 h darkness) at the facilities of the Mariculture Pilot Unit (UPIMA) of the Centro Interdisciplinario de Ciencias Marinas (CICIMAR), which is located in La Paz, BCS, Mexico (24°08'27.3" N 110°21'06.4" W.
Experimental design
Prior to beginning the experiment, the abalone underwent a 30-day acclimatization period. The organisms were fasted for two days before the start of the experiment. Food preference was determined through multiple-choice selection tests, following the methodology of Dunstan et al. (2002) and Roussel et al. (2020) with modifications (Fig. 1). Briefly, circular 600-L tanks were used with water flow (200 L/h) and continuous aeration. The photoperiod during the experiment was 24 h of darkness. The attraction and consumption tests were conducted in triplicate with 150 organisms per tank.
Three devices were installed in each tank to provide food randomly every 24 h (Fig. 1). These devices were placed equidistantly along the periphery of each tank to ensure all abalone had equal access to food. The feeders consisted of a circular plastic base (circumference: 30 cm; Fig. 1) with an attached circular container (circumference: 15 cm, height: 0.5 mm) that contained the food (Fig. 1). The abalone remained near the center of the tank where they were provided with refuge.
Food preference: multiple-choice selection tests
The attraction and consumption of EA01, EA02, and ER03 were determined on day 1, 6, and 12 through multiple-choice selection tests. A total of 15 g of each food was provided each day, and excess food was removed after 24 h.
The attraction and consumption of EA01, EA02, and ER03 were determined on day 1, 6, and 12 through multiple-choice selection tests. A total of 15 g of each food was provided each day, and excess food was removed after 24 h. The leftover food was dried in a convection oven at 70 °C for 24 h and weighed. Consumption was determined using Eq. (2) from Uki & Watanabe (1992):
where G is the weight of the food provided (g), S is stability, and R is the weight of the leftover food (g).
Attraction was determined through visual observation and photography. Only organisms within the food container device were counted. Data were recorded at 2, 4, 6, 8, 10, and 12 h. In addition, precautions were taken to ensure that no light source affected the organisms during the observation periods.
Statistical analysis
Statistical analyses were performed in R (R Core Team, 2021) to compare the physical variables of hardness and stability and the food selection variables of attraction and consumption among the three food types. The data were tested for normality and homoscedasticity using the Shapiro-Wilk and Levene tests, respectively. As the data were normally distributed and showed homoscedasticity, a one-way ANOVA and Tukey post-hoc tests were utilized to analyze the data (Zar 2010).
The total polyphenol content of natural flour was 33.3 mg GAE/g and the ethanol-treated flour was19.4 mg GAE/g. This represent a reduction of 13.9 mg GAE/g in polyphenol content in the ethanol-treated flour, which is a decrease of 41.7% (Table 2).
The stability of the formulated foods differed significantly (p < 0.05; Table 3), with EA01 and EA02 showing the highest stability (> 88%) and ER03 showing the lowest stability (< 67%). This pattern was also observed with food hardness (p < 0.05), with EA01 (687.1 g cm-2) and EA02 (685.7 g cm-2) showing the higher hardness and ER03 showing the lowest hardness (285.2 g cm-2).
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Table 2. Total polyphenol content in the Eisenia arborea flour used to formulate EA01 and EA02. The results are expressed as mg of gallic acid equivalent (GAE)/g of dry weight |
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Seaweed flour |
Treatment |
mg GAE/g |
|
Natural E. arborea (EA01) |
--- |
33.3 ± 1.2 |
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Treated E. arborea (EA02) |
EtOH |
19.4 ± 1.1 |
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--- indicates no treatment. ± indicates standard deviation. |
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Table 3. Stability (%) and hardness (g cm-2) of the three foods used in this study: a formulated food made with Eisenia arborea flour without reduced polyphenol content (EA01), a formulated food made with E. arborea flour with reduced polyphenol content (EA02), and a control consisting of rehydrated E. arborea (ER03) 24 h after immersion. |
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Food |
Stability (%) |
Hardness (g cm-2) |
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EA01 |
89.2 ± 0.3 a |
687.1 ± 1.9 a |
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EA02 |
89.5 ± 0.1 b |
685.7 ± 1.8 a |
|
ER03 |
66.4 ± 1.1 d |
285.2 ± 2.9 c |
± indicates standard deviation. a,b,c,d Superscripts indicate significant differences (p < 0.05)
The results of the Tukey post-hoc test indicated that significant differences were present with respect to attraction (number of organisms; Fig. 2). The higher attraction values on day 1, 6, and 12 were recorded for ER03 and EA02, with no significant differences between these average values (p > 0.05). However, EA01 was significantly less attractive than ER03 or EA02.
Consumption differed significantly among food types (p > 0.05; Fig. 3). ER03 (> 8 g/day) and EA02 (> 6 g/day) showed the highest consumption values on day 1, 6, and 12. In addition, no significant differences were present between these values on day 6 and 12 (p > 0.05). In contrast, EA01 was consumed significantly less than the other two foods by the abalone (> 5 g/day; p > 0.05).
Eisenia arborea is considered to be a dominant species in both the eastern and western North Pacific. This species is characterized by its ample tolerance to unfavorable environmental conditions and by being an important grazing resource for invertebrates, both of which are factors that influence the production of secondary metabolites (Mekinić et al. 2019; Shin et al. 2021). The total polyphenol content in untreated E. arborea was 33.3 mg GAE/g, which is lower than what was reported by Raja et al. (2015) and Ito et al. (2018), who reported values > 59 mg GAE/g. However, polyphenol content is also influenced by biotic factors, such as predator interactions and developmental stage and abiotic factors, such as light intensity, temperature, and nutrient concentrations, which account for the wide variations in polyphenol content that have been observed at the species level (Díaz-Gutiérrez et al. 2015; Imbs & Zvyaginstseva 2018; Mekinić et al. 2019).
Polyphenols can be released into the water column by algae to defend against grazing, epiphytism, encrustation, and pathogens (Stiger et al. 2014; Lemesheva & Tarakhovskaya 2018). To this end, we reduced the polyphenol content in a formulated food to determine if this would affect the feeding preference of juvenile abalone. Aminina et al. (2020) and Mekinić et al. (2019) determined that the method, duration, and solvent type influence the extraction process and found that ethanol favored the effective acquisition of polyphenols. As expected, the polyphenol content in ethanol-treated flour (EA02) was reduced in this study. The method proposed by Kuda et al. (2007) was used to extract polyphenols from E. arborea. As expected, the polyphenol content in ethanol-treated flour (EA02) was reduced in this study.
The stability of the foods supplied to aquatic organisms influences their growth rates, feeding activity, and health as well as the water quality of the tank (Kinkerdale et al. 2010; Bansemer et al. 2014), which makes this characteristic one of the most important when selecting food. Under culture conditions, formulated foods must show minimal loss within the first 24 h after they are supplied to ensure that the essential nutrients that are needed for proper development are ingested by abalone, which are relatively slow-feeding organisms (Viana 2000; Lee et al. 2018). Thus, highly stable foods are favored in abalone culture systems because they are able to provide essential nutrients to the developing organisms over extended periods of time. The stability of the formulated foods EA01 (89.2%) and EA02 (89.5%) was higher than that of the control food (ER03, 66.4%) 24 h after being supplied. This result is similar to what was observed by Lee et al. (2016) and Lee et al. (2018), who also found that seaweeds showed lower stability than formulated foods. The low stability of ER03 may be due to the dehydration and rehydration process used to produce it, which may have worn down the algae blades.
When formulating foods for aquatic organisms, attraction is a fundamental factor that must be taken into consideration, as attractive foods promote interaction and consumption (Aaqillah-Amr et al. 2021). The attractiveness of foods is influenced by the concentration and release of chemo-attractants, which are compounds that can be detected by the olfactory organs of organisms (Yacoob & Suresh 2003; Aaqillah-Amr et al. 2021). For example, O'Mahoney et al. (2014) described the ability of the abalone H. discus to select food based on its composition, which suggests that the attractiveness of a food can be attributed to the chemo-attractants in its ingredients.
Although the seaweed flour (i.e., the major ingredient) in EA02 was treated with ethanol to remove polyphenols, compounds such as nucleic acids, phospholipids, and amino acids, which are considered to be important attractants in abalone foods, may have also been extracted (Boonyaratpalin 2000; Bai et al. 2015). Nonetheless, the attractiveness of EA02 recorded on day 1, 6, and 12 was greater than that of EA01. Thus, the reduction in polyphenol content in EA02 may have favored attraction. However, the attractiveness of EA02 was not significantly different to that of ER03 (control). This could be related to the high release of low-molecular-weight compounds from ER03 due to the physical wear sustained by E. arborea blades during its processing, which may have favored its attractiveness. Indeed, damaged or decomposing macroalgae tissues quickly release compounds, such as nucleotides, biogenic amines, monosaccharides, phospholipids, and amino acids, which are notable attractants to both aquatic invertebrates and vertebrates (Yacoob & Suresh, 2003; Walker et al. 2005; Hossain et al. 2019).
The consumption of macroalgae and formulated foods by abalone is likely influenced by several factors, including hardness, the presence of attractants and chemical defense compounds like phlorotannins (Cornwall et al. 2009; Angell et al. 2012; Roussel et al. 2020). Food hardness directly influences its consumption by abalone, as has been demonstrated with H. rubra and H. tuberculata (McShane et al. 1994; Roussel et al. 2020). Rivero & Vianna (1996) reported that H. fulgens can consume foods with hardness values greater than 500 g cm-2, such as those recorded for EA01 and EA02 in this study. On the other hand, abalone radula configurations can vary between species, with different configurations favoring the consumption of different types of micro and macroalgae (Kuehl & Donovan 2020). Therefore, the radula configuration of H. fulgens could facilitate the consumption of algae with both soft and thin structures as well as those with rigid and thick structures. As such, it is unlikely that the radula configurations of the abalone in this study influenced the consumption of EA01, EA02, or ER03.
In aquatic organisms, food composition is a characteristic that fundamentally influences consumption. Some compounds promote attraction and consumption, whereas other compounds have the opposite effect. In brown algae, polyphenolic compounds (e.g., phlorotannins) are characterized as deterrents given that they are used in chemical defense mechanisms to avoid herbivory (Flores-Molina et al. 2015, Mekinić et al. 2019). Studies such as those by Pavia & Toth (2000) and Toth et al. (2007) with Ascophyllum nodosum; Macaya et al. (2005) with Glossophora kuntthi; Schwartz et al. (2016) with Sargassum muticum, S. fusiforme, and S. horneri; and Kurr & Davies (2019) with S. muticum have indicated that polyphenols discourage and even prevent algae from being consumed by both vertebrate and invertebrate herbivores. Furthermore, Haliotis abalone are known to be selective when it comes to both natural and formulated foods, and food consumption could thus be linked to food composition and the concentrations of various compounds that either attract or deter abalone (Conrwall et al. 2009; Bullon et al. 2022).
As such, we observed that EA02, which had reduced polyphenol content, was consumed more on day 1, 6, and 12 than EA01. Although the effects that polyphenols have on abalone have not been adequately documented, both Jaquette (2017) and Roussel et al. (2020), who studied H. fulgens and H. tuberculata, respectively, indicated that low polyphenol concentrations in macroalgae could favor their consumption by abalone. However, there were no differences in consumption between EA02 and ER03. As such, other factors, such as low stability or the release of low molecular weight compounds, could have promoted the consumption of ER03 in this study.
Although there were no significant differences in consumption between ER03 (control) and EA02 (reduced polyphenol content), the abalone did show a significantly preference for and consumption of the formulated food EA02, which underwent a reduction in polyphenol content, over the other formulated food (EA01). Thus, we can conclude that the reduction of polyphenol content in food promotes its attractiveness and consumption by abalone. Foods, such as EA02, represent viable alternatives for fishing cooperatives to employ in their abalone culture facilities due to their optimal nutritional composition. However, further feeding experiments are needed to evaluate how foods with reduced polyphenol content influence the growth of important fisheries resources like abalone.
Funding
This study was supported by Instituto Politécnico Nacional (SIP20221048).
Acknowledgements
We wish to thank Sociedad Cooperativa Progreso de Producción Pesquera S.C. de R.L. for donating the juvenile abalone used in this study. We also thank Professor Mauricio Contreras Olguín for his support and assistance in installing the cultivation system in the Mariculture Pilot Unit (UPIMA) of the Interdisciplinary Center for Marine Sciences (CICIMAR). Finally, we also thank the Seaweed Chemistry Laboratory and Food Development Laboratory of CICIMAR-IPN for the use of their facilities for food preparation. MAVA thanks CONACyT and BEIFI for the scholarships awarded (CVU:554883 y B180669). GHC and MMO thank EDI and COFAA for the productivity scholarships awarded.
Competing interests
The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.
Availability of data and material
The raw data can be consulted in the following link : https://docs.google.com/spreadsheets/d/1I5ULRR0U5L-GgndXEk8d07k8LMzShAKx/edit#gid=1035756254
Author contributions
Conceptualization: Villa-Arce, Muñoz-Ochoa; Data curation: Villa-Arce, Godínez-Peréz, Mendoza-Cruz; Formal analysis: Villa-Arce, Godínez-Peréz; Funding acquisition: Hernández-Carmona; Investigation: Villa-Arce; Methodology: Villa-Arce, Mendoza-Cruz; Project administration: Hernández-Carmona; Resources: Hernández-Carmona, Muñoz-Ochoa; Software: Godínez-Peréz, Vélez-Arellano; Supervision: Hernández-Carmona, Muñoz-Ochoa ; Validation: Hernández-Carmona, Muñoz-Ochoa; Visualization: Vélez-Arellano; Writing – original draft: Villa-Arce; Writing – review & editing: Muñoz-Ochoa, Villa-Arce.
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No competing interests reported.