# The Use of Mesquite Pods (Prosopis spp.) as an Alternative to Improve the Productive Performance and Methane Mitigation in Small Ruminants: A Meta-Analysis

Juan Carlos Angeles-Hernandez, Ever del Jesús Flores Santiago, Eduardo Cardoso-Gutiérrez, Sara Valencia-Salazar, Oscar Enrique del Razo Rodriguez, Erwin Paz, Juan Ku-Vera, Ermias Kebreab, Mohammed Benaouda, Ángel Garduño García

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Juan Carlos Angeles-Hernandez, Ever del Jesús Flores Santiago, Eduardo Cardoso-Gutiérrez, Sara Valencia-Salazar, Oscar Enrique del Razo Rodriguez, et al. The Use of Mesquite Pods (Prosopis spp.) as an Alternative to Improve the Productive Performance and Methane Mitigation in Small Ruminants: A Meta-Analysis. Fermentation, 2024, 10 (12), pp.625. 10.3390/fermentation10120625. hal-05007907

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Systematic Review

# The Use of Mesquite Pods (*Prosopis* spp.) as an Alternative to Improve the Productive Performance and Methane Mitigation in Small Ruminants: A Meta-Analysis

Juan Carlos Angeles-Hernandez <fnref n="1" />*, Ever del Jesús Flores Santiago <fnref n="2" /> ID, Eduardo Cardoso-Gutiérrez <fnref n="3" />,
Sara S. Valencia-Salazar <fnref n="4" /> ID, Oscar Enrique del Razo Rodriguez <fnref n="3" />, Erwin A. Paz <fnref n="5" />, Juan C. Ku-Vera <fnref n="6" />,
Ermias Kebreab <fnref n="7" />, Mohammed Benaouda <fnref n="8" /> ID and Ángel Garduño García <fnref n="9" />,*

<figure><img src="image_2.png" /></figure>

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updates

**Citation:** Angeles-Hernandez, J.C.; Santiago, E.d.J.F.; Cardoso-Gutiérrez, E.; Valencia-Salazar, S.S.; Rodriguez, O.E.d.R.; Paz, E.A.; Ku-Vera, J.C.; Kebreab, E.; Benaouda, M.; Garduño García, Á. The Use of Mesquite Pods (*Prosopis* spp.) as an Alternative to Improve the Productive Performance and Methane Mitigation in Small Ruminants: A Meta-Analysis.
*Fermentation* **2024**, *10*, 625.
https://doi.org/10.3390/fermentation10120625

Academic Editor: Cláudia Braga Pereira Bento

Received: 1 November 2024

Revised: 2 December 2024

Accepted: 3 December 2024

Published: 7 December 2024

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**Copyright:** © 2024 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).

**Abstract:** Mesquite (*Prosopis* spp.), a highly nutritious legume from arid regions characterized by its secondary metabolites, offers a cost-effective resource to provide energy and protein for small ruminant farmers in harsh environments. In addition, the high concentrations of secondary metabolites found in mesquite pods could be an option to mitigate methane (CH₄) emissions. Thus, the aim of this study was to conduct an analytical review to assess the impact of adding mesquite pods on small ruminant productivity and enteric CH₄ emissions. A comprehensive and structured search of scientific articles resulted in a database of 38 trials. The response variables were evaluated through raw mean differences (RMDs) and standardized mean differences (SMDs), followed by a meta-regression, used to investigate the heterogeneity of the explanatory variables. Supplementation with mesquite pods significantly increased the dry matter intake (DMI) and average daily gain (ADG) and reduced the feed conversion ratio (FCR), with sheep showing the highest effect. The meta-regression demonstrated that the mesquite pod effect was influenced mainly by the species, level of incorporation and processing of the pods. Studies employing in silico CH₄ estimation reported increased emissions when the diets included mesquite pods. In contrast, in vivo studies demonstrated promising results, showing a significant reduction in CH₄ emissions when mesquite pods were included in small ruminant diets. Therefore, future research should focus on evaluating mesquite pod supplementation using precise methods to assess CH₄ emissions.

**Keywords:** digestibility; intake; goat; sheep; *Prosopis*

## 1. Introduction

Small ruminant production systems have been established mostly in regions where the agroclimatic and topographic conditions do not allow for the implementation of cattle farming [1]. The use of pods from trees and shrubs constitutes a promising alternative

<footnote n="1">¹ Departamento de Medicina y Zootecnia de Rumiantes, Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autónoma de Mexico, Ciudad de Mexico 04510, Mexico</footnote>

<footnote n="2">² Unidad Regional Universitaria Sursureste—Universidad Autónoma Chapingo, Km 7.5 Carretera Teapa Vicente Guerrero, Teapa 86807, Mexico; ejfloress@chapingo.mx</footnote>

<footnote n="3">³ Instituto de Ciencias Agropecuarias, Universidad Autónoma del Estado de Hidalgo, Tulancingo 43688, Mexico; cardosoge89@gmail.com (E.C.-G.); oscare@uaeh.edu.mx (O.E.d.R.R.)</footnote>

<footnote n="4">⁴ The Alliance of Bioversity International and International Center for Tropical Agriculture (CIAT), Km 17 Recta Cali-Palmira, Apartado Aereo 6713, Cali 763537, Colombia; saraudea@gmail.com</footnote>

<footnote n="5">5 UWA Institute of Agriculture, The University of Western Australia, Perth 6009, Australia;
ewin.pazmunoz@uwa.edu.au</footnote>

<footnote n="6">⁶ Laboratory of Climate Change and Livestock Production, Faculty of Veterinary Medicine and Animal Science, University of Yucatan, Merida 97000, Mexico; kvera@ correo.uady.mx</footnote>

<footnote n="7">⁷ Department of Animal Science, University of California, Davis, CA 95616, USA; ekebreab@ucdavis.edu</footnote>

<footnote n="8">⁸ L'Institut Agro Dijon, 26 bd Docteur Petitjean, 21079 Dijon, France; mohammed.ben-aouda@agrosupdijon.fr</footnote>

<footnote n="9">⁹ Departamento de Ingeniería Mecánica Agrícola, Universidad Autónoma Chapingo, Carr. Mexico—Texcoco Km. 38.5, Chapingo 56230, Mexico</footnote>

<footnote>* Correspondence: juanangeles@fmvz.unam.mx (J.C.A.-H.); agardunog@chapingo.mx (Á.G.G.)</footnote>
as a livestock feed [2]. Small ruminant farmers in arid regions have found that supplementing with mesquite pods is a reasonable strategy to improve productivity because it is a low-cost source of energy and protein. Mesquite is a xenophyte native to tropical and subtropical regions around the world, which has been recently used as an animal feed resource [3]. Mesquite fixes atmospheric nitrogen, is drought- and salinity-tolerant and grows relatively fast [3,4].

This legume is an important source of crude protein (7–22%), crude fiber (11–35%), and carbohydrates (30–75%); therefore, it represents an excellent alternative animal feed [5]. In addition, mesquite is rich in secondary metabolites such as alkaloids, flavonoids, terpenes and phenolic compounds that suggest prospective medicinal applications in human and animal health such as antibacterial, antifungal, anti-inflammatory, antioxidant and anthelmintic medications [4].

The rising demand of animal products due to the growing human population and changing consumption patterns, has led to an increase in livestock numbers across the globe [6,7]. Consequently, the increasing environmental impact of the livestock sector is expected according to the increasing greenhouse gas (GHG) emissions [8]. For instance, the entire livestock commodity chain with the agriculture sector (land use, feed production, livestock farming, waste management and the processing of products and transport), is responsible for 14.5% of the total anthropogenic GHG emissions [8]. Recently, Herrero et al. [9] estimated that the total emissions from the livestock sector from 1995 to 2005 ranged between 5.6 and 7.5 GtCO₂-eq yr⁻¹, while CH₄ accounted for 1.6 to 2.6 GtCO₂ eq yr⁻¹, and nitrous oxide (N₂O) associated with food production ranged from 1.3 to 2.0 GtCO₂-eq yr⁻¹ and that with land use for animal feed and pasture was ~1.6 GtCO₂-eq yr⁻¹. Hence, it is necessary to be proactive to mitigate GHG emissions without compromising animal production, because livestock systems benefit many low-income communities around the globe.

Forages with a high digestibility have been shown to improve productive performance and reduce CH₄ emissions [10]. In addition, the high concentrations of secondary metabolites found in mesquite could be an option to mitigate CH₄ emissions [4,9,11]. In vivo and in vitro experiments have demonstrated that biocomponents of mesquite pods, primarily alkaloids, have a beneficial impact on the rumen environment. This is due to their ability to enhance energy and protein utilization, increase the propionate ratio and reduce enteric CH₄ emissions [12]. However, the results of studies evaluating the effects of adding mesquite to ruminant diets are inconsistent. In this context, a meta-analysis would allow researchers to synthetize the available scientific evidence to address a specific research question. Thus, the aim of this study was to carry out an analytical review to quantify the effect of the inclusion of mesquite on the productive performance and CH₄ emissions of small ruminants through a meta-analytical methodology. In addition, the effect of covariates that could explain the heterogeneity of mesquite supplementation was explored using a meta-regression analysis.

## 2. Materials and Methods

### 2.1. Data Collection

A comprehensive and structured search of scientific publications was carried out according to PRISMA guidelines [13] and the protocol was registered using the Covidence platform. The search was performed by three field experts to avoid reviewer bias, using five electronic databases: Google Scholar, Primo (UAEH), PubMed, Science Direct and ISI Web of Knowledge. The following keywords were used in the search: "Mesquite", "Prosopis spp.", "sheep", "lamb", "kid", "goat", "dry matter intake", "growth performance", "methane" and "enteric methane", which were combined by Boolean logic ("AND", "OR"). Only peer-reviewed papers written in English that assessed the effect of supplementation with mesquite in small ruminant diets were used. Additional studies were identified from the list of references of papers found in the first search and were included in the global
database. The bibliographic search resulted in 27 articles published between 2005 and 2019, of which 13 articles met the inclusion criteria, obtaining a total of 38 trials (Figure 1).

<figure><img src="image_4.png" /><figcaption>**Figure 1.** PRISMA study flow diagram of the systematic review from initial search and screening to final selection of publications to be included in the meta-analysis.</figcaption></figure>

Given our aim of quantifying the effect of inclusion of mesquite pods on productive performance (dry matter intake, average daily gain and feed conversion ratio) and enteric CH₄ emissions, only studies that reported productive performance and/or enteric CH₄ emissions from control vs. supplemented sheep or goats were used. In addition, the studies had to meet the following criteria: (a) studies published in an international peer-reviewed scientific journal, (b) studies that specified the procedure of random assignment of animals to each treatment (experimental design), (c) studies that reported the least square means and the variability of the measurements (coefficient of variation, standard deviation or standard error) and (d) studies that reported the sample size of each group. Unpublished manuscripts, conference proceedings, and dissertations were therefore excluded.

After selecting the studies that met the previous eligibility criteria, the final database included 38 trials with the following response variables: dry matter intake (DMI), average daily gain (ADG), feed conversion ratio (FCR), digestibility (g/100 g DM) and estimated methane emissions (CH₄; g/d). Most studies did not directly report CH₄ emissions; therefore, these emissions were estimated in silico using data on DMI and diet digestibility values, applying the equation proposed by Sauvant et al. [14]:

$$CH_4 = (7.14 + 0.22 \times \text{DOM}) \times \text{DMI} \quad (1)$$
where CH₄ (g/d) is enteric methane emissions; DOM is the digestible organic matter content in the diet (DOM [% of DM] = organic matter content [% of DM] × digestibility of organic matter [% of DM]) and DMI is dry matter intake (kg/d).

The meta-analysis procedure requires a central tendency measure (i.e., mean) and a dispersion measure (standard deviation) of the control and the supplemented groups to estimate the effect size. Therefore, an error propagation process was carried out for the calculated mean and standard deviation of the control and the supplemented groups in each trial. Uncertainty propagation was carried out using the Propagate Package [15] in R statistical software [16] through Monte Carlo simulation (MCS). Propagate functions of MCS were introduced with the number of replicates, mean and standard deviation of DMI and DOM of each study. To define the number of simulations to be performed, an adaptive method was carried out by increasing the number of simulations until reaching the stabilization of values of the uncertainty of the estimated variables.

## 2.2. Meta-Analytical Procedure

The summary effect measures in this study were the standardized mean differences (SMDs) calculated using the method proposed by Hedges [17]. All analyses were performed in R environment for statistical computing version 4.0.2 [16] using the package ‘meta’ version 4.13-0 [18]. A random-effects model for meta-analysis was used, which was expanded to a mixed model to deal with the heterogeneity across studies. The mean effect size and the test of heterogeneity were displayed in a forest plot as well as heterogeneity between subgroups based on the processing of mesquite pods. The raw mean difference (RMD) was calculated for response variables that shared the same scales, allowing for the interpretation of summary effect under the original unit of measurement [19]. Begg’s test was performed in order to evaluate evidence for publication bias. The degree of heterogeneity was systematically assessed by I², which represents the proportion of between-study variability [20].

Further exploration of this heterogeneity was performed using a meta-regression analysis to find variables that explain the variability of the effect size estimations. A priori explanatory variables were selected including level of incorporation of mesquite, species (goat and sheep), breed, live body weight (LBW, kg) and processing of the mesquite pods (ground, chopped, extract and meal). The multi-predictor models were manually reduced by backward selection of variables until all predictors were significant (p < 0.05). Mixed-effects regression models (meta-regression analysis) were constructed in the “metafor” package [21]. Models were compared and selected by means of information of theoretical criteria using Akaike’s Information Criterion and Bayesian Information Criterion. In addition, the goodness of fit was evaluated by the coefficient of correlation analogue (R²) for meta-regression, which was calculated as follows:

$$R^2 = \frac{\tau^2 REM - \tau^2 MEM}{\tau^2 REM} \qquad (2)$$

where τ²REM is the estimated total heterogeneity based on the random-effects model and τ²MEM is the total heterogeneity of the mixed-effects regression model.

## 3. Results

The chemical composition of the control and mesquite diets are shown in Table 1. Numerical variations were observed between the unsupplemented and mesquite pod groups regarding the main dietary components. The diets supplemented with mesquite pods exhibited higher concentrations of DM, CP and EE, while showing lower levels of OM, ADF, NDF and ash compared to the unsupplemented diets. Table 2 shows the descriptive statistics of the response variables evaluated in the current study. The number of trials analyzed, mean of the control group, SMD (95% confidence interval (95% CI)), RMD (95% CI), test of heterogeneity and bias are shown in Table 3.
<table><caption>**Table 1.** Chemical composition of unsupplemented and mesquite pod diets.</caption><thead><tr><th>Item</th><th></th><th>Mean</th><th>Median</th><th>SD</th><th>Min</th><th>Max</th><th>Skewness</th><th>Kurtosis</th></tr></thead><tbody><tr><td rowspan="2">DM, g/kg</td><td>U</td><td>912.7</td><td>909.0</td><td>26.4</td><td>867.0</td><td>957.0</td><td>0.05</td><td>-0.97</td></tr><tr><td>S</td><td>914.4</td><td>911.2</td><td>26.5</td><td>862.0</td><td>958.0</td><td>-0.08</td><td>-0.72</td></tr><tr><td rowspan="2">CP, g/kg DM</td><td>U</td><td>131.3</td><td>140.8</td><td>39.9</td><td>39.0</td><td>174.0</td><td>-1.06</td><td>0.02</td></tr><tr><td>S</td><td>136.3</td><td>149.0</td><td>36.6</td><td>42.3</td><td>183.0</td><td>-1.33</td><td>0.71</td></tr><tr><td rowspan="2">OM, g/kg DM</td><td>U</td><td>910.8</td><td>897.5</td><td>48.5</td><td>852.0</td><td>991.0</td><td>0.47</td><td>-1.36</td></tr><tr><td>S</td><td>904.5</td><td>899.9</td><td>39.8</td><td>847.0</td><td>990.3</td><td>0.33</td><td>-0.68</td></tr><tr><td rowspan="2">ADF, g/kg DM</td><td>U</td><td>279.7</td><td>205.0</td><td>194.6</td><td>96.4</td><td>681.8</td><td>0.78</td><td>-0.82</td></tr><tr><td>S</td><td>268.4</td><td>203.0</td><td>148.7</td><td>132.0</td><td>608.8</td><td>0.86</td><td>-0.77</td></tr><tr><td rowspan="2">NDF, g/kg DM</td><td>U</td><td>465.9</td><td>390.5</td><td>193.9</td><td>225.0</td><td>775.0</td><td>0.30</td><td>-1.65</td></tr><tr><td>S</td><td>431.7</td><td>377.0</td><td>161.9</td><td>222.0</td><td>755.0</td><td>0.74</td><td>-0.87</td></tr><tr><td rowspan="2">EE, g/kg DM</td><td>U</td><td>42.7</td><td>39.4</td><td>13.2</td><td>28.0</td><td>67.4</td><td>0.64</td><td>-0.95</td></tr><tr><td>S</td><td>47.1</td><td>41.9</td><td>20.1</td><td>18.7</td><td>99.0</td><td>1.26</td><td>1.04</td></tr><tr><td rowspan="2">Ash, g/kg DM</td><td>U</td><td>68.6</td><td>68.5</td><td>19.1</td><td>46.4</td><td>96.0</td><td>0.13</td><td>-1.77</td></tr><tr><td>S</td><td>65.5</td><td>71.0</td><td>13.3</td><td>47.4</td><td>88.4</td><td>-0.03</td><td>-1.54</td></tr></tbody></table>

SD = standard deviation; U = diets unsupplemented with mesquite pods; S = diets supplemented with mesquite pods; DM = dry matter; CP = crude protein; OM = organic matter; ADF = acid detergent fiber; NDF = neutral detergent fiber; EE = ether extract.

<table><caption>**Table 2.** Descriptive statistics of data used in mesquite pod supplementation meta-analysis.</caption><thead><tr><th>Item</th><th></th><th>Mean</th><th>Median</th><th>SD</th><th>Min</th><th>Max</th><th>Skewness</th><th>Kurtosis</th></tr></thead><tbody><tr><td rowspan="2">DMI, g/d</td><td>U</td><td>933.38</td><td>822.09</td><td>404.93</td><td>399.0</td><td>2034.0</td><td>0.92</td><td>0.55</td></tr><tr><td>S</td><td>992.72</td><td>887.3</td><td>394.0</td><td>291.0</td><td>2038.0</td><td>0.7</td><td>0.24</td></tr><tr><td rowspan="2">ADG, g/d</td><td>U</td><td>142.54</td><td>177.0</td><td>100.09</td><td>6.67</td><td>292.0</td><td>0.02</td><td>-1.44</td></tr><tr><td>S</td><td>146.67</td><td>146.0</td><td>94.69</td><td>-21.0</td><td>282.0</td><td>-0.01</td><td>-1.5</td></tr><tr><td rowspan="2">FCR, g/g</td><td>U</td><td>29.04</td><td>5.5</td><td>52.91</td><td>3.97</td><td>143.94</td><td>1.64</td><td>0.74</td></tr><tr><td>S</td><td>7.99</td><td>6.2</td><td>5.51</td><td>4.33</td><td>27.67</td><td>2.49</td><td>6.14</td></tr><tr><td rowspan="2">DIG, g/100 g DM</td><td>U</td><td>64.94</td><td>65.9</td><td>9.9</td><td>45.4</td><td>80.8</td><td>-0.51</td><td>-0.1</td></tr><tr><td>S</td><td>65.65</td><td>67.3</td><td>8.03</td><td>47.1</td><td>77.8</td><td>-0.7</td><td>-0.43</td></tr><tr><td rowspan="2">CH<sub>4</sub>, g/d</td><td>U</td><td>9.66</td><td>7.99</td><td>5.9</td><td>4.11</td><td>23.9</td><td>1.48</td><td>1.09</td></tr><tr><td>S</td><td>9.89</td><td>8.12</td><td>5.05</td><td>4.12</td><td>23.2</td><td>1.38</td><td>0.85</td></tr></tbody></table>

SD = standard deviation; U = diets unsupplemented with mesquite pods; S = diets supplemented with mesquite pods; DMI = dry matter intake; ADG = average daily gain; FCR = feed conversion ratio; DIG = digestibility; CH₄ = enteric methane emissions.

<table><caption>**Table 3.** Standardized mean difference (SMD) and raw mean difference (RMD) of random-effects model with 95% CI of DMI, ADG, FCR, DIG and estimated CH₄ of small ruminants supplemented with mesquite pods.</caption><thead><tr><th rowspan="2">Item</th><th rowspan="2">Trials (n)</th><th rowspan="2">Control Mean (SD) <sup>a</sup></th><th rowspan="2">RMD (95% CI) <sup>b</sup></th><th colspan="3">Effect Size</th><th colspan="2">Heterogeneity</th><th rowspan="2">Bias</th></tr><tr><th>p-Value</th><th>SMD (95% CI) <sup>c</sup></th><th>p-Value</th><th>I<sup>2</sup> (%)</th><th>p-Value</th></tr></thead><tbody><tr><td>DMI, g/d</td><td>37</td><td>933.38 (404.93)</td><td>+68.57 (41.71, 95.43)</td><td>0.0001</td><td>+0.64 (0.29, 0.99)</td><td>0.0003</td><td>92.8</td><td>0.001</td><td>0.73</td></tr><tr><td>ADG, g/d</td><td>19</td><td>142.54 (100.09)</td><td>+9.94 (0.74, 19.15)</td><td>0.03</td><td>+1.51 (0.04, 2.99)</td><td>0.04</td><td>99.8</td><td>0.001</td><td>0.65</td></tr><tr><td>FCR, g/g</td><td>18</td><td>29.04 (52.91)</td><td>-21.18 (-29.62, -12.73)</td><td>0.0001</td><td>+0.39 (-0.16, 0.96)</td><td>0.16</td><td>99.5</td><td>0.001</td><td>0.87</td></tr><tr><td>DIG, g/100 g DM</td><td>23</td><td>64.94 (9.9)</td><td>+1.45 (0.03, 2.92)</td><td>0.045</td><td>+0.28 (-0.09, 0.66)</td><td>0.14</td><td>80.4</td><td>0.01</td><td>0.11</td></tr><tr><td>CH<sub>4</sub>, g/d</td><td>26</td><td>7.8 (2.89)</td><td>+0.29 (-0.24, 0.84)</td><td>0.27</td><td>+0.39 (-0.12, 0.91)</td><td>0.13</td><td>74.9</td><td>0.0001</td><td>0.55</td></tr></tbody></table>

DMI = dry matter intake; ADG = average daily gain; FCR = feed conversion ratio; DIG = digestibility; CH₄ = enteric methane emissions. <sup>a</sup> Mean and standard deviation of unsupplemented group. <sup>b</sup> RMD is the raw mean difference that estimates the global effect expressed in the original unit measures. <sup>c</sup> SMD is the standardized mean difference estimated of the random model. <sup>d</sup> I² is measure of heterogeneity of random model.
### 3.1. Dry Matter Intake

Thirty-seven randomized trials that examined the effect of mesquite pod supplementation on the DMI compared with a control group were identified. The RMD for the DMI between the mesquite-supplemented and control treatments from the random-effects analysis was +68.67 g/d (95% CI: +41.71, +95.43; *p* = 0.0001) with an SMD of +0.64 (95% CI: +0.29, +0.99; *p* = 0.0003). Substantial heterogeneity was observed for the DMI data (*I*² = 92.8; *p* = 0.001), which constrains the evaluation of the pooled estimates of mesquite supplementation (Table 3) and the exploration of sources of heterogeneity through a meta-regression procedure.

The forest plot of the DMI for the random-effects meta-analysis stratified by techniques of processing mesquite pods and for all studies combined are presented in Figure 2. There were differences in the magnitude of RMD among the techniques of processing mesquite pods. The studies that provided mesquite pods as a meal showed the largest RMD of the DMI (+157.3 g/d), followed by extract (+107.5 g/d) and ground (+50.4 g/d) treatments. Supplementation with chopped mesquite pods negatively affected the DMI of the small ruminants (−46.8 g/d) (Figure 3). These results are confirmed by the significant effect of processing on the SMD's magnitude for the DMI in the meta-regression analysis (extract +171; meal +220) (Table 4). The dry matter intake was also affected by the level of incorporation of mesquite pods (+0.22; *p* < 0.05), breed (*p* < 0.0001) and animal species (sheep +113.1; *p* < 0.01) (Table 4).

<table><caption>**Table 4.** Slopes and significance of covariables included in the multivariate meta-regression analysis.</caption><thead><tr><th rowspan="2">Item</th><th rowspan="2">Level of Incorporation</th><th rowspan="2">Specie</th><th colspan="3">Covariates</th><th rowspan="2">R<sup>2</sup></th></tr><tr><th>Breed <sup>a</sup></th><th>LBW</th><th>Processing</th></tr></thead><tbody><tr><td>DMI, g/d</td><td>+0.22 *</td><td>Sheep +113.1 **</td><td>AW −9.35 ***<br>RA −9.23 ***<br>SA −9.51 ***<br>SI −8.39 ***</td><td></td><td>Extract +170.72 *<br>Meal +219.68 **</td><td>55.37</td></tr><tr><td>ADG, g/d</td><td>+0.089 *</td><td>Sheep +26.25 *</td><td>AW +40.02 ***<br>SI −23.21 *</td><td></td><td></td><td>99.01</td></tr><tr><td>FCR, g/g</td><td>−0.125 ***</td><td>Sheep −44.46 **</td><td>AW +51.7 ***<br>RA +50.1 ***<br>BA +52.1 ***</td><td>+8.97 ***</td><td></td><td>94.31</td></tr><tr><td>DIG, g/100 g DM</td><td>−0.079 **</td><td></td><td>AW −8.87 ***<br>RA −9.09 ***<br>SI −8.96 ***<br>MA −8.83 ***</td><td>+0.76 ***</td><td>Extract +41.74 *<br>Ground +40.33 **</td><td>99.2</td></tr><tr><td>CH<sub>4</sub>, g/d</td><td></td><td>Sheep +3.91 ***</td><td>Dp −1.96 ***</td><td></td><td>Ground −3.98 ***<br>Extract −3.79 **</td><td>79.8</td></tr></tbody></table>

DMI = dry matter intake; ADG = average daily gain; FCR = feed conversion ratio; DIG = digestibility; CH₄ = enteric methane emissions. R² = amount of heterogeneity accounted for the mixed model. Significance codes: *** *p* < 0.001; ** *p* < 0.01; * *p* < 0.05. <sup>a</sup> Sheep breeds: Afar (AF), Awassi (AW), Santa Ines (SI), Rambouillet (RA), Malpura (MA) and Dorper (Dp). Goat breads: Batina (BA), Black (BL), Dhofari (DH) and Saanen (SA).
<figure><img src="image_5.png" /><figcaption>**Figure 2.** Forest plot of dry matter intake (DMI, g/d) from studies on mesquite pods used as dietary supplement in small ruminants [22–33].</figcaption></figure>
<figure><img src="image_6.png" /><figcaption>**Figure 3.** Bubble plot of raw mean difference for dry matter intake (DMI, g/d) by the level of mesquite pod inclusion and processing method.</figcaption></figure>

## 3.2. Average Daily Gain

A total of 19 trials provided sufficient information to estimate the effect of mesquite pod incorporation on the ADG with an SMD of +1.51 (CI: +0.04, +2.99; *p* = 0.04), which means an increase of +9.94 g/d in the body weight (CI: 0.74, 19.15; *p* = 0.03) of the supplemented small ruminants. There was sufficient heterogeneity (*I*² = 99.8) of the ADG random model to conduct the mixed-effects model. A meta-regression analysis revealed a positive relationship of the ADG's effect size with the level of incorporation of mesquite pods (+0.089; *p* < 0.05), species (sheep + 26.25; *p* < 0.05) and breed (*p* < 0.001) (Table 4).

## 3.3. Feed Conversion Ratio and Digestibility

The FCR summary effect (SMD) between the mesquite pod treatment and control group was not significant (*p* = 0.16); however, the RMD of the FCR showed a reduction of -21.2 g/g of the supplemented treatment (Table 3). The RMD of the digestibility showed an increase of +1.45 g/100 g DM (CI: +0.03, +2.92; *p* = 0.045) in the mesquite-treated group as compared with the controls; however, the summary effect (SMD) was not significant (+0.28; *p* = 0.14) (Table 3). The forest plot for digestibility showed that the effect of mesquite incorporation on the digestibility was affected by the method of processing the pods, with a higher RMD from the studies using meal (+4.51 g/100 g DM) and extract (+3.85 g/100 g DM) than in the other studies (Figure 4).
<figure><img src="image_7.png" /><figcaption>**Figure 4.** Forest plot of digestibility of dry matter (g/100 g) from studies on mesquite pods used as dietary supplement in small ruminants [23–25,27,30–33].</figcaption></figure>

### 3.4. Enteric Methane Estimation

Data from 26 trials allowed for the estimation of the overall effect of mesquite pod incorporation on the estimated CH₄ emissions in small ruminant diets, with a significant SMD of +0.39 (CI: -0.12, +0.91; *p* = 0.13). A non-significant increase of +0.29 g/d (CI: -0.24, +0.84; *p* = 0.27) in the estimated CH₄ emissions from the animals fed mesquite was observed. The response to mesquite incorporation was higher in the studies with sheep (+3.91 **\***\***) (Table 4). Figure 5 depicts the forest plot of the summary effect of the mesquite pods on the estimated CH₄ emissions, classified according to the methodology employed for CH₄ estimation. The studies that estimated the CH₄ in silico revealed an increase in the CH₄ emissions from animals that were supplemented with mesquite pods (SMD +0.58; CI: +0.10, +1.07). Conversely, the in vivo studies demonstrated a reduction in the CH₄ emissions as a consequence of feeding the animals with mesquite pods (SMD -1.47; CI: -2.67, -0.27).
<figure><img src="image_8.png" /><figcaption>**Figure 5.** Forest plot of estimated methane emissions (CH₄, g/d) from studies on mesquite pods used as dietary supplement in small ruminants [12,23–25,27,30–33].</figcaption></figure>

## 4. Discussion

Mesquite is largely available in arid regions, which eases its use by small ruminant producers. Studies on the impact of dietary supplementation with mesquite pods have shown inconsistent results. This is the first study that uses a meta-analytic approach to analyze the effect of dietary supplementation with mesquite pods on animal performance and enteric CH₄ emissions.

The small ruminant response to mesquite incorporation in the diet involved an increase in the DMI, which could be associated with the better feed quality of mesquite pod diets. Although the mesquite pods had a variability in the DM% (from 85.8% to 95.0%), crude protein (from 7% to 18.3%) and NDF (from 19.5% to 40%), they are considered a low-cost source of protein and energy for small ruminant diets in dry regions [34]. In addition, mesquite can survive under limited water availability conditions with an annual production of 2 to 10.5 kg of pods per tree [35] and an estimated production of 4.5 ton/ha [36]. However, from a practical perspective, it is important to consider that the nutritional value of a mesquite pod can vary depending on the phenological stage, geographical location and growing climatic conditions [5]. The study by Angeles-Hernandez et al. [37] revealed significant differences in the in vitro fermentation patterns and CH₄ emissions from the mesquite pods depending on the geographical
origin. The authors emphasize the importance of considering the origin of mesquite pods in the development and implementation of future nutritional and greenhouse gas mitigation strategies.

In the current work, the heterogeneity of the response variables was explored using two approaches, firstly, the sub-group analysis, as shown in the forest plot, and, secondly, implementing a meta-regression analysis. In both approaches, the processing of the mesquite pods showed a significant effect on the DMI and digestibility, with pod meal being the processing method leading to the largest improvement in the DMI and digestibility. The small particle size of the diets could determine a higher rumen degradation and a faster rate of passage of digesta. On the other hand, when pods were offered chopped, the particle size was greater, which could have generated a filling effect in the rumen, and a lower passage rate, thus reducing the DMI [38].

In this sense, the digestibility was also affected by the physical processing of the pods. A higher concentration of nutrients is found inside the seeds, so when these are offered as a meal, the surface area to which the microorganisms can attach and ferment the feed components increases, resulting in an overall improvement in the digestibility. Kononoff and Heinrichs [39] reported that a reduction in the particle size of feed can increase rumen digestion due to an increase in the surface area available for ruminal bacteria. To take advantage of the nutritional value of mesquite, adequate pod processing is critical. Experiments that offered mesquite extract showed the lowest variability in their response with $I^2 < 30\%$ for the DMI and digestibility. However, cost and other issues related to extra processing tasks associated with supplementation in the form of an extract must be considered at the farm level. Other processing techniques such as roasting have been used with mesquite pods to improve their nutritional characteristics, which induces a reduction in the content of antinutritional factors but with a detrimental effect on the organic matter and NDF digestibility [2].

Several studies have demonstrated that mesquite pods enhance the palatability of ruminant diets, a feature attributed to their favorable nutritional composition. Approximately 75% of the sugars present in mesquite pods are sucrose and fructose; these sugars are closely linked to an improvement in palatability, which contributed to an increased DMI [40,41]. This effect is further enhanced by the high content of unsaturated fatty acids, such as linoleic acid, and essential amino acids, including lysine and methionine [42]. A meta-regression analysis revealed that the response to mesquite inclusion in all the dependent variables was associated with the level of supplementation. In general, our results showed a better performance of the supplemented animals with a higher DMI and ADG. Likewise, a significant negative relationship was observed between the level of incorporation of the mesquite pods and the FCR, which suggests an improved efficiency of feed conversion into body weight gain when mesquite pods were added to the diet. This result is highly relevant for small ruminant farmers, since this plant will probably lead to the improvement of productivity. However, in relation to the DMI, the response to mesquite pod supplementation is the result of the interaction between the level of incorporation and the pod processing method. The optimum benefit of including mesquite pods in small ruminants' diets is between 400 and 450 g/kg DMI offered as a meal.

In line with these findings, Obeidat et al. [23] reported no effect on the ADG in lambs when barley grain was replaced by mesquite pods, while also observing a reduction in the feeding costs for lambs consuming mesquite pods. This cost reduction was attributed to the fact that the inclusion of mesquite pods in lamb diets does not have any additional costs other than the labor associated with collecting them. Similarly, Ravikala et al. [43] (1995) found that the feed cost per kilogram of body weight gain was significantly lower ($p < 0.05$) in lamb diets containing mesquite pods compared to a control group. This reinforces the concept that mesquite pods can serve as a low-cost natural feed resource for small ruminants [40], helping to reduce feed costs, improve animal performance and increase profitability for smallholder farmers, particularly in economically disadvantaged regions [44].
Our results revealed a better animal response to mesquite supplementation in sheep than in goats. This can be explained by the difference between the species in terms of eating behavior and rumen physiology. Several studies pointed out that goats depicted a lower DMI per unit of bodyweight in comparison with sheep, which could be associated with the fact that the goats spent more time eating and ruminating [45,46]. Also, Abijaode et al. [47] reported that goats have a strong ability to differentiate various fodder based on their physical structure and palatability, which probably allowed the goats to identify and to select the mesquite pods. The higher DMI and digestibility in sheep resulted in a superior ADG and FCR, which is consistent with previous studies that reported a greater growth rate in sheep in comparison with goats [48,49]. In this sense, Lin et al. [50] observed that sheep exhibited a higher feed utilization efficiency compared to goats under identical feeding patterns. They attributed this difference primarily to variations in the rumen microbial community, particularly within the *Succinivibrionaceae* family. In terms of nutritional requirements, Nielsen et al. [51] found that the fasting energy expenditure was significantly higher in goats than in sheep. Additionally, sheep demonstrated a reduction in N excretion, indicating an efficient mechanism through which they adapt their metabolism and urinary excretory patterns of N in accordance with the dietary N availability.

The in silico methodology-based CH₄ emissions were higher in animals that received diets supplemented with mesquite pods. These findings are associated with the fact that the CH₄ methane emission was calculated based on the DMI, which is theoretically supported by early studies that indicated that daily enteric CH₄ production is directly determined by the DMI [52,53]. Nevertheless, the in vivo trials, although fewer in number, demonstrated a reduction in the CH₄ emissions as a consequence of including mesquite pods in the diets of small ruminants. This is consistent with studies utilizing diverse legume pods and demonstrating a reduction in methane emissions, which have revealed a high starch content [54]. This soluble carbohydrate, when fermented, increases the proportion of propionic acid in the rumen, thereby reducing methane production. The source of carbohydrate is a primary factor influencing CH₄ synthesis, and, thus, is responsible for the observed fermentation patterns and increase in the DMI.

Plant species from tropical and arid regions have a high diversity and abundance of secondary metabolites due to the agroclimatic conditions in which they are cultivated. Secondary metabolites can modify the population of microorganisms, shift CH₄ synthesis and reduce CH₄ emissions by up to 20% on average, although the results are highly variable and depend on the characteristics of the metabolites [11]. Table 5 describes the main biocomponents identified from mesquite pods. The in vivo studies carried out on lambs and the in vitro studies showed that these biocomponents, mainly of an alkaloid chemical nature, have a positive effect on the rumen environment, improving energy and protein utilization, increasing the rumen propionate proportion with a consequent reduction in enteric CH₄ emissions; this positive effect is probably related to the alteration of the ruminal microbiota, including archaea, proteolytic and fibrolytic bacteria. Along the same lines, Argôlo-Batista et al. [55] found that diets supplemented with 66.7% and 100% replacement of corn by mesquite pod meal in goat diets resulted in a reduced population of methanogenic archaea compared to a control group without mesquite pods. This reduction may be related to a decrease in protozoa, which in turn reduces methanogens associated with these microorganisms either by adhesion or endosymbiosis.

The results of this meta-analysis regarding CH₄ emissions are inconclusive due to the methods used for CH₄ estimation. The studies employing in silico CH₄ estimation reported increased emissions when the diets included mesquite pods. In contrast, the in vivo studies revealed promising results, demonstrating a significant reduction in CH₄ emissions with mesquite pod inclusion in small ruminant diets. Therefore, future research should focus on evaluating mesquite pods under isonitrogenous and isoenergetic conditions, using precise techniques to assess CH₄ emissions, as current scientific data provide sufficient information to determine the global effect of mesquite pods on the productive performance of small
ruminants, but do not allow for a clear understanding of the true impact of mesquite pods on the rumen fermentation patterns.

<table><caption>**Table 5.** Identified biocomponents from mesquite pods.</caption><thead><tr><th>Biocomponent</th><th>Chemical Formula</th><th>Type of Study</th><th>Observed Effects</th><th>Duration</th></tr></thead><tbody><tr><td>Juliprosinine [12,56]</td><td>C<sub>40</sub>H<sub>71</sub>N<sub>3</sub>O<sub>2</sub></td><td>In vivo (lambs)<br>In vitro</td><td>Improves energy and protein utilization, alters ruminal microbial populations (including archaea, proteolytic and fibrolytic bacteria), improves nitrogen utilization and retention, reduces CH<sub>4</sub> emissions, promotes higher final body weight, improves feed conversion efficiency and increases rumen propionate ratio.</td><td>27 days [12]<br>84 days [56]</td></tr><tr><td>Juliprosopine<br>(Juliflorine) [12,56,57]</td><td>C<sub>40</sub>H<sub>75</sub>N<sub>3</sub>O<sub>2</sub></td><td>In vivo (lambs)<br>In vitro</td><td>Improves energy and protein utilization, modifies rumen microbial populations (including archaea, proteolytic and fibrolytic bacteria), improves nitrogen utilization and retention, reduces CH<sub>4</sub> emissions and increases rumen propionate ratio.</td><td>27 days [12]<br>84 days [56]<br>24 h [57]</td></tr><tr><td>Prosopinine [12]</td><td>C<sub>18</sub>H<sub>35</sub>NO<sub>3</sub></td><td>In vivo (lambs)</td><td>Modulates ruminal microbiome populations (including archaea, proteolytic and fibrolytic bacteria) and reduces CH<sub>4</sub> emissions.</td><td>27 days [12]</td></tr><tr><td>Julifloridine [12]</td><td>C<sub>18</sub>H<sub>37</sub>NO<sub>2</sub></td><td>In vivo (lambs)</td><td>Modulates ruminal microbiome populations (including archaea, proteolytic and fibrolytic bacteria) and CH<sub>4</sub> emissions.</td><td>27 days [12]</td></tr><tr><td>Prosoflorine [56,57]</td><td>C<sub>40</sub>H<sub>72</sub>N<sub>3</sub>O<sub>2</sub></td><td>In vivo (lambs)<br>In vitro</td><td>Improves fiber digestibility, promotes higher final body weight, improves feed conversion efficiency, adjusts rumen fermentation patterns and increases rumen propionate ratio.</td><td>84 days [56]<br>24 h [57]</td></tr></tbody></table>

**5. Conclusions**

Mesquite pod feeding markedly improves the productive performance of small ruminants, increasing the DMI and ADG and decreasing the FCR. The positive effect on the DMI can be explained by the enhanced nutritive value, digestibility and palatability of mesquite diets. The heterogeneity of response was substantial in all of the variables examined. The meta-regression demonstrated that the effect size was influenced mainly by the species, breed, level of supplementation and method of processing the mesquite pods. A greater productive response was observed in the studies that supplemented mesquite pods as meal with a range of supplementation from 400 to 450 g/kg DMI. The studies employing in silico CH<sub>4</sub> estimation reported increased emissions when the diets included mesquite pods. In contrast, the in vivo studies demonstrated promising results, showing a significant reduction in CH<sub>4</sub> emissions when mesquite pods were included in small ruminant diets. Therefore, future research should focus on evaluating mesquite pod supplementation using precise methods to assess CH<sub>4</sub> emissions.

**Author Contributions:** Conceptualization, J.C.A.-H.; methodology, J.C.A.-H., E.d.J.F.S. and M.B.; software, J.C.A.-H. and Á.G.G.; validation, S.S.V.-S., O.E.d.R.R., J.C.K.-V. and E.K.; formal analysis, J.C.A.-H. and E.C.-G.; investigation, S.S.V.-S., E.d.J.F.S., J.C.K.-V. and Á.G.G.; resources, J.C.A.-H., E.d.J.F.S. and Á.G.G.; data curation, E.C.-G., S.S.V.-S. and M.B.; writing—original draft preparation, J.C.A.-H., E.C.-G. and S.S.V.-S.; writing—review and editing, E.d.J.F.S., E.C.-G., S.S.V.-S., E.A.P., J.C.K.-V., E.K. and Á.G.G.; visualization, J.C.A.-H. and M.B.; supervision, J.C.A.-H. and E.d.J.F.S.; project
administration, J.C.A.-H.; funding acquisition, J.C.A.-H. and Á.G.G. All authors have read and agreed to the published version of the manuscript.

**Funding:** This work was supported by the Mexican Ministry of Education (SEP-PRODEP-823).

**Institutional Review Board Statement:** Not applicable.

**Informed Consent Statement:** Not applicable.

**Data Availability Statement:** The database used and analyzed is available from the corresponding authors upon reasonable request.

**Acknowledgments:** Eduardo Cardoso-Gutiérrez thanks the Consejo Nacional de Humanidades, Ciencias y Tecnologías (CONAHCYT) of Mexico for the financial support.

**Conflicts of Interest:** The authors declare no conflicts of interest.

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