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Article

Pollinator Species at Risk from the Expansion of Avocado Monoculture in Central Mexico

by
Jesús E. Sáenz-Ceja
1,*,
J. Trinidad Sáenz-Reyes
2 and
David Castillo-Quiroz
3
1
Centro de Investigaciones en Geografía Ambiental, Universidad Nacional Autónoma de México, Morelia 58190, Michoacán, Mexico
2
Campo Experimental Uruapan, Instituto de Investigaciones Forestales, Agrícolas y Pecuarias, Uruapan 60500, Michoacán, Mexico
3
Campo Experimental Saltillo, Instituto de Investigaciones Forestales, Agrícolas y Pecuarias, Saltillo 25315, Coahuila, Mexico
*
Author to whom correspondence should be addressed.
Conservation 2022, 2(3), 457-472; https://doi.org/10.3390/conservation2030031
Submission received: 28 June 2022 / Revised: 23 July 2022 / Accepted: 25 July 2022 / Published: 1 August 2022
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Abstract

:
The monoculture of avocado (Persea americana) has triggered the loss of large forested areas in central Mexico, including the habitat of threatened species. This study assessed the potential habitat loss of ten threatened pollinator species due to the expansion of avocado monoculture in Mexico. First, we modeled the distribution of avocado and pollinators. Then, we overlapped their suitable areas at a national level and within the Trans-Mexican Volcanic Belt (TMVB). We also identified the areas with more affected pollinators and coinciding with protected areas. As a result, 78% of the suitable areas for avocado coincided with the distribution of at least one pollinator. Although only two pollinators lost more than one-fifth of their distribution at a national level, the habitat loss increased to 41.6% on average, considering their distribution within the TMVB. The most affected pollinators were Bombus brachycephalus, B diligens, Danaus plexippus, and Tilmatura dupontii, losing more than 48% of their distribution within this ecoregion. The areas with a greater number of affected species pollinators were found in the states of Michoacán, Mexico, and Morelos, where most of the area is currently unprotected. Our results suggest that the expansion of the avocado monoculture will negatively affect the habitat of threatened pollinators in Mexico.

1. Introduction

Pollinators are a functional group that includes insects, mammals, and birds, which are crucial for providing the pollination service for wild plants and crops [1]. Pollinator species assist the reproduction of at least 78% of the angiosperms in temperate regions, 94% in tropical ecosystems [2], and 68% of the crops [3]. Therefore, pollination plays a fundamental role in maintaining the structure and function of forest ecosystems, agricultural production, human nutrition, and food security [4].
The decline in pollinator populations has become a global issue for at least the last three decades [5,6,7]. Land-use change, competition with exotic pollinators, parasitic infections, use of pesticides and chemical fertilizers, and climate change are the main drivers of the decrease in pollinator abundance and richness [8,9]. Among these drivers, land-use change is recognized as the main force of pollinator decline due to habitat loss, degradation, and fragmentation, which implies the disruption of ecological processes and biotic interactions that limit the population regeneration long-term [10,11]. Moreover, pollination decline is more evident in homogeneous landscapes such as plantation forests and monocultures due to poorer-quality local habitats and fewer floral resources [12,13].
The main native pollinator groups affected by the land-use change are bumblebees, bees, wasps, butterflies, bats, and hummingbirds [6,14]. The abundance of native pollinators has decreased by 44% in high-intensity croplands of tropical regions, reaching up to 80% in Lepidoptera and Diptera species, 30% of Passeriformes, and 44% for Hymenoptera [7]. The pollinator decline will impact mainly restricted-distribution species and those with a narrow diet breadth and solitary behavior [8,15], particularly those distributed in anthropogenic landscapes [16]. In addition, wild plants specialized in a single pollinator will be pollen-limited [17]. On a global scale, the decrease in pollinators will represent a risk to food production [4].
Mexico is the leading producer of avocado (Persea americana Mill.) variety Hass, providing 43% of the global demand [18]. However, the extensive monoculture of this crop has been associated with the loss of 30% of the extent of temperate forests between 1990 and 2006 within the locally known “Avocado Strip” of the state of Michoacán, the global hotspot of avocado production, located in western-central Mexico [19]. In this region, land-use change rates related to avocado cover expansion reached 16 km2 yr−1 between 2007 and 2014 [20]. The Avocado Strip has recently spread to Jalisco and Mexico State, adjacent to Michoacán; these three states account for 85.5% of the surface under avocado cultivation [21]. In addition, the expansion of avocado cultivation has reached the states of Nayarit, Morelos, and Puebla, within the Trans-Mexican Volcanic Belt (TMVB) [22,23].
Pine-oak forest, tropical montane cloud forest, and subtropical scrubland have been the most affected ecosystems due to the deforestation associated with the expansion of avocado monoculture in Michoacán [24]. In terms of wildlife biodiversity, the conversion of various types of native forests to avocado orchards has been linked to less abundance of wild felines such as the mountain lion (Puma concolor Linnaeus), the margay (Leopardus wiedii Schinz), and the bobcat (Lynx rufus Schreber) due to the loss of habitat and spatial connectivity [25], as well as pollinators, a phenomenon associated with the wide use of pesticides and chemical fertilizers [26]. In addition, since avocado fruiting depends strongly on pollination [27], the rent of honey bee (Apis mellifera Linnaeus) hives has become increasingly common to cover the pollen requirements for this crop [28]. However, the introduction of non-native species can replace native pollinators long-term as a result of competence for floral resources [29].
Due to the global increase in avocado consumption during the last 25 years [30], the agri-food policies of the Mexican government have incentivized the massive establishment of Hass avocado inside and outside the Avocado Strip of Michoacán [31]. Indeed, to cover the growing demand for Hass avocado in national and international markets, the authorities of the agricultural sector intend to increase the national production by 67% by 2030 [32]. This rising necessarily will imply the expansion of the area under avocado cultivation, which in turn would trigger the loss of large forested areas where avocado cultivation is suitable, including the habitat of pollinator species.
Little is known about the effect of the expansion of avocado monoculture on the habitat of pollinator species. Among them are included threatened species listed on the Red List of the International Union for the Conservation of Nature and Natural Resources (IUCN) [33] (IUCN, 2022) and the Mexican Endangered Species Act [34]. For example, under this scenario is the monarch butterfly (Danaus plexippus Linnaeus). This migratory pollinator overwinters in conifer forests of the Monarch Butterfly Biosphere Reserve (MBBR), where circa 10 km2 of avocado orchards have been established within the buffer zone of this protected area [35]. Furthermore, many pollinator bats are distributed in temperate and subtropical forests of the TMVB, on areas covered by avocado plantations [36].
The main limitation to assessing the effect of avocado expansion on pollinator habitat is the lack of information on the distribution of pollinator species and the surface that overlaps with suitable areas for avocado cultivation under current climatic conditions. For this purpose, ecological niche modeling (ENM) can be a helpful tool to delineate the spatial distribution of the species according to their environmental requirements, such as temperature, rainfall, elevation, and soil types on which they can grow [10]. Modeling by maximum entropy (Maxent) has become one of the main ENM methods since it enables obtaining of robust estimations of the environmental suitability of restricted species or with scant occurrence data [37,38].
The aims of this study were: (i) to identify the threatened pollinator species distributed in suitable areas for avocado monoculture in the TMVB of central Mexico; (ii) to model the potential distribution of P. americana and the threatened pollinator species; (iii) to identify the pollinator species with high potential habitat loss due to the expansion of avocado monoculture; and (iv) to detect the most vulnerable areas to pollinator habitat loss and those included within protected areas.

2. Materials and Methods

2.1. Acquisition of Species Occurrence Data

First, we identified the threatened pollinator species listed in the IUCN Red List [33] and the Mexican Endangered Species Act [34] with occurrence records in temperate forests along the TMVB. As a result, we identified ten pollinator species, including four insects, four bats, and two bird species. Then, we downloaded their occurrence records in Mexico from the Global Biodiversity Information Facility (GBIF) [39] (Table 1), a database that includes records from human observations, preserved specimens, and species occurrence in field-based papers.
In the case of the monarch butterfly (D. plexippus), we only considered the records belonging to the migratory route that crosses from northern to central Mexico along with the Eastern Sierra Madre and the overwintering sites in central Mexico. Records pertaining to populations of southern and western Mexico were not included in the study [40,41].
Second, we identified georeferenced points of presence of Hass avocado orchards along the TMBV through photo-interpretation of satellite imagery with Google Earth Pro [42] with dates between 2 October 2020 and 18 April 2021, at a scale of 1:20,000, following Sáenz-Ceja and Pérez-Salicrup [35]. The Hass avocado occurrence records were complemented with different studies that reported the location of orchards within the Avocado Strip [21,43,44,45,46,47,48]. The total number of Hass avocado occurrences was 241 (Figure 1).

2.2. Species Distribution Modeling

Since climate seasonality plays a strong role in delineating the distribution of many animal and plant species in subtropical and tropical regions of Mexico [36,49], we downloaded the layers of 19 bioclimatic variables [50], as well as soil type [51] and elevation [52] in raster format at a spatial resolution of 1 km2 (Table 2), which were clipped to the polygon of Mexico. Then, we cleaned the species occurrence database through boxplots (function Boxplot, R package ‘car’) to identify outliers regarding the mentioned environmental layers [53]. The final number of occurrences is shown in Table 1. The cleansing of presence data was conducted in R version 4.1.2 [54].
The species distribution of P. americana and pollinator species was modeled with Maxent version 3.4.1 [56], using 75% of occurrence points for the modeling and 25% as verification points, logistic regression, and 1000 iterations. Since the exclusion of highly correlated variables does not significantly influence model performance [57], we used the 21 bioclimatic variables for the modeling. In addition, we performed Jackknife analyses to assess the contribution of the environmental variables for the modeling [58].
The species distribution models were evaluated through analyses of the area under the curve (AUC) and partial-ROC (Receiver Operation Characteristics), considering 50% of the presence data as verification points and 1000 iterations (function kuenmproc, R package ‘kuenm’) [59]. AUC values between 0.7 and 0.9 indicated rational predictive models, whereas AUC values higher than 0.9 denoted models with a high predictive capacity [60]. Furthermore, partial-ROC values between 1 and 2 were associated with robust models; however, they were assessed through Z-tests to determine whether they differed from random (function z.test, R package ‘TeachingDemos’) [61].
The spatial models were reclassified to discard cells with a low probability of occurrence, deleting those pixels with a probability less than the 25th percentile [62]. The resultant binary maps were converted to vectorial format with Lambert Conformal Conic projection. Then, we deleted polygons that overlapped water reservoirs and urban settlements [53], using as a base the Mexican Vegetation and Soil Use Cover Map (7th Series), with a scale of 1:250,000 [63].

2.3. Effect of the Expansion of Avocado Monoculture on Pollinator Habitat

First, we estimated the potential extent (km2) suitable for cultivating Hass avocado within central Mexico. Second, we calculated the potential extent of the pollinator species at a national level and within the TMVB, identifying the ecoregions where they are distributed, according to the North American Environmental Cooperation Commission (CEC) classification, level II [64]. Then, we overlapped the maps of the Hass avocado and the pollinator species distribution to estimate the potential surface affected by the expansion of avocado monoculture. In addition, we summed the pollinator species distribution maps and intersected the resultant map with the Hass avocado map to obtain the areas with the most pollinator species at risk. Finally, we overlapped these areas with the map of federally protected areas [65].

3. Results

3.1. Species Distribution Models

AUC values ranged between 0.817 and 0.982, whereas partial-ROC values spanned between 1.313 and 1.962; all of them were independent of random according to the Z-test (p < 0.001) (Table 3). The species distribution was influenced mainly by elevation (80% of the species), temperature seasonality (Bio04) (40%), and precipitation seasonality (Bio15) (40%). Other relevant variables were the minimum temperature of the coldest month (Bio06) (30%), the annual temperature range (Bio07) (30%), and precipitation of the wettest quarter (Bio16) (30%).
The elevation was the most relevant variable for the potential distribution of the short-headed bumble bee (Bombus brachycephalus Handlirsch), the abejón bumble bee (Bombus diligens Smith), and the Mexican big-eared bat (Corynorhinus mexicanus Allen). Bio06 determined the distribution of the Mexican long-tongued bat (Choeronycteris mexicana Tschudi) and the lesser long-nosed bat (Leptonycteris yerbabuenae Martínez & Villa). Bio07 was the most relevant variable for the monarch butterfly (D. plexippus) and the Mexican long-nosed bat (Leptonycteris nivalis Saussure). Bio15 was determinant for the distribution of the Steindachner´s bumble bee (Bombus steindachneri Handlirsch) and the Rufous hummingbird (Selasphorus rufus Gmelin), whereas Bio16 was the most relevant variable only for the sparkling-tailed woodstar (Tilmatura dupontii Lesson).

3.2. The Potential Distribution of Persea americana Mill

The potential distribution of Hass avocado within the TMVB and a small portion of the Southern Sierra Madre (SSM) reached an extent of 21,338 km2, distributed in eight states (Figure 1), of which Michoacán (48% of the total area), Jalisco (26%), and Mexico State (12%) accounted together the 86% of the total extent (Figure 2a). The suitable areas for cultivating Hass avocado were found in seven landscape types, of which 37% of the extent were located on croplands, 30% in pine-oak forests, and 12% in pine forests. Other landscape types found in suitable areas were oak forests, grasslands, tropical dry forests, and tropical montane cloud forests (Figure 2b). The suitable areas were found in an elevational gradient spanning 1200–2800 m; however, 56% of the total extent was located between 1800–2400 m (Figure 2c). The most dominant soil type in suitable areas was Andosol (34% of the total area), followed by Luvisol (14%), Cambisol (13%), and Acrisol (12%) (Figure 2d). In addition, 78% of the suitable area coincided with the distribution of at least one threatened pollinator species.

3.3. Pollinator Species Distribution and Habitat Loss

The potential distribution of the ten pollinator species is shown in Figure 3. No species were restricted to the TMVB, but they were distributed in at least three ecoregions. The species in fewer ecoregions were B. steindachneri, D. plexippus, and T. dupontii. The bat species were generally found in more ecoregions (Table 4). The species with minor extent was D. plexippus (31,286 km2), followed by B. brachycephalus (34,702 km2) and T. dupontii (56,240 km2). In contrast, the species more spread were L. nivalis, L. yerbabuenae, and C. mexicana.
Only two species (B. brachycephalus y B. diligens) had areas with more than 20% of their potential distribution that overlapped with suitable areas for Hass avocado cultivation at a national level. The remaining species had habitat loss of between 3.1 and 16.7% (Table 4). However, when considering the habitat loss within the TMVB, these percentages increased to 41.6% on average. The species that lost more than 48% of their habitat within the TMVB were B. brachycephalus, B. diligens, T. dupontii, and D. plexippus. In contrast, C. mexicanus, C. mexicana, and S. rufus had the lowest percentages of habitat loss.
The zones with the highest number of species (9–10) that overlapped suitable areas for Hass avocado cultivation represented 3.9% of the total extent with the presence of threatened pollinator species (16,660 km2). These zones were found mainly in five locations: the southern State of Mexico, northern Morelos, and small portions of western (Tancítaro Peak), central (sierra of Madero), and eastern (sierra Mil Cumbres) Michoacán (Figure 4). The zones hosting between seven and eight pollinator species were located in the Avocado Strip of Michoacán, accounting for 28.2% of the total area, whereas zones with between five and six pollinator species (39.3% of the total area) were found in eastern Jalisco and central-eastern Michoacán. Zones hosting between one and four pollinator species summed up 28.6% of the total area, found in the highlands of the Avocado Strip of Michoacán, Mexico State, and Morelos, as well as in the SSM of Michoacán.
The surface within protected areas covered only 9.5% of the area where at least one of the threatened pollinator species is distributed. Regarding this protected surface, the highest percentage was found in areas hosting between one and four pollinator species (24.7%), whereas only 8.5% of the areas hosting between nine and ten pollinator species are currently protected (Table 5). Moreover, eleven protected areas hosted at least one pollinator species, of which seven hosted more than seven pollinator species (El Tepozteco, Chichinautzin, El Carmen, and Valley of Bravo in the State of Mexico, José María Morelos in Michoacán, El Jabalí in Colima, and the Forest Protection Zone 043 in Nayarit, and Jalisco) (Figure 4). Other protected areas hosting less than six pollinator species were Sierra of Manantlán and Sierra of Quila in Jalisco and Colima, as well as the Tancítaro Peak and Monarch Butterfly in Michoacán.

4. Discussion

The expansion of Hass avocado monoculture in Mexico represents a hazard to ten threatened pollinator species that share suitable areas with this crop. The elevation and the climate seasonality (Bio04 and Bio15) were the most relevant environmental variables that shaped the species distribution, results that coincided with studies on the potential distribution of Mexican pollinator bats [36] and the monarch butterfly [41]. Among these variables, elevation plays a significant role in shaping temperature and precipitation gradients in tropical montane regions; for example, temperature decreases when elevation increases, substantially influencing species distribution [66]. In addition, the climate seasonality, typical of subtropical regions in central and southern Mexico, defines phenological patterns of flowering, germination, and growth of wild plants, which in turn influence the abundance and distribution of pollinator species [49,67].
As occurs with pollinators, the elevation and climate seasonality also shape the distribution of tree species, including avocado, in pine-oak forests [68,69]. Consequently, the massive establishment of Hass avocado orchards has replaced many pine-oak forests of Michoacán since this vegetation type meets the temperature, precipitation, elevation, and soil requirements for Hass avocado growth and fruiting [70,71]. Furthermore, pine-oak forests have become the most affected landscape type, with deforestation the primary driver of forest loss, particularly in western Michoacán, where few forest fragments remain with low spatial connectivity [72,73].
The lack of spatial connectivity represents a risk to the integrity and long-term continuity of plant and pollinator populations [74]. Although the potential loss of pollinator habitat was low at a national level, the risk increased when considering the TMVB, with severe implications for the mobility and feeding of the evaluated species. For example, the loss of habitat within the TMVB could imply the interruption of the migratory route from Mexico to the southern United States of pollinator bats such as C. mexicana, L. nivalis, and L. yerbabuenae [36]. Similarly, the conversion from conifer forests to avocado orchards and the massive use of herbicides in adjacent zones to the overwintering colonies of the monarch butterfly would represent less availability of milkweed plants (genus Asclepias, Apocynaceae), the primary nectar source for this butterfly, and the subsequent interruption of its wintering migration [35,75].
Therefore, the preservation of pollinators and associated plant habitat facing the eventual expansion of Hass avocado monoculture is crucial, mainly within the current Avocado Strip. This region has become the global hotspot of avocado production, characterized by high deforestation rates, with an apparent deficit of protected areas that leaves vulnerable the habitat and connectivity between remnant fragments of pine-oak and tropical montane cloud forests [20,68,76]. Moreover, preserving the areas with the highest number of pollinator species at risk is also necessary, such as eastern Michoacán, southern Mexico State, and northern Morelos. In these regions, avocado production has still not reached the levels found in western Michoacán, but they are expected as the following hotspots of avocado production in Mexico [48,70,77].
The establishment of new protected areas can be a helpful mechanism to preserve them since, in many cases, it has demonstrated its effectiveness in decreasing habitat loss [78]. Unfortunately, a trend to establish protected areas in small portions of temperate highlands of the central mountain ranges has existed historically in Mexico, prioritizing criteria such as species richness, scenic beauty, recreative uses, or presence of charismatic species [79,80]. This situation has left unprotected the habitat of several endemic species of flora and fauna in lowlands and subtropical ecosystems [81]. It could explain why less than 10% of the threatened pollinator habitat overlapped with protected areas in this study. Furthermore, it coincides with findings in other pollinator groups, such as hummingbirds [82] and bats [83], as well as for plants such as the genera Abies [84] and Pinus [69].
Hence, we suggest that new protected areas should be created in regions such as the TMVB of Jalisco and Michoacán, where the pressure for the massive establishment of avocado orchards is high [71]. Furthermore, we propose the establishment of biological corridors between the current protected areas, which can enhance the mobility and connectivity of fauna species, including pollinators [76]. For example, between the protected areas located in western Michoacán, southern Mexico State, and Morelos, they could maintain the migratory corridors of bats and the monarch butterflies.
In addition, incorporating agroecological practices in avocado production is crucial to protect the floral resources for pollinators, such as maintaining herbaceous vegetation, biological pest control, and substitution of chemical fertilizers and pesticides [26]. The adoption of such practices applies especially to protecting the monarch butterfly, the only species of this study listed in both the IUCN Red List and the Mexican Endangered Species Act. Its decline is strongly linked to the wide use of herbicides and pesticide exposure along its migratory route [75,85]. Although the evaluated species have not been detected as avocado pollinators [86], the decline in pollinators will drastically affect the production of avocado and other crops, which is highly dependent on this service given by both wild and domesticated pollinators [87].
In addition, due to warmer conditions, a reduction in habitat by up to 67% for bumble bees (género Bombus, Apidae) has been projected, including the three species evaluated in this study [88]. Similar projections are expected for hummingbird species, losing up to 59% of their potential habitat [89], and pollinator bats, such as L. nivalis, which could lose up to 79% of their habitat [90]. Therefore, further research is needed to assess the effect of climate change on pollinator species distribution and its relationship with land-use change related to the establishment of avocado orchards. For example, by 2050, an elevational rise of suitable areas for avocado production in western-central Mexico is expected [24], affecting pollinators living in higher lands.
Finally, it is essential to conduct field-based demographic studies on the effect of avocado cover expansion on pollinator and wild plant populations, which could enable having a clearer view of the population decline, especially in threatened species [91]. This study was the first assessment of the impact of avocado cover expansion on the habitat of threatened pollinators in Mexico. However, more information is needed to prevent their decline due to other human and natural disturbances, such as pest outbreaks, displacement by exotic pollinators, wildland fires, and extreme climatic phenomena.

Author Contributions

Conceptualization, J.E.S.-C., J.T.S.-R. and D.C.-Q.; methodology, validation, and formal analysis, J.E.S.-C.; writing—original draft preparation, J.E.S.-C.; writing—review and editing, J.E.S.-C., J.T.S.-R. and D.C.-Q. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Postdoctoral Fellowship Program DGAPA at the Universidad Nacional Autónoma de México.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on reasonable request from the corresponding author.

Acknowledgments

The authors thank the academic support of the Postdoctoral Fellowship Program DGAPA at the Universidad Nacional Autónoma de México.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. The presence points of Hass avocado orchards and potential distribution of Persea americana Mill. in central Mexico.
Figure 1. The presence points of Hass avocado orchards and potential distribution of Persea americana Mill. in central Mexico.
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Figure 2. Percentage of suitable areas for the cultivation of Hass avocado according to (a) state, (b) land cover, (c) elevation, and (d) soil type. Key of states: Mich: Michoacán; Jal: Jalisco; Mex: México; Nay: Nayarit; Mor: Morelos; Pue: Puebla; Col: Colima; Gro: Guerrero. Key of landscape type: CL: Cropland; POF: Pine-oak forest; PF: Pine forest; OF: Oak forest; GL: Grasslands; TDF: Tropical dry forest; MCF: Montane cloud forest. Key of soil type: And: Andosol; Luv: Luvisol; Cam: Cambisol; Feo: Feozem; Reg: Regosol; Lit: Litosol; Oth: Others.
Figure 2. Percentage of suitable areas for the cultivation of Hass avocado according to (a) state, (b) land cover, (c) elevation, and (d) soil type. Key of states: Mich: Michoacán; Jal: Jalisco; Mex: México; Nay: Nayarit; Mor: Morelos; Pue: Puebla; Col: Colima; Gro: Guerrero. Key of landscape type: CL: Cropland; POF: Pine-oak forest; PF: Pine forest; OF: Oak forest; GL: Grasslands; TDF: Tropical dry forest; MCF: Montane cloud forest. Key of soil type: And: Andosol; Luv: Luvisol; Cam: Cambisol; Feo: Feozem; Reg: Regosol; Lit: Litosol; Oth: Others.
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Figure 3. Potential distribution of ten threatened pollinator species at risk from the expansion of Hass avocado monoculture in Mexico. Species key: (a) Bombus brachycephalus, (b) Bombus diligens, (c) Bombus steindachneri, (d) Danaus plexippus, (e) Choeronycteris mexicana, (f) Corynorhinus mexicanus, (g) Leptonycteris nivalis, (h) Leptonycteris yerbabuenae, (i) Selasphorus rufus, (j) Tilmatura dupontii.
Figure 3. Potential distribution of ten threatened pollinator species at risk from the expansion of Hass avocado monoculture in Mexico. Species key: (a) Bombus brachycephalus, (b) Bombus diligens, (c) Bombus steindachneri, (d) Danaus plexippus, (e) Choeronycteris mexicana, (f) Corynorhinus mexicanus, (g) Leptonycteris nivalis, (h) Leptonycteris yerbabuenae, (i) Selasphorus rufus, (j) Tilmatura dupontii.
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Figure 4. Number of threatened pollinator species that overlapped suitable areas for Hass avocado cultivation in Mexico. Key of protected areas: 1: El Tepozteco; 2: Biological Corridor Chichinautzin; 3: Desierto del Carmen; 4: Valley of Bravo; 5: Monarch Butterfly; 6: José María Morelos; 7: Tancítaro Peak; 8: El Jabalí; 9: Sierra of Manantlán; 10: Sierra of Quila; 11: Forest Protection Zone 043 Nayarit.
Figure 4. Number of threatened pollinator species that overlapped suitable areas for Hass avocado cultivation in Mexico. Key of protected areas: 1: El Tepozteco; 2: Biological Corridor Chichinautzin; 3: Desierto del Carmen; 4: Valley of Bravo; 5: Monarch Butterfly; 6: José María Morelos; 7: Tancítaro Peak; 8: El Jabalí; 9: Sierra of Manantlán; 10: Sierra of Quila; 11: Forest Protection Zone 043 Nayarit.
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Table
Table 1. Identity, habitat, distribution, risk category, and the number of occurrences of pollinator species potentially affected by the expansion of avocado monoculture in central Mexico.
Table 1. Identity, habitat, distribution, risk category, and the number of occurrences of pollinator species potentially affected by the expansion of avocado monoculture in central Mexico.
Scientific NameCommon NameFamilyHabitatDistributionRisk CategoryNumber of Occurrences
IUCN Red List Mexican
Endangered Species Act
Class Insecta
Bombus brachycephalus HandlirschShort-headed bumble beeApidaePOF, TDFMX, CAEN-73
Bombus diligens SmithAbejón bumble beeApidaePOF, TDFMXNT-162
Bombus steindachneri HandlirschSteindachner’s bumble beeApidaePOF, TDFMXEN-194
Danaus plexippus LinnaeusMonarch butterflyNymphalidaeFF, PF, POFCN, US, MXENPR668
Class Mammalia
Choeronycteris mexicana TschudiMexican long-tongued batPhyllostomidaeTEF, TDF, POFUS, MX, CA-A536
Corynorhinus mexicanus AllenMexican big-eared batVespertilionidaeTDF, POF, PFMXNT-175
Leptonycteris nivalis SaussureMexican long-nosed batPhyllostomidaeDS, POF, PFUS, MX-A239
Leptonycteris yerbabuenae Martínez & VillaLesser long-nosed batPhyllostomidaeDS, TDF, POFUS, MX-PR790
Class Aves
Selasphorus rufus GmelinRufous hummingbirdTrochilidaeDS, POF, PFCN, US, MX-A1976
Tilmatura dupontii LessonSparkling-tailed woodstarTrochilidaeTDF, POFMX, CA-A567
Key of habitat: POF: Pine-oak forest; TDF: tropical dry forest; FF: Fir forest; PF: Pine forest; TEF: tropical evergreen forest; DS: desert scrubland. Key of the country: MX: Mexico; US: United States; CN: Canada; CA: Central America. Key of risk category: IUCN Red List: EN: Endangered; NT: Near threatened; Mexican Endangered Species Act: A: Threatened; PR: Under special protection.
Table
Table 2. Environmental variables used for the species distribution modeling of Hass avocado and threatened pollinator species in Mexico.
Table 2. Environmental variables used for the species distribution modeling of Hass avocado and threatened pollinator species in Mexico.
KeyBioclimatic Variable
Bio01Annual mean temperature
Bio02Mean diurnal range
Bio03Isothermality
Bio04Temperature seasonality
Bio05Maximal temperature of the warmest month
Bio06Minimum temperature of the coldest month
Bio07Temperature annual range
Bio08Mean temperature of the wettest quarter
Bio09Mean temperature of the driest quarter
Bio10Mean temperature of the warmest quarter
Bio11Mean temperature of the coldest quarter
Bio12Annual precipitation
Bio13Precipitation of the wettest month
Bio14Precipitation of the driest month
Bio15Precipitation seasonality
Bio16Precipitation of the wettest quarter
Bio17Precipitation of the driest quarter
Bio18Precipitation of the warmest quarter
Bio19Precipitation of the coldest quarter
ElevElevation
SoilSoil type *
* Soil classification of the Food and Agriculture Organization of the United Nations (FAO) [55].
Table
Table 3. Descriptors of the species distribution modeling and contribution percentage of the three most relevant environmental variables in the potential distribution of Persea americana Mill. and ten threatened pollinator species in Mexico.
Table 3. Descriptors of the species distribution modeling and contribution percentage of the three most relevant environmental variables in the potential distribution of Persea americana Mill. and ten threatened pollinator species in Mexico.
SpeciesAUCPartial-ROCZ-Valuep-ValueVariable and Contribution (%)
Persea americana0.9821.9628434.6<0.001Soil (25.4)Elev (17.7)Bio16 (15.9)
Bombus brachycephalus0.9631.8561071.7<0.001Elev (26.9)Bio16 (23.1)Bio12 (12.3)
Bombus diligens0.9531.8272401.7<0.001Elev (32.3)Bio04 (22.4)Bio13 (16.8)
Bombus steindachneri0.9281.685821.8<0.001Bio15 (31.2)Bio06 (15.2)Bio04 (13.3)
Danaus plexippus0.9441.7321934.4<0.001Bio07 (23.5)Elev (18.9)Bio09 (11.4)
Choeronycteris mexicana0.8171.313867.8<0.001Bio06 (28.5)Elev (15.8)Bio07 (13.2)
Corynorhinus mexicanus0.9571.6931250.3<0.001Elev (59.7)Bio05 (7.7)Bio04 (5.0)
Leptonycteris nivalis0.8971.5551142.6<0.001Bio07 (27.1)Bio19 (16.3)Elev (14.1)
Leptonycteris yerbabuenae0.8281.373884.3<0.001Bio06 (37.8)Bio15 (29.3)Bio12 (5.4)
Selasphorus rufus0.8351.5022448.7<0.001Bio15 (19.4)Elev (11.7)Bio10 (10.7)
Tilmatura dupontii0.9361.7593134<0.001Bio16 (30.6)Bio04 (15)Bio15 (8.7)
Table
Table 4. Potential distribution and habitat loss of ten threatened pollinator species due to the expansion of Hass avocado monoculture in Mexico.
Table 4. Potential distribution and habitat loss of ten threatened pollinator species due to the expansion of Hass avocado monoculture in Mexico.
SpeciesEcoregionsPotential
Distribution
Mexico
(km2)		Habitat Loss Mexico
(%)		Potential Distribution TMVB
(km2)		Habitat Loss TMBV
(%)
Bombus brachycephalusCASM, ESM, SSM, TMVB34,70226.514,84057.8
Bombus diligensESM, MHP, SSM, TMVB, WSM51,93323.118,34756.2
Bombus steindachneriSSM, TMVB, WSM104,3555.414,27936.1
Danaus plexippusESM, MHP, TMVB31,28616.7977748.9
Choeronycteris mexicanaCASM, ESM, MC, MHP, SSM, TMVB, TTSP, WD, WPCP, WSM, WSMP353,7040.827,60130.3
Corynorhinus mexicanusESM, MHP, TMVB, WSM, WSMP84,7209.129,47725.1
Leptonycteris nivalisESM, ID, MHP, TMVB, SSM, WD, WSM162,9026.624,12238.6
Leptonycteris yerbabuenaeESM, ID, MHP, SSM, SPCP, TMVB, WD, WPCP256,4673.116,99434.8
Selasphorus rufusMHP, SSM, TMVB, WSM181,3569.442,62633.9
Tilmatura dupontiiCASM, SSM, TMVB56,24015.512,40854.4
Key of ecoregions: CASM: Central American Sierra Madre; ESM: Eastern Sierra Madre; ID: Interior Depressions; MC: Mediterranean California; MHP: Mexican Highland Plateau; TMVB: Trans-Mexican Volcanic Belt; SPCP: Southern Pacific Coastal Plains; SSM: Southern Sierra Madre; TTAP: Tamaulipas–Texas Semiarid Plain; WD: Warm Deserts; WPCP: Western Pacific Coastal Plains; WSM: Western Sierra Madre; WSMP: Western Sierra Madre Piedmont.
Table
Table 5. Potential extent and surface covered by protected areas according to the number of threatened pollinator species that overlapped suitable areas for avocado cultivation in Mexico.
Table 5. Potential extent and surface covered by protected areas according to the number of threatened pollinator species that overlapped suitable areas for avocado cultivation in Mexico.
Number of SpeciesPotential Extent (km2)Protected
Extent (km2)		Protected Areas
9–10653561, 2, 4
7–846744431, 2, 3, 4, 6, 8, 11
5–665495001, 2, 3, 4, 6, 7, 8, 9, 10, 11
3–443035301, 2, 4, 5, 7, 9, 10, 11
1–2481607
Key of protected area categories: BR: biosphere reserve; FFPA: flora and fauna protection area; NRPA: natural resource protection area; NP: national park. Key of protected area: 1: El Tepozteco NP; 2: Biological Corridor Chichinautzin FFPA; 3: Desierto del Carmen NP; 4: Valley of Bravo NRPA; 5: Monarch Butterfly BR; 6: José María Morelos NP; 7: Tancítaro Peak PPFA; 8: El Jabalí FFPA; 9: Sierra of Manantlán BR; 10: Sierra of Quila FFPA; 11: Forest Protection Zone 043 Nayarit NPRA.
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Sáenz-Ceja, J.E.; Sáenz-Reyes, J.T.; Castillo-Quiroz, D. Pollinator Species at Risk from the Expansion of Avocado Monoculture in Central Mexico. Conservation 2022, 2, 457-472. https://doi.org/10.3390/conservation2030031

AMA Style

Sáenz-Ceja JE, Sáenz-Reyes JT, Castillo-Quiroz D. Pollinator Species at Risk from the Expansion of Avocado Monoculture in Central Mexico. Conservation. 2022; 2(3):457-472. https://doi.org/10.3390/conservation2030031

Chicago/Turabian Style

Sáenz-Ceja, Jesús E., J. Trinidad Sáenz-Reyes, and David Castillo-Quiroz. 2022. "Pollinator Species at Risk from the Expansion of Avocado Monoculture in Central Mexico" Conservation 2, no. 3: 457-472. https://doi.org/10.3390/conservation2030031

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