Opuntia (Cactaceae; Opuntioideae) Flower-Visiting Insects: Comparison
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Please note this is a comparison between Version 2 by Lindsay Dong and Version 1 by Alfredo Ramírez-Hernández.

Opuntia species are cacti with high ecological, economic and conservation interest in semiarid environments, particularly in Mexico. Despite the economic and cultural importance of Opuntia, there is a significant lack of knowledge about the flower-visiting insects and their taxonomic identity. Although some Opuntia species could be visited by birds such as hummingbirds, the most dominant taxonomic group of pollinators are the insects. 

  • insecta
  • pollination
  • drylands
  • core species
  • conservation

1. Introduction

Cactaceae Juss, 1789, is a highly diversified family of xerophytes that are dominant through the arid and semiarid environments of the Americas, which is its center of origin and diversification [1]. Cacti comprise approximately 1400–1800 described species in the world [2][3][4], and Mexico is the country with the greatest diversity, with 52 genera and 850 species, of which an estimated 84% are endemic [4][5]. In addition, nearly 31% of cacti are globally threatened [6] due to changes in land use; introduction of exotic species; and uncontrolled harvesting of these plants for use as food, raw material, and other purposes [7]. Some of them are listed by the International Union for the Conservation of Nature (IUCN) under various threat categories (https://www.iucnredlist.org/, accessed on 22 April 2021), which points to the need for conservation efforts.
Opuntia Mill. (Cactaceae; Opuntioideae) is the richest genus within the Cactaceae with nearly 200 described species [2][8][9]. Opuntia species are well-adapted to drought-stressed conditions [10], being highly distributed throughout arid and semiarid environments [9]. The genus Opuntia is endemic to the Americas and it is distributed from Canada to Argentina [8], showing a high number of regional endemic species in Mexico [11].
However, some Opuntia species were introduced to other continents after the Spanish conquest [12][13][14] due to their traditional uses as medicinal plants, fruits, vegetables, dyes, food ingredients, and forage, among others [15][16][17][18].
In some cases, they have been naturalized [19][20], often resulting in problems for conservation efforts, as in Spain [20]. In some other cases, they became naturalized without any ecological problem and became a useful genetic resource with promising potential applications in cosmetics, the pharmaceutical industry, and bioenergy production [16][17]. In Mexico, the genus has a marked importance both historically and culturally because of the production of “nopal” (the Mexican denomination for the edible young cladodes developed by cacti species belonging to the genera Opuntia and Nopalea, which is translated into English as “prickly pear”) and “tuna” (Mexican name for the edible fruit of cacti species belonging to the genera Opuntia and Nopalea). In this regard, it has been estimated that the exploitation of Opuntia plants could generate jobs for approximately 2000 families in rural areas [21]. Asexual propagation in Opuntia cacti occurs naturally by stem or cladode detachment [22]. Nonetheless, sexual reproduction remains important, especially for generating viable genetic pools in wild populations, as well as for the production of “tunas” [23]. Sexual reproduction depends mainly on insects [24][25]. Therefore, improving our understanding of the relationships between Opuntia plants and insect pollination is critical for the conservation of both plants and insects [26][27][28] as well as for crop productivity [24]. Insect pollination has probably been crucial for the diversification and success of Opuntia in colonizing the American continent [1][23]. Bees in particular have been widely recognized as the main pollinators of Opuntia species [29], where mellitophilous syndrome dominates [25]. Visitation by insects depends on the color and scent of the flower (which is usually hermaphroditic), taste and quality of the nectar, and pollen production [30], as well as on the morphology of the visitors and the spatiotemporal abundance of both flowers and flower visitors [31]. Although some Opuntia species could be visited by birds such as hummingbirds (see Pimienta and del Castillo [32]), the most dominant taxonomic group of pollinators are the insects.

2. Opuntia (Cactaceae; Opuntioideae) Flower-Visiting Insects

In Mexico, Opuntia species represent one of the most important crops, because they cover about 30% of the country’s land area, and they are mainly distributed throughout arid and semiarid regions (Figure 1) [33]. Mexico is the main producer of prickly pears, supporting 43% of annual world production, which is estimated at 1,060,000 t in an area of 100,000 ha [34]. The area planted with "nopal" in Mexico in 2019 was 45,746 ha, which was mainly in the Mexican High Plateau (central Mexico).

Figure 1. Distribution of Opuntia species throughout Mexico, highlighting the states where studies in articles retrieved were carried out, as extracted from the Global Biodiversity Information (GBIF).

2.1. Timeline of

Opuntia

Studies

Since the botanical family Cactaceae is endemic to the Americas [9], it is not surprising to find a higher number of articles published on this continent, particularly in the U.S.A. and Mexico (nine articles each). It is evident that insect pollination attracted the interests of early researchers [35][36], who studied the main flower-visiting insects on O. humifusa and O. macrorhiza, with a taxonomic description of new bee species of the genus Perdita (Hymenoptera) in the U.S.A.
Further research papers were published in the 1970s that were focused on both pollination and the reproductive system of Opuntia spp. Grant and Grant [37] and Grant et al. [38] studied the behavior of insects and their efficiency as pollinators of O. basilaris, O. littoralis, and O. lindheimeri. At the end of the 1980s, new research was conducted on flower-visiting insects in San Luis Potosí in the southern Chihuahuan Desert (Mexico) [39][40].
In the twenty-first century, 18 studies have been published around the world: six in Mexico and 12 in other countries. These studies were focused on Opuntia biology, including pollinators [41]. Outside of the Americas, Opuntia species are recognized as exotic, with some considered fully naturalized, and they are often cultivated and used [42][43]. For example, Opuntia species have been exploited since the eighteenth century in Sicily, which is the center of cultivation of this genus in Italy [24]. Other studies addressed the invasive nature of certain Opuntia species, which can modify the native community structure due to their greater attraction of native insects in comparison to native plants [19][20][44].

2.2. Insect Diversity: Are All the Species Efficient in Pollen Transport?

The studies conducted worldwide indicate that the main flower-visiting insect species in Opuntia spp. are bees (Hymenoptera, Apidae), beetles (Coleoptera), and some lepidopterans (Lepidoptera). However, the effectiveness of pollinator species varied broadly. Early studies [37][38] showed that both bees and beetles were the main groups of insects that pollinated Opuntia plants; however, beetles species were not found to be efficient for pollen transport because they feed on the stamens and petals [37][38]. Therefore, the probability of pollen adhering to their bodies is very low [45]. Moreover, beetles do not fly in search of more flowers, and thus, cross-pollination between plants is limited. In addition, the body size of insects plays a critical role in determining their effectiveness as pollinators [45]. Due to their smaller body size, bees of the genus Perdita sp. (2.0 mm to 10.0 mm) are not considered very effective pollinators, because they can slip into a flower without coming into contact with the stigma [38], thus limiting pollination. The recognized effective pollinators of Opuntia are medium and large-sized bees, such as species belonging to the genera Diadasia, Lithurge, Melissodes, Bombus, Agapostemon, and Megachile [38][46]. The few studies carried out in Argentina, Brazil and Canada were devoted to learning the structure of Opuntia flowers and the diversity of insects that visit them. For example, when bees touch the filaments, they stimulate the movement of sensitive stamens, causing the Opuntia flower to hide most of its pollen from flower visitors [23]. This floral adaptation benefits oligolectic (pollen-specialist) pollinating bees, which can reach the lower layers of the anthers, where 80% of the flower pollen is located [47]. According to the results obtained in the meta-analysis, oligolectic species (such as Ptilothrix fructifera, Lithurgus rufiventris and Cephalocolletes rugata) are the only effective pollinators in Opuntia [47][48][49]. Reliance on oligolectic bees for pollination has been similarly documented for a high number of plant species belonging to different plant families [50][51], including other Cactaceae [41][52]. Therefore, this seems to be quite likely for all Opuntia species as well. However, evidence in studies of other plant taxa highlights that the pollination effectiveness of different flower-visiting insects can also vary depending on other factors, such as season or geographical area, where other insects, including non-oligolectic bees, can act as effective pollinators [50]. For instance, in Lobularia maritima (L.) Desv. (Brassicaceae), the effectiveness of ants in pollination during the summer was comparable to the most effective insects in other periods such as spring [50]. Ants were also the main pollinators of Jatropha curcas L. (Euphorbiaceae) in Mediterranean croplands, unlike what is described for this species in its native distribution area [53]. As Opuntia spp. display a wide blooming period (ranging from early spring to the whole summer), and some of them are important crop species that are commonly grown out of their native area, it would be interesting to examine whether ants (as they are usually documented to be abundant flower visitors) or other animal species might also constitute effective pollinators in certain cases. However, it is also important to bear in mind that ants (as occurs with other common flower-visiting insects) could not generally participate in active Opuntia pollination, as these plants have extrafloral nectaries (EFN). Ecologically, extrafloral nectar is important as a sugared reward for ants to assure ant protection against herbivores [54][55][56]. Having EFN, plants also prevent ants from taking nectar directly from flowers, thus ensuring pollination by other more efficient species [57] in order to achieve successful cross-pollination between different Opuntia individuals. In this regard, ants could be even considered nectar thieves, because the pollen is not transported to other plant individuals as a result of their visit (mainly due to their small body size and absence of hair), and the plant does not benefit from the interaction from the sexual reproduction point of view (e.g., Komamura et al. [58]). Although there are few ant species able to transport pollen, the usual presence of metapleural gland secretion on the integument can also reduce the viability of pollen grains in these particular cases, as documented by Beattie et al. [59], Rostás et al. [60], and Rostás and Tautz [61], therefore, not contributing to the effective cross-pollination. In addition, Rostás et al. [60] found that ants visiting the flowers of Euphorbia seguieriana Neck. do not facilitate outcrossing because the worker ants were mainly plant dwellers; therefore, it was only flying insects that were responsible for pollination, thus increasing the real sexual reproduction measured by success in seed germination rates. Therefore, the role of ants (or other animal species) in Opuntia pollination beyond oligolectic bees should be carefully studied in order to achieve a better understanding of the reproductive ecology of these plants. It is well known that cross-pollination mediated by insects in Opuntia species is crucial for crop productivity [62]. According to Ávila-Gómez et al. [63], Opuntia spp. crop productivity (e.g., number of fruits) is related to the number and species composition of bees. In addition, cross-pollination maintains the genetic diversity in plant populations. Nonetheless, this issue has not been studied for Opuntia spp., and further research must focus on understanding how these complex interactions could support the genetic variability of Opuntia spp. and the impact it might have on the plant–pollinator network structure.

2.3. The Relationship between

Opuntia

and Insects in Mexico

Two studies were conducted in the Mapimi Biosphere Reserve, which is part of the Chihuahuan desert. These studies were focused on O. rastrera [40] and O. microdasys [64]; however, few records of flower visitors were obtained. In contrast, Morales-Trejo et al. [32] studied the insect diversity associated with O. pilifera, and they recorded the highest number of insects so far (Hymenoptera, Coleoptera, Hemiptera, Diptera, Neuroptera, and Lepidoptera were identified). Differences in the number of species recorded could be due to the different sampling methods employed. For instance, studies performed on O. rastrera and O. microdasyswere focused on visual records of the frequency that insects pollinated Opuntia flowers. The research conducted on O. pilifera employed a more complete set of harvesting methods mainly consisting of direct collection using entomological nets to capture flying insects and entomological forceps for species found inside the flowers [32]. Santa Anna-Aguayo et al. [65] used a sampling method that consisted of video camera recordings in order to study the behavior of the introduced species A. mellifera and the native species Lithurgus littoralis. They highlighted possible interference by competition between native and non-native bee species that visit the flowers of O. huajuapensis. The use of diverse sampling methods to study the same group of insects often produces different results. This may generate biased conclusions that in turn make it difficult to compare the diversity of species and interactions, and their implications for biodiversity conservation [66]. It is difficult to standardize a single method for insect sampling, and a recommendation to achieve more complete coverage of diversity is to coordinate all data produced by different sampling approaches [67]. In this regard, assimilating information collected using multiple methods, observations, and other sources into a composite database on Opuntia and insect interactions would provide a basis for a better understanding of plant–insect interactions between these groups. Moreover, focusing research efforts on interactions between threatened species of Opuntia and insects will help the conservation and management of these species.

2.4. The Role of Core Species in the Community Structure

We found that O. ficus-indica, O. pilifera, and O. monacantha constitute the generalist core of the Opuntia spp. global network (Figure 2; 3), whereas only O. pilifera was core in the Mexican network (Figure 2). In a broad sense, the importance of Opuntia in the network can vary according to the number of studies carried out in each species as well as the sampling effort. This is probably the case for O. ficus-indica, which is a domesticated species with a long history of uses and has been cultivated in several countries [68][69].

Figure 2. Circular network configuration of flower-visiting orders of insects associated with Opuntia species constructed with the databases of the retrieved articles between 1911 and 2020. Databases were sorted to construct a (a) global network and (b) network of Mexico. Numbers and abbreviations are defined as follows: Hym: Hymenoptera; Col: Coleoptera; Lep: Lepidoptera; Dip: Diptera; Ort: Orthoptera; Hem: Hemiptera; Neu: Neuroptera; Der: Dermaptera; Thy: Thysanoptera. 1: O. ficus-indica; 2: O. pilifera; 3: O: polyacantha; 4: O. fragilis; 5: O. stricta; 6: O. elata; 7: O. maxima; 8: O. tomentosa; 9: O. monacantha; 10: O. lindheimeri; 11: O. robusta; 12: O. anacantha; 13: O. rastrera; 14: O. basilaris; 15: O. humifusa; 16: O. macrorhiza; 17: O. quimilo; 18: O. microdasys; 19: O. littoralis; 20: O. viridirubra; 21: O. spinulifera; 22: O. sulphurea; 23: O. phaeacantha; 24: O. retrorsa; 25: O. streptacantha; 26: O. dillenii; 27: O. huajuapensis; 28: O. macrocentra; 29: O. engelmannii.

Figure 2. Examples of species that constituted part of the core in both global and Mexico networks. Upper figures show the flowering Opuntia species (a) O. ficus-indica, (b) O. pilifera, and (c) O. monacantha and lower figures show core bees (d) Diadasia rinconis, (e) Agapostemon texanus, and (f) Bombus terrestris. Note that the photos are not scaled. Figure 2. Examples of species that constituted part of the core in both global and Mexico networks. Upper figures show the flowering Opuntia species (a) O. ficus-indica, (b) O. pilifera, and (c) O. monacantha and lower figures show core bees (d) Diadasia rinconis, (e) Agapostemon texanus, and (f) Bombus terrestris. Note that the photos are not scaled. For this reason, it is not surprising that O. ficus-indica constitutes part of the core species in the global network (Figure 2a; 3a). O. ficus-indica was first introduced to Europe via Spain during the fifteenth century, and it has been cultivated in many parts of the world for various purposes, including carminic acid extraction from Dactylopius coccus Costa, 1835 [18][70]. In this regard, Padrón et al. [20] found that O. maxima is an invader species that behaves as a core species in native communities, where it becomes naturalized. It is known that flowers of alien plants are usually compatible with the body size of native insects [71]. Accordingly, these plants may attract a broad number of native insect pollinators, acting as competitors of the native flora, modifying the network’s structure and the function of the original communities because pollen transported by insects may be dominated by pollen from alien plants [43][72]. In addition, some Opuntia species have no limits to their pollen production, so they might sustain a vast community of insects, thus increasing seed production. Therefore, the probability that these species would expand their range of distribution is high [19]. In the Mexican network (Figure 2b), O. pilifera alone constituted the core species. However, these results are probably influenced by the study conducted by Morales-Trejo et al. [32], who carried out extensive field observations with the goal of recording the highest possible number of insect species and individuals visiting the flowers of O. pilifera and finding seven orders of insects. They also found a temporal segregation of insects in the morning versus the afternoon. This variation can most likely be attributed to the environmental pulses that occur at different times of the day because of changes in the main abiotic factors across the day (such as humidity, temperature, solar irradiation, etc.), which can affect insect behavior and activity [73]. More comprehensive studies on the pollination ecology of Opuntia species from Mexico, ideally conducted with standardized insect harvesting methodologies, would be necessary to ascertain whether O. pilifera is still a core species in the Mexican network, as well as to elucidate the role of other Opuntia species as core species for this network. In terms of the insect fauna recorded visiting Opuntia flowers, species belonging to the genera Diadasia, Lithurge, Melissodes, Bombus, Agapostemon, and Megachile, which were also the most effective pollinators, were core to the global network. Species of these genera have been documented as the most effective plant pollinators due to their body size [38][46]. The Eurasian honeybee, A. mellifera, had the highest core value. Despite the global economic importance of A. mellifera [74][75], it is an exotic species in the Americas [76], and its effects on the structure and functioning of native communities should also be considered. In this regard, Santa Anna-Aguayo et al. [65] found that females of L. littoralis avoid flowers that have been previously visited by A. mellifera. There is still little information about the competition effect of honeybees on native bees, and therefore, general conclusions cannot be stated. In spite of the fact that A. mellifera is included in the IUCN Red Lists [77][78], it could be of great interest to assess the effects of this species on the conservation of native pollinators in areas where it is not native, such as the American continent. It is important that future research prioritize the study of native bees to discover their conservation status, since competition with A. mellifera could be reducing their populations and affecting the reproductive capacity of Opuntia species. Bumblebees (Bombus sp.) face important conservation challenges in North America due to their natural habitat transformation for large-scale intensive agricultural production [79][80][81] with many species included in the IUCN Red Lists. Therefore, to maintain (or recover) the conservation status and population levels of bumblebees, it could be useful to maintain the Opuntia species that they visit.

3. Conclusions and Future Perspectives

Despite the historical, economical, and cultural importance of Opuntia species in Mexico, the scarce number of studies about the insect pollination of these species is remarkable, and research is completely lacking on Opuntia with conservation interests. Further research is needed to standardize an effective sampling protocol to monitor the broad insect diversity. Bees have been considered the main and most efficient pollinator insects, and this has probably diverted attention from other entomofauna. More research is needed to improve knowledge of the diversity of flower-visiting insects associated with Opuntia, especially directed toward restricted endemic, rare, or threatened plant species. These future studies should analyze the roles of all visitors in natural community maintenance and the influence of crop productivity. In addition, it is important to expand knowledge of both the influence of exotic entomofauna on native fauna, and the impact that exotic Opuntia spp. can have on specialized pollinators, thereby providing us with a broader panorama of this interaction. Finally, because pollination is crucial for crop production, a better understanding of ecological interaction networks would inform management measures undertaken to strengthen biodiversity and agriculture sustainability and productivity in arid and marginal lands.

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