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Floral visitors of Astrophytum myriostigma in La Sierra el Sarnoso, Durango, Mexico.

The composition and abundance of floral visitors are essential to understanding pollination systems and how ecological processes occur in plant and flower visitor interactions. This is perhaps more important for species that are distributed within communities rich in endemics (Moran, 1961; Waser et al., 1996; Giovanetti et al., 2007), as well as for rare species or those with a conservation status, such as many cacti (Moldenke, 1975; Grant and Grant, 1979a; Barbour et al., 1987; Johnson, 1992; Blair and Williamson, 2008; Martinez-Adriano, 2011; Martinez-Peralta and Mandujano, 2011). Understanding which floral visitors are the most effective and important pollinators of these plants is crucial to their conservation and recovery.

The reproductive biology and plant-pollinator interactions are determined by the morphological characteristics of the flower, the type and amount of reward offered, display time, and floral phenology (Murillo, 1981; Cota, 1993; Martinez-Peralta and Mandujano, 2011). For some plant species, cross-pollination is critical for seed production and maintaining viable populations (Coronado-Padilla and Marquez-Delgado, 1981; Huerta-Martinez, 1995; Arizaga et al., 2000; Giovanetti et al., 2007; Blair and Williamson, 2008; Martinez-Peralta and Mandujano, 2011). Cross-pollination is closely related to pollinator availability and pollinator compatibility with specific plant species, and may result in the modification of the population and community in which the interaction occurs (Moeller, 2004).

Within angiosperms, cacti have a large number of species (Anderson, 2001). Many of them are listed as threatened or endangered as a result of several factors that reduce their populations (SEMARNAT, 2010). Cacti are known for their strong dependence on floral visitors as pollen vectors for cross-pollination (Johnson, 1992; Cota, 1993; Valiente-Banuet et al., 1996; Strong and Williamson, 2007). Pollination is considered of great importance for cacti demographic processes because many species are self-incompatible and require animal vectors for pollination (Valiente-Banuet et al., 1997; Strong and Williamson, 2007). Interactions with these vectors generate a "pollination syndrome" that is helpful in predicting the most likely pollinators (Beutelspacher and Ramirez, 1973).

A large spatial and temporal taxonomic diversity within confluent pollinator guilds has been found (Herrera, 1988; Fishbein and Venable, 1996; Groman and Pellmyr, 1999; McIntosh, 2005). Pollination systems evolve rapidly in response to the selective pressure produced by the pollinators (Ollerton, 1996; Wilson and Thomson, 1996; Gomez, 2002) because only a small number of visiting species are potential pollinators (Howell, 1977; Johnson and Steiner, 2000; Gomez, 2002). In most ecosystems, insects are more dominant and diverse than other taxa (Richards, 1986; Del Castillo, 1994; Waser et al., 1996; Pohl-Pohl, 2003). For cacti, the primary pollinators are hummingbirds, doves, bats, hawk moths (Sphingidae), and bees (Apidae, Halictidae, Megachilidae) (Beutelspacher, 1971; Grant and Conell, 1979; Grant and Grant, 1979b; Cota, 1993; Fleming et al., 1996; McIntosh, 2005; Fagua and Ackerman, 2011). However, a number of studies have shown that for cacti with a floral structure similar to that found in Astrophytum myriostigma (e.g. Astrophytum asterias, Echinocereus spp., Ferocactus spp.), medium-large cactus specialist (= oligolectic) solitary bees (e.g. Megachile spp., Diadasia spp., Lithurge echinocacti, Ashmeadiella opuntiae, Svastra duplocincta) are more effective pollinators than other common floral visitors such as ants, flower beetles (Carphophilus spp., Acmaeodera spp.), smaller bees (Perdita/Macrotera spp., Lassioglossum/Dialictus spp.), and non-specialist (= polylectic) bees (Apis mellifera, Lassioglossum/Dialictus spp.) (Beutelspacher, 1971; Grant and Grant, 1979a, 1979b; Cota, 1993; McIntosh, 2005; Blair and Williamson, 2008; Fagua and Ackerman, 2011).

The composition of visitors for Astrophytum includes a diverse group of pollinators; however, only a small number of visitors have been shown to have an effect on seed production (Huerta-Martinez, 1995). For example, Diadasia rinconis was found to be the most important pollinator of A. asterias (Blair and Williamson, 2008). Our objectives were to determine the composition and frequency of floral visitors of A. myriostigma and to classify visitor types (intra and/or extra-floral) during anthesis. The current study is important because it increases our understanding of both the floral visitors and pollination ecology of a rare cactus, as well as contributes to the general knowledge of pollination ecology of the Cactaceae.

MATERIALS AND METHODS--Species description--Astrophytum myriostigma is an endangered species (SEMARNAT, 2010), distributed in northeastern Mexico. It is a globose-columnar plant, simple or tufted 10-60 cm tall and 10-20 cm in diameter. It usually has five ribs in its stem. The flower is yellow, campanulate, 4-6 centimeters long and born at the stem apex. The flowering is asynchronous throughout the year (Bravo-Hollis and Sanchez-Mejorada, 1986). Astrophytum myriostigma is cross-pollinated like the other three species of this genus (Huerta-Martinez, 1995).

Study area description--The study was carried out in La Sierra El Sarnoso, in Gomez Palacio, Durango, Mexico. The nearest village is called "Las Palmas". According to the classification of Koppen modified by Garcia (1981), the climate is subtype BWhw (very dry and warm with summer rains). The temperature ranges from 1.6[degrees]C (in January) to 37.4[degrees]C (in June), with an annual rainfall of 200-350 mm (Muro-Perez et al., 2012). Sierra El Sarnoso has intermittent streams that are located in the lower north (Arroyo "Las Canoas" and Arroyo "El Salto"). The dominant soils on hills and slopes are litosol with regosol and yermosol in low valleys (CETENAL, 1978). The vegetation type is xerophytic scrub (Rzedowski, 1962, 1986; Gonzalez-Elizondo et al., 2007) with rosette subtype (Gonzalez-Elizondo et al. 2007). Some of the most common species are lechuguilla (Agave lechuguilla), biznaga (Coryphantha durangensis), candelilla (Euphorbia antisyphilitica), ocotillo (Fouquieria splendens), biznaga (Hamatocactus hamatocanthus), oregano (Lippia graveolens), huizachillo (Mimosa sp.), guajillo (Acacia berlandieri), limoncillo or vara resinosa (Viguiera stenoloba), nopal cegador (Opuntia rufida), cardenche (Cylindropuntia imbricata var. imbricata), tasajillo (Cylindropuntia leptocaulis var. longispinus and C. leptocaulis var. brevispinus), higuerilla silvestre (Randia pringlei), bolita dorada (Thelocactus bicolor), and palmita china (Yucca filifera).

Experimental design--Before establishing a systematic sampling grid, surveys were carried out to locate sites where the study species was locally abundant. Six 10 x 10 m permanent plots were set with stakes and cord (Harris et al., 1987). We recorded 105 plants for all six plots. Each plant was marked with a metal label and progressive numbers for database identification.

Collecting and preserving floral visitors--Prior to floral visitor collection, visits were made at two week intervals to determine asynchronous bloom times. The goal was to ensure data collection began prior to anthesis. Throughout the flowering period, all floral visitors and potential pollinators (defined based on contact with both reproductive structures, anthers and stigma) were documented between 0900 h and 1800 h (time when flowers were open).

Floral visitor collections were made using a glass jar with a screw cap. The jar was placed above the flowers to capture the organisms with as little disturbance as possible. A photographic compendium of floral visitors of A. myriostigma was developed using a digital camera (Sony Cybershot DSC-P73). Captured floral visitors were placed in a lethal chamber (Riley, 1892; Borror and White, 1970; Bland, 1978; Lorea, 2004). Once killed, the insects were separated, labeled and placed into vials with 70% alcohol. The identification was made using taxonomic keys, and field guides (Borror and White, 1970; Bland, 1978; Milne and Milne, 1980). Additional species identification was done by specialists. Each visitor was labeled with the date, plant number, plot number, collection key, picture number, frequency, visit type, color and morphotype (bee, fly, or beetle). Specimens that could not be identified (e.g. unidentified beetle) at the time of collection were identified to family to posterior identification.

Visit types--The captured insects were compared with field pictures to separate them according to the proposed classification of floral visitor type (intra and/or extra-floral). Insects that landed on the outside of the flower (tepals) and/or calyx (Te and Vc respectively) were considered extra-floral visitors. Intrafloral visitors were those that landed inside the tepals and on sexual organs of the flower. These were sub-classified into six categories: 1) Forager (F): those insects that fed on pollen without entering the nectar camera (a groove at the base of the style); 2) Nectarivore (N): those that entered the nectar camera to feed and representing specialized pollen collecting behaviors of cactus specialist bees (Schlindwein and Wittmann, 1997); 3) Forager-nectarivore (FN): those who visited the flower to feed on pollen and nectar; 4) Visitors of inner tepals (Ti): those who landed inside the tepals without feeding on pollen or nectar; 5) Florivory on stamens (Fe): those individuals that visited during the flowering process to feed on stamens; 6) Florivory on tepals (Ft): those individuals that were present during the flowering process to feed on tepals. We determined the frequency per visit type and flower visitor during floral opening hours. A visit was defined as the insect landing on some part of the flower and remaining for any length of time.

Statistical analysis--A Kruskal-Wallis test (H) was used to test for differences in floral visitor composition and frequency throughout the flowering period (Brower and Zar, 1980; Dytham, 2003; Zar, 2010), for grasshoppers species we performed a Wilcoxon Signed Rank test (W) to see the differences before and after these species visited the flowers, and a [chi square] test to test for statistical differences between the visit types that occurred with R statistical software (R Development Core Team, 2011).

Using observed frequency data of visit types, a hierarchical cluster analysis of dissimilarity (Dytham, 2003) was carried out for visitor frequency based on time of day and on time of day and plant visited, for composition, and to establish which groups were present. A Kruskal-Wallis test was used for composition and frequency and to test for differences between the times of day monitored.

RESULTS--Composition and frequency--Pollination data were collected in two synchronous blooms during the months of June 2007 and July 2008. In total, seven species of flower visitors on A. myriostigma, were observed on 10 flowering plants in summer. We found seven visitor species, three species belong to Hymenoptera (two Apidae: Ancyloscelis apiformis (Fabricius, 1793), and Diadasia olivacea (Cresson, 1878), one to Halictidae: Augochloropsis metallica (Fabricius, 1793)); two species to Diptera (Anthrax irroratus (Say, 1823) and Musca domestica L.) (families Muscidae and Bombyliidae respectively); one species to Orthoptera (Phaedrotettix sp. (Scudder, 1897), Acrididae); and one species to Coleptera (Anambodera sp., Buprestidae).

Visit types--We found that Anamboderasp. visited flowers of Astrophytum myriostigma most often (122 individuals). This species visited before flowers were fully opened and some individuals remained on the flowers after they closed. The most frequent visit type was FN, but there were also visit types N, Ti, and Te (Table 1). Hymenoptera species (visitors that have visit type N) Ancyloscelis apiformis, Diadasia olivacea and Augochloropsis metallica had more contact with the reproductive structures inside the nectar camera.

We observed to Diadasia olivacea as the most frequent nectarivorous visitor type (N) with a total of 16 individuals recorded (Table 1). These insects initially rested on the stigma and rapidly moved into the nectar camera and during the search of reward (nectar), they had contact with anthers and stigma. They then left the flower to visit another flower. These visitors flew away immediately if they encountered another visitor from the same or from a different species on a flower.

The visiting Diptera species found as floral visitors were Anthrax irroratus and Musca domestica, but both species were only occasional F type visitors (with one and two individuals respectively) (Table 1). Phaedrotettix sp. was visit type Fe and Ft. This species also was observed as a type Vc visitor, although they were observed outside the monitoring time and we observed that when this species occurred with Fe or Ft visit types, the frequency of other flower visitors decreased significantly (W = 21, P = 0.017). Phaedrotettix sp. destroys the flower so other insects do not visit it (Fig. 1).

Timing of visits was not significant (H = 13.81, n = 9, P = 0.087); however, there was a significant difference between visit types ([chi square] = 66.323, n = 7, P < 0.001). The most frequent visit type was FN, followed by N and Fe (Table 1).

[FIGURE 1 OMITTED]

Composition and frequency based on monitoring hours--The composition of A. myriostigma flower visitors varied significantly throughout the day (H = 15.835, n = 9, P = 0.045), having up to seven species visiting from 1200 h 1300 h and one species (Anambodera sp.) from 0900-1000 h.

The hierarchical dissimilarity test based in day hours and composition showed two sets of visitor species (Agglomerative coefficient = 0.51), the first comprised of Anambodera sp., Diadasia olivacea and Phaedrotettix sp. and the second by Musca domestica, Anthrax irroratus, Ancyloscelis apiformis, and Augochloropsis metallica (Fig. 2a). In the case of composition based on visited plants, we found the same two groups of visitors (Agglomerative coefficient = 0.46). In this case, Anambodera sp., Diadasia olivacea and Phaedrotettix sp. formed one group and Musca domestica, Anthrax irroratus, Ancyloscelis apiformis, and Augochloropsis metallica formed another group (Fig. 2b).

The highest visitor frequency recorded for A. myriostigma flowers was 32 individuals from 1100 h -1200 h. This number decreased in later hours to eight individuals. The variation for visitor frequency during flower opening hours was not significant (H = 5.883, df = 8, P = 0.660). However, the hierarchical dissimilarity test showed two main groups of floral visitor frequency (Agglomerative coefficient = 0.77) with Anambodera sp. forming a separate group from the other visitor species (Fig. 2c). We found three main groups of flower visitors based on day hours (Agglomerative coefficient = 0.61): one formed by Phaedrotettix sp.; the second by Ancyloscelis apiformis and Diadasia olivacea; and the last group by Augochloropsis metallica, Anthrax irroratus and Musca domestica (Fig. 2d).

Discussion--Knowledge of the composition and abundance of floral visitors is fundamental especially in communities rich in endemic species (Moran, 1961; Waser et al., 1996; Giovanetti et al., 2007). Several authors found insects to be very important pollinators in arid and temperate zones (Moldenke, 1975; Grant and Grant, 1979a; Barbour et al., 1987; Johnson, 1992; Martinez-Adriano, 2011). For cacti, pollination by bees is considered an effective mechanism to transfer pollen because bees do not require specific floral syndromes (Cota, 1993; Schlindwein and Wittmann, 1997). Weiss et al. (1994) also found bees as main visitors of some species of four climbing cacti. A study with Melocactus inortus showed that its flowers are visited mainly by three species: Anthracothorax dominicus (Antillean mango hummingbird), Apis mellifera (honey bee) and Solenopsis cf. invicta (fire ant). Another ant (Monomorium sp.) and a member of the Halictidae family were also observed visiting flowers of M. inortus (Fagua and Ackerman, 2011). Bees and beetles have also been recorded as floral visitors for Echinocereus fasciculatus, with three main groups: medium-large bees (Megachile spp. and Apis spp.); small solitary bees (Ceratina spp., Evylaeus spp. and Perdita spp.) and beetles (Carpophilus spp., Trichochrous spp., Acmaeodera spp. and Ptelon spp.). For Ferocactus wislizenii, the most abundant floral visitors were medium-sized bees: Megachile sidalceae, Lithurge echinocacti and Diadasia australis (Grant and Grant, 1979a). This last genus (Diadasia) also was a nectarivorous vistor of Astrophytum myriostigma. Grant and Connell (1979) identified beetles of the genus Carpophilus as visitors of seven Opuntia species, three Echinocereus species, and one species of Ferocactus. These findings are in agreement with the presence of beetles (Anambodera sp.) on Astrophytum myriostigma flowers.

Echinomastus erectrocentrus flowers were visited by many species of bees, mainly from the Andrenidae, Anthophoridae, Halictidae and Megachilidae (Johnson, 1992). As in our study of A. myriostigma, beetles, introduced bees, and native solitary bees including Diadasia sp. were found as floral visitors of Ariocarpus fissuratus (Martinez-Peralta and Mandujano, 2011). Other cacti for which floral visitors were recorded are: cardon (Pachycereus pringlei), saguaro (Carnegiea gigantea), and pithaya (Stenocereus thurberi). Nocturnal visitors to these cacti included moths (species not mentioned) and bats (Leptonycteris sp.), as well as Antrozous pallidus, while diurnal floral visitors included nine species of birds and Apis mellifera, an exotic bee species (Fleming et al., 1996). These last results are similar to those found for columnar cacti (Neobuxbaumia tetetzo) (Valiente-Banuet et al., 1996) with Leptonycteris curasoae and Choeronycteris mexicana as unique visitors. Bats were also found as main visitors for Pachycereus weberi and Pilosocereus chrysacanthus (Valiente-Banuet et al., 1997) and bats and moths for Agave macrocantha (Arizaga et al., 2000). Although the bishop star cactus has a columnar morphology, its floral habits and visitors were not the same as those of other columnar cacti. Some species of cacti appear to be visited mainly by insects, as in the case of A. myriostigma, whose only recorded visitors were insects. Schlindwein and Wittmann (1997) documented 41 species of insects (bees) for Opuntia brunneogemmia and 30 species for Opuntia viridirubra in Rio Grande do Sul, Brazil, and females of three of these species were the only effective pollinators: Ptilothrix fructifera (Anthophoridae), Lithurgus rufiventris (Megachilidae), and Cephalocolletes rugata (Colletidae) were pollinators of both Opuntia species. Although the collected information in this study is from two blooming events, it can be inferred that the main floral visitors for A. myriostigma in Durango, Mexico are the seven species of insects observed in this study.

[FIGURE 2 OMITTED]

Of the seven species of insects observed to visit A. myriostigma, beetles (Anambodera sp.) were most numerous. The second group, and the most important because they are the most effective pollinators for cacti (Schlindwein and Wittmann, 1997), was bees including Ancyloscelis apiformis, Augochloropsis metallica and Diadasia olivacea; the latter species also has been observed as visiting flowers of Ferocactus cylindraceus and F. wislizeni (McIntosh, 2005). Diadasia rinconis is also a floral visitor of Opuntia streptacantha (Huerta-Martinez, 1995) and the most effective pollinator of Astrophytum asterias (Blair and Williamson, 2008).

The high number of beetles and bees as floral visitors of A. myriostigma is supported by the findings of other authors studying the pollination systems of cacti (Moran, 1961; Beutelspacher, 1971; Grant and Grant, 1979b; Beutelspacher and Ramirez-Martinez, 1973; Del Castillo, 1994; Huerta-Martinez, 1995). The species Anambodera sp., Phaedrotettix sp., and D. olivacea were the most common floral visitors of A. myriostigma. However, because Diadasia spp. are some of the most effective pollinators for cacti (Grant and Grant, 1979a, 1979b; Johnson, 1992; McIntosh, 2005; Blair and Williamson, 2008), we hypothesize that D. olivacea also could be the most effective pollinator of A. myriostigma.

One important parameter in pollination systems is the visit type carried out by floral visitors. Groman and Pelmyr (1999) found that Bombus pennsylvanicus collected both nectar and pollen from Manfreda virginica, whereas B. impatiens collected only pollen (visit types FN and F, respectively). Beutelspacher (1971) observed the Megachile bee as a N type floral visitor of O. tomentosa and O. robusta: the bee holds the pistil to access to nectariferous camera (N for A. myriostigma). This behavior also has been reported by Huerta-Martinez (1995) with regards to bees visiting O. streptacantha flowers. The small pollinator beetles of the Nitidulidae family observed by Moran (1961) and the beetles that feed on pollen and tepals observed by Del Castillo (1994) and Huerta-Martinez (1995) belong to the visit types FN, Fe and Ft. A total of eight visit types were found for A. myriostigma flowers. Two extra-floral [insects that landed on the outside of the flower (tepals) and/or calyx (Te and Vc respectively)] and six intra-floral (insects that landed inside the tepals and on sexual organs of the flower): F, N, FN, Ti, Fe, Ft. They correlate with other studies on cacti mentioned before. Using this classification system, the determination of a possible syndrome of pollination for any plant species becomes easier, because it can be inferred that if the visitor makes contact with both plant reproductive structures, anthers and stigma then it could be an effective pollinator during its visits. The most common visit type to A. myriostigma was FN, although N also occurred frequently.

Timing of floral visitor activity is an important aspect of plant-animal interactions. The recorded visitors on O. tomentosa and O. robusta were mainly active between 1100 h and 1400 h (Beutelspacher, 1971). The most active hours cited for floral visitors of Ferocactus histrix were from 0800 h to 1800 h, with the highest visitor frequency occurring from 1100 h to 1300 h (Del Castillo, 1994). Huerta-Martinez (1995) recorded the highest number of Opuntia streptacantha visitors from 1000 h-1100 h and 1200 h -1300 h. These studies show similar trends as those found for A. myriostigma. Like the flowers of T. rinconensis, A. myriostigma flowers open only for one day. The largest composition and highest frequency of floral visitors occurred from 1100 h to 1300 h, similar to those of O. tomentosa, O. robusta, and F. histrix. There were more insect visits to A. myriostigma during the morning hours (before 1300 h) which is similar to results of other studies (PohlPohl, 2003). The composition of floral visitors to A. myriostigma could be segregated into two well defined groups, for frequency two groups may also be found in the cluster test (one with Anambodera sp., and other without this beetle species). Thus, this spatial-temporal segregation might help pollinators avoid competition, interference and/or resource exploitation for resources such as pollen and nectar (Wcislo et al., 2004).

Conservation and Management Implications--Species of Astrophytum are strictly outcrossing plants (Strong and Williamson, 2007). Thus, they are dependent on their pollinators to maintain viable populations. These pollinators, in turn, depend on their pollen sources for reproduction and to maintain viable populations. Cactus specialist bees, such as D. olivacea, likely depend on the occurrence of multiple species of cacti blooming throughout their foraging season to provide a continuous source of pollen for their nests, as suggested by Blair and Williamson (2008) for pollinators of A. asterias. We suggest that conservation management plans for A. myriostigma should consider including the associated species of cacti such as C. durangensis, H. hamatocanthus, C. imbricata var. imbricata, C. leptocaulis var. longispinus, C. leptocaulis var. brevispinus, O. rufida, and T bicolor because these species co-occurring with A. myriostigma with same flowering time could also share flower visitors.

We thank R. Ayala-Baiajas for help with the identification and corroboration of bee species, L. Barrientos-Lozano for the identification and corroboration of grasshopper species and N. Espino-Favela, C. Castro-Espino, G. Cardoza-Martinez and R. Gonzalez-Quidones for their valuable help in the field, and for reviewers for their comments and suggestions that helped improve this publication.

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Acceptance recommended by Associate Editor, Flo Oxley, 18 September 2014.

CRISTIAN A. MARTINEZ-ADRIANO, ULISES ROMERO-MENDEZ, JOEL FLORES *, ENRIQUE JURADO, AND EDUARDO ESTRADA-CASTILLON

Escuela Superior de Biologia-Universidad Juarez del Estado de Durango; Av. Universidad S/N Fracc. Filadelfia A.P. 146. Gomez Palacio, Durango, Mexico (CAM, URM)

Instituto Potosino de Investigacion Cientifica y Tecnologica, Division de Ciencias Ambientales. Camino a la Presa San Jose 2055. Col. Lomas 4a. Seccion, C.P. 78216. San Luis Potosi, S.L.P., Mexico (JF)

Facultad de Ciencias Forestales-Universidad Autonoma de Nuevo Leon. Carretera Nacional km 145, C.P. 67700, A.P. 41 Linares, Nuevo Leon, Mexico (EJ, EEC)

* Correspondent: joel@ipicyt.edu.mx
TABLE 1--Number of visit types to Astrophytum myriostigma flowers in
Gomez Palacio, Durango, Mexico in June 2007 and July 2008. F =
forager; N = nectarivorous; FN = foragers-nectarivore; Ti = visitors
of inner tepals; Te = visitors of outside tepals; Ft = grazing of
tepals; Fe = grazing of stamens. Vc is not included as it was
occasionally observed only outside sampling dates.

                                          Visit types

Species                    F   N    FN    Ti   Te   Fe   Ft   Total

Anambodera sp.             0    6   112   2    2     0   0    122
Anthrax irroratus          1    0     0   0    0     0   0      1
Musca domestica            2    0     0   0    0     0   0      2
Ancyloscelis apiformis     0    3     0   0    0     0   0      3
Diadasia olivacea          0   16     0   0    0     0   0     16
Augochloropsis metallica   0    2     0   0    0     0   0      2
Phaedrotettix sp.          0    0     0   0    0    13   6     19
Total                      3   31   112   2    2    13   6    165
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Author:Martinez-Adriano, Cristian A.; Romero-Mendez, Ulises; Flores, Joel; Jurado, Enrique; Estrada-Castill
Publication:Southwestern Naturalist
Article Type:Report
Geographic Code:1MEX
Date:Jun 1, 2015
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