Folia Entorno/. Mex. 42(2): 177-190 (2003)

COMMUNITY STRUCTURE OF NATIVE IN FOURVEGETATION TYPES IN THE DRY TROPICS OF YUCA TAN, MEXICO

1 1 2 LUISA F. NOVELO-RINCÓN , HUGO DELFÍN-GONZÁLEZ , RICARDO A Y ALA ANO HEZZARD H. CONTRERAS-ACOSTA1

'Universidad Autónoma de Yucatán, Facultad de Medicina Veterinaria y Zootecnia, Departamento de Zoología. A. P. 4-116 Col. Itzimná, 97100 Mérida, Yucatán, México 2 Estación de Biología Charnela, Instituto de Biología, Universidad Nacional Autónoma de México, Apartado Postal 21, San Patricio, Jalisco, 48980, Mexico

Novelo-Rincón, L.F., H. Delfin-González, R. Ayala and H.H. Contreras-Acosta. 2003. Community structure ofnative bees in four vegetation types in the dry tropics ofYucatan, Mexico. Folia Enlomo!. Mex., 42(2): 177-190.

ABSTRACT. The structure of native communities was studied in four vegetation types in the state of Yucatan, Mexico. Community structure was established using índices (dominant, common and rare ), four lifeways and unique species. A total of 5, 701 specimens were collected, falling in five families, 55 genera and 140 species. Community structure was equal, and independent ofvegetation type. On average, rare species represented 51.2% of community structure, common species 31.2% and dominant species 17.6%, while parasocials represented 50.8%, solitaries 30.1%, eusocials 9.1% and parasitic 7.5%. Results suggest that parasocial species are the most important in terms of dominance and richness and that the sampled vegetation associations are rich in social bees. This coincides with descriptions demonstrating that eusocial and Halictidae are most common and abundant. The bee communities do not differ in the size and composition of dominant, common, and rare species assemblages, or in strata composition. The bee communities differ in richness and evenness values. Differences do exist in specific composition and the number of unique species. KEY WORDS. Apoidea, , community structure, Yucatan, Mexico.

Novelo-Rincón, L. F., H. Delfin-González, R. Ayala y H. H. Contreras-Acosta. 2003. Estructura de las comunidades de abejas nativas de cuatro tipos de vegetación en el estado de Yucatán, Méxio. Folia Enlomo!. Mex., 42(2): 177-190.

RESUMEN. Se estudió la estructura de las comunidade~ de abejas nativas de cuatro tipos de vegetación en el estado de Yucatán, México. La estructura de las comunidades se estableció mediante índices (dominantes, comunes y raras), cuatro formas de vida y especies únicas. Se colectaron 5,701 ejemplares de cinco familias, 55 géneros y 140 especies. La estructura de la comunidad fue igual e independiente del tipo de vegetación; en promedio las especies raras representaron el 51.2% de la estructura de la comunidad, las comunes el 31.2% y las dominantes el 17.6%; las parasociales el 50.8%, las solitarias el 30.1 %, las eusociales el9.1% y las parásitas el 7.5%. Los resultados sugieren que en términos de dominancia y riqueza, las especies parasociales son las más importantes y que las asociaciones vegetales muestreadas son sitios ricos en abejas sociales. Nuestros resultados concuerdan con las descripciones que señalan a los Apidae eusociales y Halictidae como más comunes y abundantes. Las comu­ nidades no difieren en tamaño y composición de los ensambles de especies dominantes, comunes y raras, ni en la composición de los estratos, sólo difieren en los valores de riqueza y equidad. Las diferencias están en la composición específica y en el número de especies únicas. PALABRAS CLAVE. Apoidea, biodiversidad, estructura de la comunidad, Yucatán, México.

Bees are one ofthe taxonomically best studied 1884 species (Aya1a et al., 1993; 1996), which in groups (Michener, 2000). In Mexico, they tum represent a1most 10% of the known wor1d­ are represented by six fami1ies, 144 genera and wide richness. The importan ce of Apoidea lies in Novelo-Rincón et al. :Community structure of native bees of Yucatan, Mexico the fact that they are pollinators that ensure se­ referring to "large", "long-tongue" and "short­ xual reproduction of many flowering plants in na­ tongue" bee groups are difficult to interpret. Reports of bee fauna in Mexico. Th~ forest, SDV: Sandy dune vegetation tural communities, as well as fruit production for Study of community structure is currently one 4 forest, POF: Pine-oak forest, TF: T human consumption. Des pite being well studied, of the research areas of greatest activity within vegetation, 7 STF: Semi-evergreen tro¡ there are still a number aspects relating to bees ecology. Communities are understood as a group Seasonal flooded forest, S about which there is little information ( e.g. beha­ of populations that interact among themselves vior, natural history, biogeographical relation­ (Price, 1997). Structure can be described via spe­ S tate Vegetati ships, ecology, etc.). Future studies will provide cies diversity, interactions and trophic group ana­ Jalisco TDF, the tools to develop management and conserva­ lysis (Milis, 1994; Schowalter, 2000). Diversity Jalisco PF,OI tion strategies for threatened habitats or for ex­ has two components: species number, frequently ploitation ofsome ofthe resources these provide defined as richness; and evenness, which refers to Jalisco TDF, (Ayala et al., 1996). the way in which abundances are distributed Guanajuato TF,' among species (Ludwig and Reynolds, 1988); the Bee fauna in the Americas is richest in desert DF A' and less rich in tropical and temperate zones (Mi­ majority ofthe communities show few dominant X chener, 1979; Ayala, 1988). In temperate clima­ species and relative high numbers of common Puebla tes richness is greater than in tropical climates species (Krebs, 1989). A community is conside­ Quintana Roo STF, TSF, TDF, S and the first communities are characterized by a red complex the greater its species richness and Yucatán Un low Apoidea frequency, apparently because ofa the fewer its dominant species. A community is Yucatán Un lack of nesting sites (Heithaus, 1979; Roubik, more even when its species have similar abun­ 1989; Pascarella et al., 2000). Community rich­ dances, or more dominant when one or more spe­ ness and abundan ce in the tropics generally expe­ cies have abundances greater than other species MATERIALS AND METH( rience strong influence from highly social bees (Begon et al., 1990). The study included two locati that are active year round and polyphagous and Based on the above, a plausible hypothesis for Yucatán, the Ría Lagartos Spec generalist (in their preferences ), but whose explaining native bee community structure, in serve and Tekom (Fig. 1) (Fli contribution to species richness is relatively low. any kind of vegetation, is that the balance bet­ 1994). The overall tendency seen in descriptions oftro­ ween the assemblages ofeusocial, parasocial and The Ría Lagartos Special B pical bee assemblages is the abundance and do­ solitary bees shows constant values and defines (21 o 24' 07" and 21 o 3 7' 22" N minance of Apidae and Halictidae ( which contain community structure in terms of richness and 87° 32' 00" and 88° 14' 37" \\ many social species), and lower abundances of abundance. Given that eusocial bees are polypha­ located on the north coast of 1 , Colletidae and Andrenidae (Rou­ gous and generalist (Thorp et al., 1994 ), and pre­ mate is type BSl(h') w"I, witl bik, 1989; Wilms, 1996). In higher latitudes Me­ sent year round, they may be dominant in tropical year round (García, 1981), and gachilidae and Apidae are dominant (Pascarella landscapes and landscapes influenced by seaso­ varying between 500 and 1000 et al., 2000). Comparison is difficult, however, as nal cycles (Bullock et al., 1995). In faunistic stu­ contains eight vegetation type. available bee community descriptions are based dies of bees carried out in Mexico (Table 1), which the predominant types, on different, not necessarily comparable, criteria. community descriptions are restricted to richness study, are: "Sandy Dune Ve¡ Sorne descriptions indicate that rare species do­ values and identification ofthe most common ta­ "Tropical Deciduous Forest" ( mínate in northem forests, deciduous tropical fo­ xa. No studies ha ve been done of heterogeneity Forest" (TF). In the SDV the p rests and savannas (Heithaus, 1979; MacKay and measurements. In the present study, native bee minated by creeping plants anc Knerer, 1979); solitary bees domínate in Medite­ communities in the four dominant vegetation meters in height, while the ser rranean communities (Neffand Simpson, 1993); types in the state ofYucatan, southeast Mexico, populations of Pseudophoem and that solitary bees are more abundant and di­ are described and compared. TDF consists oftrees with an a· verse in open forest (Moldenke, 1976). Studies ging from 6-15 meters. The Tl

178 ~ of Yucatan, Mexico Folia Entorno/. Mex. 42(2) (2003)

1 ge", "long-tongue" and "short­ Table 1 ups are difficult to interpret. Reports of bee fauna in Mexico. The vegetational types are refered as the authors described it. 1 TDF: Tropical deciduous unity structure is currently one forest, SDV: Sandy dune vegetation, 2 PF: Pine forest, OF: Oak forest, POF: Pine-oak forest, 3 TDF: Tropical deciduous forest, POF: Pine-oak forest, 4 TF: Thorn forest, TDF: Tropical deciduous forest, 5 ATS: Arid tropical scrub, 6 XV: Xeric areas of greatest activity within 7 vegetation, STF: Semi-evergreen tropical forest, TSF: Tropical subdeciduous forest, TDF:. Tropical deciduous forest, SFF: ities are understood as a group Seasonal flooded forest, S: Savanna, MF: Mangrove forest, P: Peten, SDV: Sandy dune vegetatiol). hat interact among themselves cture can be described via spe- S tate Vegetational type Families Genera Species Reference eractions and trophic group ana- Jalisco TDF, SDV 1 6 87 228 Ayala, 1988 4; Schowalter, 2000). Diversity 2 nts: species number, frequently Jalisco PF, OF, POF 5 69 171 Estrada, 1992 ss; and evenness, which refers to Jalisco TDF, POF3 5 58 172 Fierros-López, 1998 eh abundances are distributed Guanajuato TF, TDF' 6 61 177 Godínez, 1991 udwig and Reynolds, 1988); the DF ATS5 5 34 97 Hinojosa, 1996 mmunities show few dominant ive high numbers of common Puebla XV6 7 69 259 Vergara and Ayala, 2002 989). A community is conside­ Quintana Roo STF, TSF, TDF, SFF. S, MF, P, SDV' 5 40 74 Roubik el al., 1990 greater its species richness and Yucatán Undet. 5 48 69 Ayalaela/., 1996 inant species. A community is 64 its species have similar abun­ Yucatán Undet. 5 Undet. Delfín el al., 1996 ominant when one or more spe- ces greater ·than other species 0). MATERIALS AND METHODS TDF and is formed of an arboreal stratum, bet­ ove, a plausible hypothesis for The study included two locations in the state of ween 3-8 meters in height and consisting mostly bee community structure, in Yucatán, the Ría Lagartos Special Biosphere Re­ of legumes, and a bush stratum dominated by tation, is that the balance bet­ serve and Tekom (Fig. 1) (Flores and Espeje!, thomy species (Flores and Espeje!, 1994 ). Te­ ages of eusocial, parasocial and 1994). k o m (20° 35' North Latitude and 88° 35' West s constant values and defines The Ría Lagartos Special Biosphere Reserve Longitude) (INEGI, 1995) is located in the ture in terms of richness and (21 o 24' 07" and 21 o 3 7' 22" N orth Latitude, and eastem portion ofthe state. The climate is Aw1, thateusocial bees are polypha­ 87° 32' 00" and 88° 14' 37" West Longitude) is with a total average annual precipitation of st (Thorp et al., 1994 ), and pre­ located on the north coast of the state. The cli­ 1158.8 mm (García, 1981). Predominant vegeta­ ey may be dominant in tropical mate is type BS1(h') w"I, with infrequent rains tion is Tropical Subdeciduous Forest (TSF), con­ dscapes influenced by seaso- year round ( García, 1981 ), and total precipitation sisting of trees with an average height of 10-20 k et al., 1995). In faunistic stu­ varying between 500 and 1000 mm. The Reserve meters, of which 50 to 7 5% of the species shed "ed out in Mexico (Table 1), contains eight vegetation types (INE, 1993), of their leaves during the annual dry season (Flores ptions are restricted to richness which the predominant types, sampled for this and Espeje!, 1994 ). The four vegetation types cation ofthe most common ta­ study, are: "Sandy Dune Vegetation" (SDV), (SDV, TDF, TF and TSF) are in a medium con­ ve been done of heterogeneity "Tropical Deciduous Forest" (TDF} and "Thom servation condition or in an evident regeneration the present study, native be e Forest" (TF). In the SDV the pioneer zone is do­ process. e four dominant vegetation minated by creeping plants and bushes up to two Collections of bees were made from Xl/94 to ofYucatan, southeast Mexico, meters in height, while the scrub zone has large X/95 at Ría Lagartos (in all places where the se­ compared. populations of Pseudophoenix sargentii. The lected type of vegetation were presents) and TDF consists oftrees with an average height ran­ from Xl/95 to X/96 at Tekom. Collections were ging from 6-15 meters. The TF is a variation of done one day a month from 06:00 to 14:00 and

179 Novelo-Rincón et al. :Community structure ofnative bees of Yucatan, Mexico

BIODIV program (natural le (Hill, 1973; Bae and Penev, 11 measures the effective numbe1 samp1e and indicates how abun1 buted among species, accoun o abundances. The series contain A NO = total number of species; N common species, equivalent to YUCATAN rithm of the Shannon-Wiener · number of dominant species eq1 Gulfof verse of the Simpson Index. Th Mexico Index indicates the diversity of: lues el ose to 1 indicate high divc QUINTANA ROO lues close to O indicating lm Shannon-Wiener Index, and the by Hutchenson were also calcu the possible differences betweer (Ludwig and Reynolds, 1988), CAMPECHE Caribbean assemblage compositions. Sea The use of indices to generat minant, common, rare) is use fu tant not to overestimate their instance, it has been observed t cies can be rare, common or dor on the number of specimens coll localities. F or this reason, and te GUATEMALA logical significance ofthe disc1 of life were also used to descr munities: solitary bees; parasiti1 bees (i. e. any gregarious beha\ or primitive social behavior); ~ FIGURA l. Sampling localities in the Yucatán state, Mexico. 1 =Ría Lagartos Reserve, 2 = Tekom. (Michener, 1974; Wilson, 197~ formation on the specific wa: 16:00 to18:00 hours with a team of5 collectors of Kansas. The systematic treatment is based on greast majority ofthe species ti in average. All the specimens were captured with the works of Ayala et al. (1996) and Michener have given each a way of life aerial nets, seeking in all possible microhabitats, (2000). All material was deposited in the Regio­ based on the known behavior o mainly flowers. Species determination was done nal Entomological Collection ofthe Universidad Unique species were identified by the authors, and when a specimen could not be Autónoma de Yucatán (CER-UADY). possible differences among con determined to the species level, "morphospecies" Diversity for each vegetation type and land­ unique species concept we use criteria were employed (Mayr and Ashlock, scape was estimated using the following method. Colwell (2000), species preser 1991 ). Determination of Halictidae were corro­ The community structure was established using cality without considering thei borated by Dr. Robert Brooks ofthe University the Hill' s numbers series calculated with the establish whether community SI

180 i f ofYucatan, Mexico Folia Entamo/. Mex. 42(2) (2003)

BIODIV program (natural logarithmic base) dent on vegetation type or has a random dis­ (Hill, 1973; Bae and Penev, 1995). This series tribution, aX2 test was done using a contingency measures the effective number of species in a table with the CHITEST computer software pro­ sample and indicates how abundances are distri­ gram (Romesburg and Marshall, 1985). 2 buted among species, accounting for relative abundances. The series contains three numbers: RESULTS NO= total number of species; N1 = number of A total of 5,701 bee specimens for five fami­ common species, equivalent to the natura1loga­ lies, 55 genera, and 140 species (73 unidentified rithm of the Shannon-Wiener Index; and N2 = morphospecies) were collected (Table 2). The number of dominant species equivalent to the in­ values for the Hill numbers, evenness and Shan­ verse ofthe Simpson Index. The Hilr s evenness non-Wiener Indexare shown in Table 3. To test lndex indicates the diversity of a community, va­ the study hypothesis, the landscape (all the sam­ lues el ose to 1 indicate high diversity, against va­ ples as a whole) was described and analyzed in ROO lues close to O indicating low diversity. The the same way as the individual vegetation types. Shannon-Wiener lndex, and the "t" test modified The relative abundance values according to the by Hutchenson were also calculated to establish categories are shown in Tables 4, 5 and 6. A the possible differences between vegetation types complete faunistic list, the relative abundances (Ludwig and Reynolds, 1988), and between the for the four vegetation types, and the lifeways for Caribbean assemblage compositions. each bee species are included in Table 7. Sea The use of índices to generate categories (do­ Significant differences were found in richness minant, common, rare) is useful, but it is impor­ and evenness values in five of the six possible tant not to overestimate their significance. For comparisons (Table 3)(p=0.05, ~able=1.64; SDV­ instan ce, it has been observed that the same spe­ TDF tcaic=O; SDV-TF tcaic=19.11; SDV-TSF cies can be rare, common or dominant depending tcaic=10.4; TDF-TFtca~c=4.83; TDF-TSFtcaic=6.64; on the number of specimens collected in different TF-TSF tcaic=10.4). The alpha diversity was localities. For this reason, and to in crease the bio­ equal, and independent of vegetation type. The logical significan ce of the discussion, four ways contingency analyses for dominant, rare and of life were also used to describe the bee com­ common species distribution (X2 = 4.53, p = munities: solitary bees; parasitic bees; parasocial 0.95), and for solitary, parasitic, parasocial and bees (i. e. any gregarious behavior, shared nests social species (X2 = 12.87, p = 0.16) showed no or primitive social behavior); and eusocial bees differences. (Michener, 1974; Wilson, 1979). There is no in­ SDV community. Consisting of 64 species formation on the specific ways of life of the (Table 2), this community has few dominant spe­ tematic treatment is based on greast majority ofthe species that we found. We cies (38-378 individuals), one ofwhich is euso­ a et al. (1996) and Michener have given each a way of life for our purposes cial (Nannotrigona peri/ampoides, Agapostemon was deposited in the Regio­ based on the known behavior of related species. nasutus, Augoch/ore//a pomonie//a, Xylocopa Collection ofthe Universidad Unique species were identified to emphasize the mexicanorum, Centris inermis, Megachi/e denti­ tán (CER-UADY). possible differences among communities. Forthe pes, Ceratina sp 4, Ceratina aff. capitosa, Eu/ae­ h vegetation type and land­ unique species concept we use the definition of ma polychroma and Centris trigonoides ). Andre­ using the following method. Colwell (2000), species present only in one lo­ nidae was not recorded. The rare species (1-3 in­ cture was established using cality without considering their abundance. To dividuals) were predominantly parasocial, and series calculated with the establish whether community structure is depen- the common species ( 4-31 individuals) were

181 Novelo-Rincón et al. :Community structure ofnative bees of Yucatan, Mexico

Table 2 Species and abundance for families ofnative bees in four vegetation types in Yucatan state, Mexico. SDV = Sandy dune Hill's numbers and Shannon-Wiener' vegetation, TDF = Tropical deciduous forest, TF = Thorn forest, TSF = Tropical subdeciduous forest. Mexico. SDV = Sandy dune vegetati1

SDV TDF TF TSF Landscape Index

FAMILY Spp Abund. Spp Abund. Spp Abund. Spp Abund. Spp Abund. NO (Richness) NI (Common species) Andrenidae 2 3 26 5 144 5 173 N2 (Dominant species) Apidae 27 924 32 929 29 670 49 915 59 3438 Rare species Colletidae 3 20 4 13 2 22 6 44 7 99 Evenness o Shannon-W iener Halictidae 17 581 21 248 22 238 19 162 30 1229

Megachilidae 17 176 12 59 25 330 25 197 39 762 TOTAL 64 1701 71 1252 78 1286 104 1462 140 5701 this community has a greater m and rare (4-20 individuals) (Table 6). This is also the ve mainly eusocial (Table 4). The unique species fuscipennis) (Table 3). The eusocial species are which unique species represen1 represented 9.4% ofthe total, the majority being an important portion ofthe dominant species (26- tion (28.8%), most being rare ~ rare and parasocial (66.7%) (Table 6). 21 O individuals) (Table 4 ), and the parasocial sitie species. This is the only TDF community. Consisting of 71 species bees form the majority of the rare (1-4 indivi­ dominant species (Pseudopam (Table 2), this community has very few dominant duals) and common species (5-24 individuals). Trigonisca pipioli, Paratetrap species (23-250 individuals), five of which are This is the only case in which a eusocial species Diadasia olivacea) (Table 6). eusocial (Agapostemon nasutus, Augochlora ni­ (Plebeiafrontalis) was rare. The unique species, Landscape community. Com grocyanea, Centris trigonoides, Centris analis, al! rare, represented 6.4% ofthe total (Table 6). cies (Table 2), the richness is 1< Euglossa viridissima, Megachile sp 17, Nanno­ TSF community. Consisting of 104 species This community has the highc trigona perilampoides, Pereirapis caucasica, (Table 2), this community has the highest rich­ shows a community with a low Pseudaugochloropsis gramínea, Scaptotrigona ness. Its evenness shows a community wifh many minants (Agapostemon nasutw pectoralis, Trigona nigra nigra, Trigona fulvi­ dominant species and less elevated abundan ces grocyanea, Augochlora sp 4 ventris and Trigonafuscipennis) (Table 4). The than in other vegetation types (Table 3 ). Seven of rare species are mainly parasocial and solitary the dominant species are eusocial (Ancyloscelis and the common species are mostly parasocial. apiformis, Augochlora nigrocyanea, Augochlora Native bee communities composition ir sp4, Centris trigonoides, Cephalotrigonazexme­ = Tropical deciduous forest, TF = Tho Unique species represent only 7% of the total, species, R = Rare species, T =Total. and al! ofthem are rare (Table 4). niae, Ceratina sp 1, Diadasia olivacea, Euglossa TF community. Consisting of78 species, and viridissima, Eulaema polychroma, Exomalopsis SDV with one ofthe lowest abundances (Table 2), this sp 3, Hypanthidium yucatanicum, Megachile sp D R e T % community has few dominant species (Augo­ 3, Megachile sp 7, Megachile sp 11, Paratetra­ Solitary 9 18 28.1 chlora sp 4, Centris trigonoides, Centris analis, pedia moesta, Partamona bilineata, Plebeia Parasite o o 3.1 Cephalotrigona zexmeniae, Euglossa viridissi­ frontalis, Pseudopanurgus crenulatus, Pseudo­ Parasocial 18 12 38 59.4 ma, Heterosarus sp, Lasioglossum sp 5, Mega­ panurgus mexicanus, Scaptotrigona pectoralis, Eusocial 9.4 chile sp 17, Megachile chichimeca, Megachile Trigona nigra nigra, Trigona fulviventris and Undet. dentipes, Scaptotrigona pectoralis, Trigona ni­ Trigonisca pipioli) (21-184 individuals) (Table TOTAL 10 29 25 64 gra nigra, Trigona fulviventris and Trigona 4 ). The rare species are mainly parasocial, though % 15. 45. 39. 100

182 i 1 pf Yucatan, Mexico Folia Entamo/. Mex. 42(2) (2003)

1 Table 3 state, Mexico. SDV = Sandy dune Hill's numbers and Shannon-Wiener's index diversity ofnative bees communities in four vegetation types in Yucatán state, ical subdeciduous forest. Mexico. SDV = Sandy dune vegetation, TDF = Tropical deciduous forest, TF = Thom forest, TSF = Tropical subdeciduous forest.

TSF Landscape lndex SDV TDF TF TSF Landscape pp Abund. Spp Abund. NO (Richness) 64 71 78 104 140 NI (eommon species) 23.6 23.6 24.9 39.7 31.9 5 144 5 173 N2 (Dominan! species) 10.5 12.6 13.4 23.2 20.3 49 915 59 3438 Rare species 30 34 40 31 87.8 6 44 7 99 Evii:nness 0.444 0.532 0.537 0.584 0.634 Shannon-W iener 3.16 3.16 3.21 3.68 3.46 19 162 30 1229

25 197 39 762 04 1462 140 5701 this community has a greater number of common pomoniella, Centris inermis, Centris trigonoides, and rare ( 4-20 individuals) parasitic species Centris ana/is, Cephalotrigonazexmeniae, Cera: (Table 6). This is also the vegetation type in tina sp 1, Euglossa viridissima, Lasioglossum sp 3). The eusocial species are which unique species represent the highest frac­ 5, Megachile chichimeca, Megachile dentipes, ofthe dominant species (26- tion (28.8%), most being rare solitary and para­ Nannotrigona perilampoides, Pseudopanurgus able 4), and the parasocial sitie species. This is the only case with unique mexicanus, Scaptotrigona pectoralis, Trigona ni­ rity of the rare (1-4 indivi- dominant species (Pseudopanurgus mexicanus, gra nigra, Trigona fulviventris, Trigona fusci­ species ( 5-24 individuals). Trigonisca pipio/i, Paratetrapedia moesta and pennis and Xylocopa mexicanorum). As in the in which a eusocial species Diadasia olivacea) (Table 6). SDV, the number of dominant (86-472 indivi­ as rare. The unique species, Landscape community. Consisting of 140 spe­ duals) eusocial species is low (Table 4). The 6.4% ofthe total (Table 6). cies (Table 2), the richness is lower at this scale. majority of rare species (1-20 individuals) is in • Consisting of 104 species This community has the highest evenness and the parasocials, and the largest proportion of unity has the highest rich­ shows a community with a low proportion of do­ common species (23-82 individuals) is in the ows a community wifh many minants (Agapostemon nasutus, Augoch/ora ni­ solitaries (Table 5). d less _elevated abundances grocyanea, Augochlora sp 4, Augochlorel/a ion types (Table 3). Seven of s are eusocial (Ancyloscelis Table 4 ranigrocyanea, Augochlora Native bee communities composition in four vegetation types in Yucatán state, Mexico. SDV = Sandy dune vegetation, TDF ides, Cephalotrigona zexme­ = Tropical deciduous forest, TF = Thom forest, TSF = Tropical subdeciduous forest, e = eommon species, D = Dominant species, R = Rare species, T =Total. Diadasia olivacea, Euglossa a po/ychroma, Exoma/opsis SDV TDF TF TSF yucatanicum, Megachile sp D R e T % D R e T % D R e T % D R e T % egachi/e sp ll, Paratetra- Solitary 9 18 28.1 15 4 20 28.2 4 12 6 22 28.2 7 13 14 34 32.7 amona bi/ineata, Plebeia Parasite o 2 o 2 3.1 o o 1.4 o 4 6 7.7 o 9 4 13 12.5 urgus crenu/atus, Pseudo­ Parasocial 18 12 38 59.4 19 12 38 53.5 23 14 42 53.8 7 20 17 44 42.3 ' Scaptotrigona pectoralis, Eusocia1 6 9.4 o 11.3 8 10.3 o "8 7.7 a, Trigona fu/viventris and Undet. 4 4 5.6 4.8 21-184 individuals) (Table TOTAL 10 29 25 64 13 39 19 71 14 40 24 78 23 44 37 104 e mainly parasocial, though % 15. 45. 39. lOO 18. 54. 26. lOO 17. 51. 30.8 100 22. 42. 35. 100

183 Novelo-Rincón et al.:Community structure ofnative bees ofYucatan, Mexico

DISCUSSION 7.1% of total species. These results suggest that Parasocial bee species forme< The 140 species identified in this study repre­ in terms of dominance and richness, parasocial tion ofthe dominant species, th< sent 7.5% of Mexican species and demonstrate species are the most important, and that the sam­ of parasocial species were rar~ Yucatán to be a place of medium richness in pled vegetation associations are sites rich in so­ the parasocial species Euglosst comparison to other studied sites in Mexico cial bees. Centris trigonoides were domii (Table 1). Based on the authors' unpublished da­ These results agree with descriptions that show getation associations; Augochh ta, the collected species account for 10% ofMe­ that eusocial Apidae and Halictidae (parasocial) Centris analis and Agapostem xican fauna. lt should be taken into account that are most abundant and that Megachilidae, Colle­ dominant in three vegetation t) know1edge of bees in Mexico is stilllimited. tidae and Andrenidae (solitary families) are least and landscape); and Lasioglos; abundant(Roubik, 1989; Wi1ms, 1996). They are eh/ore/la pomonie/la, Centris iJ Table 5 also similar to descriptions showing rare species polychroma, and Xylocopa me Native bee communities composition in landscape in to predominate in northem forests, tropical de­ dominant in two vegetation ty): Yucatán state, Mexico. e= eommon species, D = ciduous forests and savannas (Heithaus, 1979; leve!, 19 parasocial species wen Dominan! species, R = Rare species, T = Total. MacKay and Knerer, 1979). The results contrast, tributed in al! the vegetation ass' were found in three vegetation ~ Landscape however, with those of Moldenke (1976) which in most cases). These variabl' D R e T % indicate that solitary species are more di verse and abundant in open forests, and with those of Pas­ Solitary 3 30 14 47 33.6 carella et al. (2000), which show Megachilidae Parasite o 12 13 9.3 and Apidae to be dominant. Unique species ofnative bee communit Parasocial 11 40 12 63 45.0 TDF = Tropical deciduous forest, T By combining both community description cri­ Eusocial 6 o 4 10 7.1 D teria, sorne characteristic pattems can be descri­ Undet. 5 2 7 5.0 bed for these native bee communities. In no ins­ SDV TOTAL 20 87 33 140 tance were the dominant eusocial species more % 14.3 62.1 23.6 100 than the dominant parasocial species. In almost D R e al! the cases, however, the eusocials were Solitary common, with only Plebeiafrontalis being rare Parasite o o Among the four vegetation types, bee commu­ (TF), despite its presence in two contiguous ve­ Parasocial nity structure was equal, and independent of, getation types. Four social species (Nannotrigona associated vegetation type. In other words, the perilampoides, Scaptotrigona pectoralis, Trigo­ Eusocial average number of rare species represented na nigra nigra and Trigona fulviventris) were Undet. 51.2% of the communities, the common species common in al! vegetation types, and three species TOTAL 4 2 31.2%, and the dominants 17 .6%. The parasocial (Melipona beecheii, Cepha/otrigona zexmeniae species represented 50.8% of the communities, and Trigonafuscipennis) were common to three contiguous vegetation types. The only exceptions the solitary species 30.1 %, the eusocials 9.1 %, The majority ofthe parasitic s¡ to this pattem were Partamona bilineata, which and the parasitics 7.5%. None were dominant in any o1 was not found in contiguous vegetation types, With the exception ofthe SDV, the evaluated communities, and only three co and Trigonisca pipioli, found only in TSF. Thus sites had high eusocial Apidae frequency, a clear STF and Landscape) had comm< contrast with the low frequencies reported by it can be said that in terms of biodiversity, eu­ cies. social bees are dominant or common in tropical Heithaus ( 1979) and Roubik ( 1989). Ten eusocial If the vegetation communities landscapes, probably because they are poly­ species were identified at the landscape leve!, the size. and composition of 1 phagous, generalist (in pollen preferences) and which represent 21.73% ofthe eusocial species common, and rare species asserr non-seasonal. reported in Mexico (Ayala et al., 1996), and feway strata (solitary, parasoci

184 of Yucatan, Mexico Folia Entamo/. Mex. 42(2) (2003)

These results suggest that Parasocial bee species formed the largest frac­ allow a small group to be established as do­ and richness, parasocial tion ofthe dominant species, though the majority minant. important, and that the sam­ of parasocial species were rare or common. Of Among the solitary species only Megachile llssociati

bee communities. In no ins- SDV TDF TF TSF

D R e Tot D R e Tot D R e Tot D R e Tot

Solitary 2 2 2 2 2 6 6 13 Parasite o o o o o o 5 3 8 am~"~"""~" in two contiguous ve­ Parasocial 3 4 2 2 o 5 species (Nannotrigona .-nnm•rrH7nn·npectoralis, Trigo­ Eusocial o o o Trigona fulviventris) were Undet. 2 2 2 3 ...,, .... ~mtypes, and three species TOTAL 4 2 6 5 5 5 5 4 17 9 30 Cephalotrigona zexmeniae •n••nnl.< were common to three types. The only exceptions The majority ofthe parasitic species were rare. species) composition, then the only differences Partamona bilineata, which None were dominant in any of the vegetation that can be found are in the number of species, contiguous vegetation types, communities, and only three communities (TF, their abundan ces and the number of unique spe­ found only in TSF. Thus STF and Landscape) had common parasitic spe­ cies. Detailed differences can be found analyzing in terms of biodiversity, eu­ cies. the specific composition in each one of the ve­ a»m.inwnt or common in tropical If the vegetation communities do not differ in getation types. In almost all the cases, com­ because they are poly­ the size and composition of their dominant, munities do not differ in diversity values (rich­ (in pollen preferences) and common·, and rare species assemblages, or in li­ ness and abundance ); only in the comparison of feway strata (solitary, parasocial and eusocial SDV and TDF are those differences. All, or the

185 Novelo-Rincón et al.:Community structure ofnative bees ofYucatan, Mexico majority, ofthe unique species in SDV, TDF, and Apoidea (), pp. 423-464. In: J. Llorente­ México. Bousquets, A. N. García-Aidrete andE. González-Soriano TF are rare and represent a small portion of the KREBS, C. 1989. Ecological methodolo (Eds), Biodiversidad, taxonomía y biogeografia de Publishers, New York, USA, 654 pp. species in the communities (9.3% in SDV, 7.0% artrópodos de México: Hacia una síntesis de su LUDWIG, J. A. ANDJ. f. REYNOLDS. 1988 in TDF and 6.4% in TF). For TSF, in contrast, conocimiento. UNAM, CONABIO, México. A primer on methods and computing, J unique species represent 28.8% of the species BAEV, P. AND L. PENEV. 1995. BIODIV: program for New York, USA, 337 pp. calculating biological diversity parameters, similarity, niche and include four dominant species (Diadasia MACKAY, P. A. AND G. KNERER. 1979., overlap and cluster analysis. PENSOFT, Sofia, Moscow. and abundance in a community of wi olivacea, Paratetrapedia moesta, Pseudopanur­ BEGON, M.,J. L.HARPERANDC. R. TOWSEND. 1990. Ecology field habitat in Southern Ontario. Can gus mexicanus and Trigonisca pipioli). Individuals, populations and communities. Blackwell, Mass. 111:367-376. The unique species for SDV are Centris labia­ USA, 945 pp. MAYR,E.ANDP. D. ASHLOCK. 1991. Pri, BULLOCK, S H., H. A. MOONEY ANDE. MEDINA (Eds). 1995. fa, Colletes sp 6, Exomalopsis sp 6, Lasio­ zoology. McGraw-Hill, New York, m Seasonally dry tropzca/ forest. Cambridge, London, UK, MICHENER, C. D. 1974. The social be) glossum sp 9, Megachile sp 1O and Mesoplia 450 pp. Belknap Press. Cambridge, Mass., US regalis. For TDF they are Centrisfuscata, Mega­ COLWELL, R. K. 2000. User's guide to estimate. Statistical MICHENER, C. D. 1979. Biogeography ol estimation of species richness and shared species for chile texensis, Megachile sp 23, Melissoptila sp the Missouri Botanical Garden, 66:27 samples Version 6 Ob1 MICHENER, C. D. 2000. The bees oj th and Paratetrapedia sp 2. For TF they are Halic­ DELFIN, 0 H., R. AYALA B H H CONTRERAS A C Hopkins University Press, Baltimore, 1 tus hesperus, Anthidiellum af!. apicale, Antho­ ECHAZARRETA 0. AND J. QUEZADA. 1996. Listado MILLS, N. J. 1994. Parasitoid Guilds: De dioctes agnathum, Coelioxys sp 1 and Xylocopa preliminar de géneros de Apoidea (Hymenoptera) para el of the Parasitoid Communities of E Estado de Yucatán, México. VI Congreso Latinoamericano micheneri. Finally, for STF they are Augochlora Hosts. Environmental Entomology, 23 y XXXI Congreso Nacional de Entomología, Sociedad MOLDENKE, A. R. 1976. California poi sp 7, Augochloropsis sp 7, Calliopsis hondura­ Mexicana de Entomología, México, pp. 169. vegetation types. Phytologia, 34:304-3 sica, Centris (Trachina) sp, Ceratina spp 9, 10 ESTRADA, C. M. 1992. Abejas silvestres (Hymenoptera: NEFF, J. L. AND B. B. S!MPSON. 199: and 11, Coelioxoides punctipennis, Coelioxoides Apoidea) de la Sierra del Tigre, Jalisco, Tesis de systems and plant diversity, pp. 143-1• Licenciatura en Biología, Facultad de Ciencias Biológicas, sp 6, Colletes spp 2 and 5, Epeolus sp, Exaerete and J. D. Gauld (Eds ), Hymenoptera ano Universidad de Guadalajara, México. Jnternational, Wallingiord, UK. smaragdina, condignus, Lasioglossum FIERROS-LÓPEZ, H. E. 1998. Abejas silvestres (Hymenoptera: PASCARELLA, J. B., K. D. WADDINGTO sp 1O, Megachile sp B, Megachile otomita, Me­ Apoidea) del Volcán de Tequila, Jalisco, México. Folia 2000. The bee fauna (Hymenoptera: Ap gachile totonaca, Megachile spp 4, 6 and 19, Entomológica Mexicana, 102:21-70. National Park, Florida and adjacent FLORES, J. S. AND l. ESPEJEL. 1994. Tipos de vegetación de la Monoeca mexicana, Protandrena sp, Triepeolus phenology and biogeography. Jo Península de Yucatán. Etnoflora Yucatanense. UADY, Entomological Society, 72:32-45. sp and Xylocopa muscaria. Mérida, México, Fase., 10, 135 pp. PRICE, P. W. 1997. lnsect ecology. John GARCÍA, E. 1981. Modificaciones al Sistema de Clasificación York, USA, 874 pp. de Koppen. UNAM, México, 217 pp. ACKNOWLEDGEMENTS GODÍNEZ, G. L. M. 1991. Algunos aspectos de la fenología de We wou1d 1ike to thank Peter Feinsinger and abejas silvestres (Hymenoptera: Apoidea) de San Gregario, Virginia Me1endez for their comments on this Guanajuato, Tesis de Licenciatura en Biología, Facultad de manuscript. This research was financed by Ciencias, UNAM, México. HEITHAUS, R. ·1979. Community structure of neotropical CONABIO under grant B004 administrated by S pecific abundan ce of native bees in tlower visiting bees and wasps: Diversity and phenology. Tropical deciduous forest, TF = Thorr Carlos Echazarreta G. Ecology, 60: 190-202. . Paras HINOJOSA, D. J. A. 1996. Estudio faunístico de las abejas LITERA TURE CITED silvestres (Hymenoptera: Apoidea) del Pedregal de San LS FAMILY SPECU Angel, D.F., Tesis de Licenciatura en Biología, Facultad de Ay ALA, B. R. 1988. Abejas silvestres (Hymenoptera: PS Halictidae Agapo Ciencias. UNAM, México. Apoidea) de Charnela, Jalisco, México. Folia Enlomo lógica so Apidae Ancylc HILL, M. O. 1973. Diversity and evenness. A unif)'ing notation Megachilidae Anthia Mexicana, 77:395-493. and its consequences. Ecology, 54:427-432. so AY ALA, B. R., L. T. ÜRISWOLD AND S. H. BULLOCK. 1993. Megachilidae Anthoo INE (Instituto Nacional de Ecología). 1993. Programa de ma­ so The native bees of Mexico, pp. 179-227. In: T. P. nejo de la Reserva Especial de la Biosfera de Ría Lagartos, so Megachilidae Antho. Ramamoorthy, R. Bye, A. Lot and J. Fa (Eds), Biological Yucatán, México. Secretaría de Desarrollo Social, México. so Megachilidae Ashme diversity oj Mexico: origin and distribution. Oxford INEGI. 1995. Valladolid, Estado de Yucatán, Cuaderno PS Halictidae Augoc University Press, New York. Estadístico Municipal, Gobierno del Estado de Yucatán, PS Halictidae Augoc AYALA, B. R., L. T. ÜRISWOLD AND D. YANEGA. 1996.

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pp. 423-464. In: J. Llorente­ México. ROMESBURG, C. H. AND K. MARSHALL. 1985. CHITEST: A Cia·-A.Iorere and E. González-Soriano KREBS, C. 1989. Ecological methodology. Harper Collins Montecarlo Computer program for contingency tables. taxonomía y biogeografia de Publishers, New York, USA, 654 pp. Computer and Geoscience, 11:67-78. · Hacia una síntesis de su LUDWIG, J. A ANDJ. F. REYNOLDS. 1988. Statistica/ eco/ogy. ROUBIK, D. W: 1989. Eco/ogy and natural history of the CONABIO, México. A primer on methods and computing, John Wiley and Sons, tropical bees. Cambridge University Press, New York, 1995. BIODIV program for New York, USA, 337 pp. USA, 514 pp. parameters, similarity, niche MACKA Y, P A AND G. KNERER. 1979. Seasonal occurrence ROUBIK, D. W., R. VILLANUEVA, E. F. CABRERA-CANO AND PENSOFT, Sofía, Moscow. and abundance in a community of wild bees from an old W. COLLÍ-UCÁN. 1990. Abejas nativas de la Reserva de .,,, Ar<~H .R. TOWSEND. 1990. Eco/ogy. field habita! in Southern Ontario. Canadian Entomologist, Sian Ka'an, Quintana Roo, México, pp. 317-320. In: D. and communities. Blackwell, Mass. 111:367-376. Navarro and G. Robinson (Eds), Biodiversidad Biológica en MA YR, E. AND P. D. ASHLOCK. 1991. Principies ofsystematic la Reserva de la Biosfera de Sian Ka'an, Quintana Roo, MOONEY ANDE. MEDINA (Eds). 1995. ¡oology. McGraw-Hill, New York, USA, 475 pp México. CIQRO, Chetuma1, México. forest. Cambridge, London, UK, MICHENER, C. D. 1974. The social behavior of bees. The SCHOWALTER, T. D. 2000. Insect ecology. An ecosystem Belknap Press. Cambridge, Mass., USA, 404 pp. approach. Academic Press, San Diego, USA, 483 pp. User's guide to estímate. Statistical MICHENER, C. D. 1979. Biogeography of the bees. Anna/s of THORP, R. W., A M. WENNER AND J. F. BARTHELL. 1994. richness and shared species for the Missouri Botanical Garden, 66:277-347. Flowers visited by honey bees and native bees on Santa MICHENER, C. D. 2000. The bees of the world. The Johns Cruz 1sland, pp. 351-365. In: W. L. Halvorson and G. J. ALA B., H. H. CONTRERAS A, C. Hopkins University Press, Baltimore, USA, 913 pp. Maender (Eds), The Fourth California lslands Symposium AND J. QUEZADA. 1996. Listado MILLS, N. J. 1994. Parasitoid Guilds: Defining the Structure Update on the status of resources. de Apoidea (Hymenoptera) para el of the Parasitoid Communities of Endopterygote lnsect VERGARA, C. H. AND R. AY ALA. 2002. Diversity, phenology, México. VI Congreso Latinoamericano Hosts. Environmental Entomology, 23: 1066-1083. and biogeography of bees (Hymenoptera: Apoidea) of Nacional de Entomología, Sociedad MOLDENKE, A R. 1976. California pollinator ecology and Zapotitlán de las Salinas, Puebla, Mexico. Journal of the México, pp. 169. vegetation types. Phyto/ogia, 34:304-361. K ansas Entomological Society, 75( 1): 16-30. silvestres (Hymenoptera: NEFF, J. L. AND B. B. SIMPSON. 1993. Bees, pollination WILMS, W. 1996. The highly eusocial bees of Boracéia: del Tigre, Jalisco, Tesis de systems and plant diversity, pp. 143-169. In: J. LaSalle, J. Community structure, resource partitioning, and their role as Facultad de Ciencias Biológicas, and l. D. Gauld (Eds ), Hymenoptera and biodiversity. CAB­ pollinators. Anais do Encontro Sobre Abe/has, Riverao .,.,.,.... México. lnternational, Wallingiord, UK. Preto, SP, Brasil, 2: 196-203. 1998. Abejas silvestres (Hymenoptera: PASCARELLA, J. B., K. D. WADDINGTON AND P. R. NEAL. WILSON, E. O. 1979. The insect societies. Belknap Press, de Tequila, Jalisco, México. Folia 2000. The bee fauna (Hymenoptera: Apoidea) ofEverglades Harvard, USA, 548 pp. 102:21-70. National Park, Florida and adjacent areas: Distribution, 1994. Tipos de vegetación de la phenology and biogeography. Journal of Kansas Etnoflora Yucatanense. UADY, Entomo/ogical Society, 72:32-45. 10, 135 pp. PRICE, P. W. 1997. Insect eco/ogy. John Wiley & Sons, New Recibido: 12 noviembre 2002. idificGrcio,nes al Sistema de e /a¡;ificación York, USA, 874 pp. Aceptado:14 mayo 2003. 217 pp. Algunos aspectos de la fenología de lvnnenoot1era: Apoidea) de San Gregario, APPENDIX Lic:em:iatura en Biología, Facultad de Table 7 Specific abundance ofnative bees in four vegetation types in Yucatán, Mexico. SOY= Sandy dune vegetation; TDF = Tropical deciduous forest, TF = Thorn forest, TSF =Tropical subdeciduous forest, LS = L1fe style, ES= Eusocial, PA = Parasite, PS = Parasocial, SO = Solitary, ? = Unknown. Estudio faunístico de las abejas · Apoidea) del Pedregal de San LS FAMILY SPECIES SDV TDF TF TSF TOT en Biología, Facultad de PS Halictidae Agapostemon nasutus 326 30 357 Apidae Ancyiosce/is apiformis 4 33 37 and evenness. A unifying notation so Megachilidae Anthidiellum a.ff. apicale Ecology, 54:427-432. so Megachilidae Anthodioctes (Anthodioctes) agnathum 1 de Ecología). 1993. Programa de ma- so Anthodioctes (Nananthidium) gualanense la Biosfera de Ría Lagartos, so Megachilidae 6 24 30 de Desarrollo Social, México. so Megachilidae Ashmeadiella sp nov 6 3 9 Estado de Yucatán, Cuaderno PS Halictidae Augochlora nigrocyanea 19 53 14 32 118 Gobierno del Estado de Yucatán, PS Halictidae Augoch/ora sp 2 1 JI 12

187 Novelo-Rincón et al.:Community structure ofnative bees ofYucatan, Mexico

Table 7. Continue ... Table 7. Continue ... LS FAMILY SPE LS FAMILY SPECIES SDV TDF TF TSF TOT Apidae Dia PS Halictidae Augoch/ora sp 3 2 PA Megachilidae Do1 PS Halictidae Augochlora sp 4 6 22 46 40 114 PA Apidae Epé PS Halictidae Augochlora sp 5 8 3 1 10 22 PS Apidae Epi PS Halictidae Augochlora sp 6 9 8 3 20 PS Apidae Eu~ PS Halictidae Augoch/ora sp 7 3 3 PS Apidae Eu/, PS Halictidae Augoch/orella pomoniel/a 158 19 21 7 205 PA Apidae Exa PS Halictidae Augoch/oropsis metal/ica 3 20 23 PS Apidae Exo PS Halictidae Augoch/oropsis sp 2 3 5 PS Apidae Ex o PS Halictidae Augochloropsis sp 3 5 6 PS Apidae Ex o PS Halictidae Augochloropsis sp 4 4 4 8 PS Apidae Ex o PS Halictidae Augochloropsis sp 5 1 1 2 Apidae FIOJ PS Halictidae Augoch/oropsis sp 6 3 4 6 13 PS Halictidae Ha/ PS Halictidae Augochloropsis sp 7 3 3 PS Halictidae Ha/ so Andrenidae Cal/iopsis (Cal/iopsima) hondurasica 1 so Megachilidae Her PS Apidae Centris (Centris) inermis 81 2 3 86 so Andrenidae Het, PS Apidae Centris (Hemisiel/a) nitida 10 9 5 25 so Colletidae Hy/, PS Apidae Centris (Hemisiel/a) sp 1 2 3 5 so Colletidae Hy/, PS Apidae Centris (Hemisiel/a) trigonoides 38 25 64 23 150 so Megachilidae Hyp PS Apidae Centris (Heterocentris) analis 4 43 26 18 91 PS Halictidae Lasi PS Apidae Centris (Heterocentris) sp nov 11 12 PS Halictidae Las¡ PS Apidae Centris (Frachina) sp 2 2 PS Halictidae Las1 PS Apidae Centris (Frachina) fitscata 4 4 PS Halictidae Las¡ PS Apidae Centris (Frachina) labia/a 1 PS Halictidae Las1 ES Apidae Cephalotrigona zexmeniae 6 26 66 98 PS Halictidae Las1 PS Apidae Ceratina aff. capilosa 47 13 5 17 82 PS Halictidae Las1 PS Apidae Ceratina sp 1 27 10 17 46 100 PS Halictidae Lasi PS Apidae Ceratina sp 2 1 2 3 6 PS Halictidae Lasi PS Apidae Ceratina sp 4 58 2 1 3 64 PS Halictidae Lasi PS Apidae Ceratina sp 6 3 6 9 so Megachilidae Lithl PS Apidae Ceratma sp 9 9 9 so Megachilidae Meg PS Apidae eeralina sp 10 3 3 so Megachilidae Meg PS Apidae Ceralina sp 11 5 5 so Megachilidae Meg PA Apidae Coe/ioxoides punctipennis so Megachilidae Meg PA Megachilidae Coe/ioxys (Acrocoe/ioxys) azteca 8 4 13 so Megachilidae Meg PA Megachilidae Coe/ioxys (Neocoe/ioxys) aff. assumptionis 2 3 so Megachilidae Meg, PA Megachilidae Coelioxys sp 1 2 2 so Megachilidae Meg, PA Megachilidae Coe/ioxys sp 2 1 2 2 5 so Megachilidae Meg, PA Megachilidae Coe/ioxys sp 3 2 12 14 so Megachilidae Meg, PA Megachilidae Coelioxys sp 4 2 2 so Megachilidae Meg, PA Megachilidae Coelioxys sp 6 so Megachilidae Meg, so Colletidae Col/etes sp 1 6 17 23 so Megachilidae Meg, so Colletidae Col/eles sp 2 8 8 so Megachilidae Meg< so Colletidae Col/eles sp 5 2 2 so Megachilidae Meg< so Colletidae Col/e tes SQ 6 18 18 so Megachilidae Meg_<

188 Folia Entamo!. Mex. 42(2) (2003)

Table 7. Continue ...

LS FAMILY SPECIES SOY TDF TF TSF TOT

? Apidae Diadasia olivacea 22 22 1 2 PA Megachilidae Dolichostelis costalis 3 3 6 6 22 46 40 114 PA Apidae Epeolus sp 8 3 1 10 22 PS Apidae (Epichara) elegans 2 13 15 9 8 3 20 PS Apidae Euglossa (Euglossa) viridissima 31 28 38 26 123 3 3 PS Apidae Eulaema (Apeulaema) po/ychroma 39 2 9 22 72 !58 19 21 7 205 PA Apidae Exaerete smaragdina 1 1 3 20 23 PS Apidae Exomalopsis sp 2 2 7 3 3 15 3 5 PS Apidae Exomalopsis sp 3 1 23 25 1 5 6 PS Apidae Exomalopsis sp 4 3 3 17 23 4 4 8 PS Apidae Exomalopsis sp 6 2 2 1 1 2 ? Apidae Flori/egus condignus 2 2 3 4 6 13 PS Halictidae Halictus (Halictus) ligatus 3 1 6 3 3 PS Halictidae Halictus (Seladonia) hesperus 4 4 1 1 so Megachilidae Heriades sp 11 7 4 23 81 2 3 86 so Andrenidae Heterosarus sp 1 26 2 29 1 lO 9 5 25 so Colletidae Hylaeus sp 1 4 21 10 36 2 3 5 so Colletidae Hylaeus sp 4 2 5 7 8 25 64 23 150 so Megachilidae Hypanthidium yucatanicum 5 21 26 4 43 .26 18 91 PS Halictidae Lasioglossum (Evylaeus) sp 3 5 8 11 12 PS Halictidae Lasioglossum sp 1 29 4 15 14 62 2 2 PS Halictidae Lasioglossum sp 2 6 3 3 13 4 4 PS Halictidae Lasioglossum sp 3 1 8 10 1 PS Halictidae Lasioglossum sp 5 15 13 97 6 131 6 26 66 98 PS Halictidae Lasioglossum sp 6 4 3 3 11 47 13 5 17 82 PS Halictidae Lasioglossum sp 7 2 3 27 10 17 46 lOO PS Halictidae Lasioglossum sp 8 2 3 2 3 6 PS Halictidae Lasioglossum sp 9 58 2 1 3 64 PS Halictidae Lasioglossum sp 10 4 4 6 9 so Megachilidae Lithurge (Lithurgopsis) bituro/osa 4 3 7 9 9 so Megachilidae Megachi/e (Acentron) a/bitarsis 2 3 3 3 so Megachilidae Megachi/e (Austroinegachile) habilis 3 4 5 5 so Megachilidae Megachile (Cressoniella) sp 3 4 4 5 23 36 1 so Megachilidae Megachi/e (Cressoniella) sp 4 13 13 8 4 13 so Megachilidae Megachile (Che/ostomoides) sp B 1 1 2 3 so Megachilidae Megachile (Chelostomoides) otomita 5 5 2 2 so Megachilidae Megachile (Chelostomoides) sp 17 25 31 59 2 2 5 so Megachilidae Megachile (Chelostomoides) texensis 2 12 14 so Megachilidae Megachi/e (Melanosarus) totonaca 20 20 2 2 so Megachilidae Megachile (Neomegachi/e) chichimeca 13 10 125 13 161 so Megachilidae Megachi/e (Phaenosarus) sp 1 1 6 7 6 17 23 so Megachilidae Megachile (Sayapis) dentipes 71 6 81 4 162 8 8 so Megachilidae Megachi/e (Sayapis) sp 19 5 5 2 2 so Megachilidae Megachile (Ty/omegachile) s1mplicipes 2 6 3 12 18 18 so Megachilidae Megachile sp 2 24 2 26

189 Novelo-Rincón et al. :Community structure of native bees of Yucatan, Mexico

Table 7. Continue ... CLAVE DE SIMUI LS FAMILY SPECIES SDV TDF TF TSF TOT

so Megachilidae Megachile sp 5 2 8 10 so Megachilidae Megachile sp 6 1 1 o so Megachilidae Megachile sp 7 22 24 so Megachilidae Megachile sp 10 Instituto de Limnología "Dr. Raúl Ring so Megachilidae Megachile sp 11 26 27 La Plata, Argentina), C.C. 712, so Megachilidae Megachile sp 12 31 1 32 Investigaciones Clínicas, Casilla so Megachilidae Megachile sp 21 3 4 so Megachilidae Megachile sp 22 3 5 Coscarón-Arias, C. L. 2003. Clave de, so Megachilidae Megachile sp 23 ES Apidae Melipona beecheii 22 19 13 54 RESUMEN. Los Simúlídos son bien com PS Apidae Melissodes (Melissodes) tepaneca 8 7 15 para que sus huevos maduren. Por esta ra¡ PS Apidae Melissodes sp 1 11 13 como es el caso de la oncocercosis en ell ? Apidae Melissoptila sp 1 Se presenta una clave taxonómica de ? Apidae Melitoma marginella 4 5 (Ectemnaspis) bicoloratum Malloch, S. PA Apidae Mesoplia regalis 30 30 mayuchuspi Cascarón, S. fEct.) ochrace1 so Apidae Monoeca mexicana 3 3 (Ect.) rubiginosum (Enderlein), S. (Ect.) ES Apidae Nannotrigona perilampoides 378 42 7 9 436 S. (H) seriatum Knab, S. (Notolepria) e: Apidae Paratetrapedia (Paratetrapedia) moesta 40 40 Lutz, S. (Psa.) jujuyense Paterson y Shw Apidae Paratetrapedia sp 2 2 2 S. (Psa.) quadrifidum Lutz, S. (Psilopo Apidae Paratetrapedia sp 4 4 5 (Simulium) metallicum Bellardi, S. (J'r ES Apidae Partamona bilíneata 6 42 48 Gigantodax basíriflatus Wygodzinsky y 1 PS Apidae Peponapis limitaris 4 4 19 27 cypellus Wygodzinsky y Cascarón, G.fl• PS Apidae Peponapis smithi 8 8 3 19 Wygodzinsky y Cascarón, G. lazoi Tak¡ PS Apidae Peponapis utahensis 5 11 17 Cascarón, G. multifilis Wygodzinsky y ( PS Halictidae Pereirapis caucasica 32 1 33 y Cascarón y G. zumbahuae Wygodzinsl PALABRAS CLAVE: Simuliidae, clave tax ES Apidae Plebeia (Piebeia) frontalis 29 30 Andrenidae Protandrena sp 1 so Coscarón-Arias, C. L. 2003. Key ofSi1 PS Halictidae Pseudaugochloropsis gramínea 23 3 27 so Andrenidae Pseudopanurgus crenulatus 2 28 30 ABSTRACT. Black flies (Diptera, Simuli so Andrenidae Pseudopanurgus mexicanus 112 112 of most species requiere a blood meal fo1 so Colletidae Ptiloglossa sp 1 2 5 that cause diseases such as onchocercias ES Apidae Scaptotrigona pectoralis 17 147 33 78 275 persistent biting, swarming and crawling so Apidae Tetraloniella sp 1 3 4 Ecuador: S. (Ectemnaspis) bicoloratum l\ so Apidae Tetrapedia (Tetrapedia) maura 10 11 S. (Ect.) mayuchuspi Coscarón, S. (Ect. PA Apidae Triepeolus sp 2 2 Wygodzinsky, S. (E et.) rubiginosum (En~ ES Apidae Trigona (Frieseomelitta) nigra nigra 10 61 128 31 230 paynei Vargas, S. (H) seriatum Kna ES Apidae Trigona (Trigona) fulviventris 11 205 35 184 435 (Psaroniocompsa) incrustatum Lutz, S. (J ES Apidae Trigona (Trigona) fuscipennis 12 250 210 472 oyapockense Floch and Abonnec, S. (Ps' ES Apidae Trigonisca (Trigonisca) pipioli 49 49 Wygodzinsky and Cascarón, S. (Simulium PS Apidae Xylocopa (Megaxylocopa) nautlana 13 5 18 Cascarón and Py DaJOiel, Gigantodax btJ PS Apidae Xy/ocopa (Neoxy/ocopa) mexicanorum 86 4 10 2 102 Wygodzinsky 1110d Cascarón, G. cypellw. PS Apidae Xylocopa (Schoenherria) muscaria 1 Wygodzinsky and Cascarón, G. laeviga PS Apidae Xy/ocopa (Stenoxylocopa) micheneri 3 3 Wygodzinsky 1110d Cascarón, G. misil multituberculatus Wygodzinsky and Cos Coscarón. KEY WORDS: Simuliidae, taxonomic key.

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