Diversity of Alticinae in Oaxaca, Mexico: A preliminary study (Coleoptera, Chrysomelidae)

Abstract This is a preliminary study of the diversity of the Flea Beetles (Alticinae) of the Mexican state of Oaxaca based on fieldwork by the author in 1991, 1997, and 2010, the literature, and specimens in several institutional collections. The number of genera and species for Mexico as well as for Oaxaca increased significantly from previous studies. There are now 625 species in 90 genera recorded from Mexico with 275 species in 68 genera recorded from Oaxaca. There are 113 species known only from the state of Oaxaca and another 38 species known only from Oaxaca and the surrounding states. Oaxaca has a relatively high diversity as well as a high percentage of endemism. This study also demonstrates the effects of how even a small amount of fieldwork together with extracting specimen data from institutional collections can significantly increase the total faunistic and diversity knowledge of an area. A complete list of the genera and species known from Oaxaca is included.

The Sierra de Juárez is one of Oaxaca State's wettest areas and richest in forest diversity, with perhaps 2000 of the 8000 or more plant species that are found in the state. It is mostly covered by montane cloud forest, but includes tropical evergreen forests and forests of pine, pine-oak and oak. The cloud forest forms a band from 1,000-1,400 m in height up to 2,250 meters along the northern and eastern slopes. The cloud forest climate is cool (14°-20° C) and has mean annual rainfall that exceeds 2,000 mm and is sometimes much higher. The dominant trees are 20-30 m tall and include evergreen and deciduous species, palms, tree ferns, heather shrubs, vines, and moisture-loving herbs (the facts above were taken from Wikipedia).
As evident from Maps 1 and 2 Oaxaca is positioned in a rather unique biogeographical part of Mexico and, in fact, Central America. It is bordered north and west by the rather dry and deep Rio Balsas (an almost west-east) transect of the state of Guerrero. To the north and east is the southern-most aspect of one of the other major mountain ranges of Mexico, the Sierra Madre Oriental, at that point in Veracruz. The eastern most part of Oaxaca spans the Isthmus of Tehuantepec that borders the state of Chiapas. The Isthmus of Tehuantepec is not mountainous and is distinctly the narrowest part of Mexico where the states of Oaxaca, Veracruz, Chiapas and Tabasco converge. This geographical con- striction certainly has an effect on the diversity and distribution of the fauna and flora. Presumably to the south the biodiversity is predominantly Neotropical.
For Mexico's phanerogamic flora the highest diversity is found along a belt originating in Chiapas, traversing Oaxaca, and continuing to central Veracruz in the east and to Sinaloa and Durango on the west and cloud and evergreen forests are the most diverse per unit area, endemism is prevalent, and Oaxaca has a higher number of species than any state (Rzedowski 1993). Llorente-Bousquets et al. (1993) report that based on butterflies (Papilionoidea) the two most species-rich areas in Mexico are the Sierra de Juárez (the area of the present study) and Los Tuxtlas (Veracruz), with the highest numbers of species in Oaxaca (40), Chiapas (41), and Veracruz (41). In a survey of 20 different groups of arthropods (8,599 species), the most diverse states were Veracruz (2072), Chiapas (1306), Oaxaca (1256), Guerrero (1124) (Llorente-Bousquets et al. 1996).
The current study is part of a series of publications on the diversity of Alticinae (Flea Beetles) in Mexico (Furth , 2006(Furth , 2007(Furth , 2009Savini et al. 2001). Be-Map 2. Oaxaca with the surrounding states and demonstrating the strong geographical constriction of the Isthmus of Tehuantepec. sides elucidating the biological diversity of Mexico based on this taxon of herbivores, it provides an example of how the historical literature, historical collecting based on specimens in institutional collections, and new fieldwork can be combined to relatively rapidly assess such diversity. Although the historical literature is a fixed entity, when more institutional collections are examined or surveyed for historical collecting records and when more targeted fieldwork is conducted (even for short periods), there is a significant increase in diversity knowledge very quickly. Savini (1996, 1998) listed all Alticinae known from Central America with their known distribution.  published the first accounting of Alticinae diversity in Mexico based primarily on the historic literature as well as some specimens from collections at the USNM, a few borrowed specimens from other collections, and some from very brief collecting by the author in 1991, 1993, 1995, and 1997. At that time there were 501 species in 85 genera listed from Mexico of which 96 species in 33 genera were recorded from Oaxaca. This made Oaxaca the third most diversity state behind Veracruz (182 species) and Guerrero (124 species), and just ahead of Durango Map 3. Google Earth view of the Sierra de Juárez mountains with the current study's home base of Ixtlán de Juárez and some of the collecting localities from the 2010 field trip, especially Santa Catarina Lachatao.
(87 species) and Tabasco (74 species). Because most of these data were based on very old and sporadic collecting, they were very preliminary and also may have reflected the accessibility or popularity of certain locations. Nevertheless, the biological diversity was understandably higher in most of the southern Mexican states, e.g., Chiapas, Guererro, Oaxaca, Tabasco, and Veracruz presumably due to their proximity to the Neotropics. This has also been documented for other groups of animals, including insects, such as for Odonata (González and Novelo 1996), Psocoptera (Mockford andAldrete 1996), Passalidae (Reyes-Castillo 2002), and Bruchinae (Nápoles 2002).
In Furth (2006) new data was added that changed the Alticinae diversity in the various Mexican states, but Oaxaca remained third most diverse with 122 species, Guerrero remained second with 141, and Veracruz was the most diverse with 198. Other states with significant diversity (Furth 2006) were Durango (97 species), Mo-Map 4. The Sierra de Juárez mountains of Oaxaca with the surrounding smaller mountain systems. relos (84), Tabasco (81), and Chiapas (81). It is noteworthy that of these seven most diverse states, five are surrounding Oaxaca.
As discussed in  in Mexico there is a major biogeographic transition zone between the Nearctic and Neotropical Regions and biogeographic affinities may also vary greatly depending on the group considered. Also levels of endemism vary greatly depending on the group considered and, of course, depending on the relative knowledge of the group. As with any country some vertebrate and plant groups are well known, whereas most insect groups are not. Aspects of Mexican biogeography and endemism were also discussed in  with some examples from other groups provided. Biogeography and endemism will be treated below relative to the data from this study regarding Oaxaca and surrounding states.

Materials and methods
The data for this study was taken from three primary sources: first, from previously published literature, especially , Furth (2006) that included original published literature, including ; second, from museum specimens borrowed from a variety of collections as follows: University of California, Berkeley The Appendix is a combination of older records from the literature, a few collections (USNM, MCZ, NHMB), and new collection records from 8 other institutions above and the author's field work (DGF 1991(DGF , 1997(DGF , 2010.
Examination and determination of the specimens was made using a Leica MZ APO binocular dissecting microscope. The digital photos of Figure 10 were produced by Karolyn Darrow using the Visionary Digital ™ imaging system and Adobe Photoshop ™.
The fieldwork was primarily based out of the Universidad de la Sierra Juárez (USJI) ( Figure 11). Alticinae were collected by general and/or host plant-targeted sweeping with a 15 inch diameter aerial insect net using an aspirator. The majority of the field sites were in the vicinity of Santa Catarina Lachatao (SCL) and daily trips were accompanied by Prof. Atilano Contreras Ramos (UNAM), Prof. Jose Arturo Casasola (USJI), and various members of the SCL community ( Figure 12). After the fieldwork extensive collection examination and curation was done at the Colección Nacional de Insectos, Instituto de Biología, UNAM (Figure 13, 14)

Results
As a result of a week of fieldwork in Sierra de Juárez of Oaxaca, Mexico, in 2010 and subsequent determination of the specimens collected, as well as examination of several institutional collections, the number of known species of Alticinae of Mexico increased from 524 (Furth 2006) to 625 ( Figure 1) -an increase of over 19%. At the generic level there was only one genus added to the overall fauna of the country (Figure 2). Also resulting from the new fieldwork and collections examined, the number of recorded species for the state of Oaxaca increased from 121 (Furth 2006, 122 were reported but one found later to be in error) to 275 ( Figure 3) -an increase of almost 79% and the number of Oaxacan genera rose from 37 to 68 ( Figure 4) -an increase of 84%. At both   Furth ( , 2006 and the current study. the species and generic levels in Oaxaca these increases were significantly more than the increases from  to Furth (2006) for species of 96 to 121 (26%) ( Figure 3) and for genera from 30 to 37 (23%) ( Figure 4).
As for the endemism of Oaxaca as demonstrated by the Alticinae, Figure 5 shows that in Furth ( , 2006 there were 9 and 11 species, respectively, recorded only from the state of Oaxaca, but as a result of the 2010 fieldwork there are 113 speciesan increase of almost 930% from Furth (2006). Many of these (81 species or 72 %) currently only have morphospecies names and probably a significant proportion of these are new to science (see Appendix for OM species numbers). If the endemism is examined at a somewhat broader perspective, i.e., including species recorded in Oax-   Furth ( , 2006 and the current study.

Figure 5.
A comparison of the number of endemic species of Alticinae from Oaxaca only and from Oaxaca plus the surrounding states as recorded in Furth ( , 2006 and the current study. aca as well as the surrounding states (those bordering Oaxaca, plus Tabasco) then the endemic species from the 2010 data is a less dramatic increase from Furth ( , 2006 or 25 to 38 -an increase of 52% ( Figure 5). This means that of the 275 species recorded from the 2010 fieldwork from Oaxaca, 155 (55%) species are endemic at some level; 41% are restricted endemics known only from Oaxaca and 14% are more broadly endemic; known also from surrounding states ( Figure 6). Figure 7 shows the numbers of species (62) and genera (29) collected by the author during fieldwork from different trips to Oaxaca (1991Oaxaca ( , 1997Oaxaca ( , 2010. Of these the 2010 collecting trip alone resulted in 49 species and 26 genera. The 1991 collecting trip was 5 days, the 1997 trip 2 days, and the 2010 trip 7 days. Thus, the 2010 trip alone produced 79% of the species and 90% of the genera (Figure 7).

Figure 7.
A comparison of the numbers of species/genera recorded from total evidence (literature, collections, author fieldwork), from all fieldwork (1991,1997,2010), and from the 2010 field trip alone. Examining the biogeographical affinities of the Alticinae diversity of Oaxaca at the generic level, i. e, the biogeographic affinities of the 68 genera recorded, there are 6 (9%) genera of Nearctic affinity, 7 (almost 10%) of Cosmopolitan affinity, and 54 (81%) of Neotropical affinity (Figure 8).
Another way to look at the diversity of the Oaxacan Alticinae is to examine the number of species per genus. As shown in Figure 9 of the 68 genera recorded from Oaxaca there is a high number of genera (26) with only one species and a high number of species (16 + 19 + 23 + 24) or 82 from only one genus, with a trend towards more species from fewer genera. Figure 10 illustrates a few representatives of Alticinae genera and species that demonstrate presumed endemism and significant affinities of the biogeographical elements and distributional extensions in Oaxaca. Sphaeronychus OM sp. 2. (Figure 10A) represents one of two probable new species in a genus known from Brazil (25 species), one each from Ecuador and Peru, and only 2 known species from Central America. Allochroma OM sp. 1 ( Figure 10B) is a probably new species representing a Neotropical genus with 11 known species from Mexico (Furth 2006), another 18 from Central America, and about 7 from South America. Deuteraltica OM sp. 1 ( Figure 10C) is an undescribed species of a monotypic genus only known from Mexico, Guatemala, and El Salvador . Hypolampsis OM sp. 2 ( Figure 10D) is a probably new species of a very large genus (possibly the largest Neotropical genus of Alticinae) with only 4 known species from Mexico (Furth 2006), another 15 known from elsewhere in Central America , and more than 60 from South America. Disonycha nigrita Jacoby ( Figure 10E) is new to Mexico from the south, previously known only from Guatemala and El Salvador. Trichaltica zapotensis (Jacoby) ( Figure 10F) is new to Mexico from the south, only previously only known from Guatemala and originally described as a species of Crepidodera. New Genus OM A ( Figure 10G) is almost certainly a new genus probably of Neotropical affinity. Phyllotreta aeneicollis Crotch ( Figure 10H) is a Nearctic element, new to Mexico from the north, previously only known from southeastern, south central, southwestern USA.

Discussion
As indicated in the Introduction and evident from Maps 1-4, Mexico is geographically positioned rather uniquely between North America and South America and with a large diversity of landscapes, climates, and microhabitats; these are reflected in its diversity of flora and fauna. The southern state of Oaxaca is an interesting reflection of this diverse Mexican geography and its habitats with its own set of special features.
The data in Furth ( , 2006 were compiled primarily from researching the historical and more recent literature as well as from searching and determination of a few collections (i. e., the USNM, MCZ, and NHMB). The author's previous studies of Alticinae diversity of Mexico were published (2004,2006) and were based on the literature and examination of primarily two research collections. The current study resulted from more extensive examination of collections from a variety of institutional research collections and a single, brief field trip to one area of Oaxaca. This multifaceted strategy of reviewing the literature, then searching and examining historical research collections at a larger variety of institutions, as well as increased fieldwork is   demonstrated well by the current study. Primarily as a result of the rather brief 2010 fieldwork coupled with the study of at least eight additional institutional collections the number of species known from all of Mexico as well as from Oaxaca increased dramatically, 19% and 79%, respectively. After all examination of historical collections or "indoor collecting", as it is sometimes called, is the result of many different collecting events (and methods) over many years by different collectors. Also targeted fieldwork by an expert produces significant increase in the known fauna in a relatively short time. The efficacy of the combination of these two aspects (examining new collections and new collecting) is demonstrated by the significant increase in Oaxacan Alticinae diversity by 79% for species and 84% for genera.
The three expert field collecting trips by the author in 1991, 1997, and 2010 were of different lengths and, in the case of 1991, at somewhat different seasons. In each case at least one day was spent collecting in the general vicinity of Oaxaca City, but the 1991 and 2010 field trips overlapped considerably geographically. Therefore, the increase in recorded Alticinae diversity for Oaxaca is due to the addition of a significant number of institutional collections examined as well as the intensive 7 days of fieldwork in 2010.
As mentioned above in the Introduction several previous studies of various members of the flora and fauna have demonstrated the high levels of endemism in southern Mexico, especially in Oaxaca. Again, the current study with its increased examination of institutional collections and additional targeted field collecting demonstrated a very large increase (almost 10 times) in apparent endemic species when limited to those only recorded from the state of Oaxaca. Of course, some of this is the result of the fact that many of these species could not be determined to species; therefore, only recorded as Oaxaca, and may either be new to science or previously rarely collected and they may in fact have somewhat broader distribution outside Oaxaca. However, when endemism is extended to the states directly surrounding Oaxaca, a more conservative and probably more realistic demonstration of Oaxacan Alticinae species endemism is revealed of 55%. Of these 41% (113 species) are currently known to be restricted to the state of Oaxaca and 14% (38 species) are known from Oaxaca and the surrounding states.
As mentioned above, one of the objectives of this study is to demonstrate how a variety of research strategies provides a comprehensive account of the diversity for particular region through a combination of researching historical literature, examination of historical collections, and fieldwork. Figure 7 illustrates this on the left-hand histogram through the total results of this study of Oaxacan species and genera of Alticinae. However, to demonstrate the effectiveness of targeted expert fieldwork the middle histogram bars show the 1991 (5 days), 1997 (2 days) and 2010 fieldwork by the author combined and those on the right-hand show the Alticinae diversity captured only for the more extensive (7 day) trip in 2010. The 2010 fieldwork produced 79% of the species and 90% of the genera collected during the author's fieldwork. However, this may also reveal something about seasonality for collecting Alticinae in Oaxaca; that is, it is best earlier in the season (July rather than August), especially because the majority of collecting in 1991 was in the Sierra de Juárez, like in 2010.  As demonstrated in Figure 9 it is interesting to review the Alticinae taxa of Oaxaca and to note how many species are represented in each genus. For 26 genera (38%) there is only a single species known, whereas there is one genus that has 24 species (9 %) and 82 species (30%) in 4 genera (6%) are represented by single genera. At this time it is not evident the exact cause of this, yet it is still of interest to see this U-shaped curve of species to genera.
Biogeographically it is not surprising that 81% of the genera of Alticinae in Oaxaca show a Neotropical affinity. Other Coleoptera groups also show a strong Neotropical affinity in Mexico overall such as for the species of Curculionidae (41%) (Anderson and O'Brien 1996) and Carabidae at the generic level (40%) are Neotropical (Ball and Shpeley 2000). The geographic position of the state of Oaxaca that includes the extreme "bottleneck" like constriction of the relatively flat Isthmus of Tehuantepec is apparently very important biogeographically and apparently even serves as a kind of transition zone between the more southern Neotropical fauna and the more northern Nearctic fauna. It is probably here that the strong Neotropical influence begins to filter northwards as indicated in  within the southern, more tropical climates of Veracruz and Guerrero. As reported in Furth (2006) the high species diversity in all of Mexico generally is in the southern states of Veracruz (198), Guerrero (141), Oaxaca (122), Chiapas (81), and Tabasco (81). This diversity is certainly influenced strongly by the Neotropical affinities of the taxa. As a result of the current study Oaxaca has jumped to first place among Mexican states as the most Alticinae-diverse, with 275 species -a combination of more extensive examination of collections and the 2010 fieldwork.
In this particular study the 2010 expert fieldwork was done only in one relatively small area of this large tropical state (Oaxaca), i. e., Sierra de Juárez. Given the fact that Oaxaca has many other kinds of habitats and geography (see Maps) one would expect the actual Alticinae diversity to be significantly greater. When other areas of Oaxaca are sampled and even more research collections examined this fact will certainly be realized.
The flora and fauna of Oaxaca is truly diverse demonstrated here by the Alticinae, but the people and culture of Oaxaca is also especially diverse and endemic as can be experienced in the annual festival celebrating this cultural diversity -the Guelaguetza (Figure 15). For help and collaboration with access to the Mexican National Insect Collection (Universidad Autonóma de México, Instituto de Biología) as well as with collecting and export permits I am especially gratefull to Atilano Contreras-Ramos, Joaquin Bueno, Silvia Santiago, Santiago Zaragoza; Jose Arturo Casasola (Universidad de la Sierra Juárez, Ixtlán, Oaxaca) for various special arrangements and logistics during much of the 2010 fieldwork. And to the officials and people of Santa Catarina Lachatao a special thanks for allowing our group to work in their municipality.
List of genera and species names, species authors for Alticinae currently known from Oaxaca. Also listed in the columns are the known distribution in Mexican states outside of Oaxaca (see list below) for these standard state abbreviations), the sources for any records found by the author in various institutional collections (see Methods for abbreviations), and records from the author's fieldwork indicated as DGF1991, DGF1997, DGF2010. OM sp.1 indicates a morphospecies name (one that cannot currently be associated with any already described species) found by the author in Oaxaca, Mexico, i.e., OM. Taxon names with a "?" afterwards have some question as to the correct determination of this species. A species with a "?" after the state acronym means that there is some question as to the certainty of the locality from that state. Author names for genera can be found in Savini (1996, 1998). The references for this Appendix are listed separately.