TY - JOUR
AU - Escoto-Moreno, Jaime, A
AB - Abstract We describe the biodiversity, seasonal variation, and the possible edge effect of Coleoptera found in the canopy of the cloud forest in Tlanchinol in the state of Hidalgo. The coleopterans were collected by means of three fogging events during the dry season and another three during the rainy season in three sites of the forest: the edge, an intermediate, and an internal site. In total, 3,487 coleopterans were collected, belonging to 325 morphospecies from 52 families. The family with the largest number of morphospecies and abundance was Staphylinidae, followed by Curculionidae and Chrysomelidae. Species richness and abundance were higher in the dry season than in the rainy season. The biodiversity analyses, however, suggest that the rainy season showed the highest biodiversity levels, mainly because of the pronounced dominance of some species in the dry season. Species composition was different between the dry and rainy seasons. The internal site showed the lowest biodiversity compared with the intermediate and edge sites. The main edge effect detected was that species composition in the edge site differed from the intermediate and internal sites. Species composition did not differ significantly between the two latter sites. These results suggest that the study zone had a considerable level of biodiversity of Coleoptera and that it was very likely in a well-preserved condition, which supports the findings of another study previously performed in the same site using flight intercept traps. beetles, conservation, diversity, edge effect, fogging The forest canopy hosts a considerable portion of global biodiversity and constitutes an active photosystem of biomass in ecosystems (Lowman and Wittman 1996). It is estimated that global species richness is represented by a high number of canopy arthropods (Erwin 1982, Stork 1987, Stork et al. 1997). Trees are the main structure forming the forest canopy; the trunks and branches are the infrastructure that provides support for thousands of species of plants and arboreal animals (Nadkarni et al. 2001). Erwin (1983b) referred to the tropical forest canopy as “the last biotic frontier” because of the vast, yet scarcely studied species richness, particularly arthropods. The arthropod fauna inhabiting the forest canopy has been studied globally using various sampling techniques, but one of the most used techniques in the past decades has been canopy fogging, which has provided surprising results regarding the great species biodiversity found in this ecosystem and has been effective for comparing arboreal fauna in the different canopy stratum (Erwin 1983b). In Mexico, there are no studies on diversity of Coleoptera of the cloud forest canopy. Pérez García (1996), however, analyzed the coleopteran fauna in the foliage of a deciduous forest in the Chamela region, in the state of Jalisco, using malaise traps and canopy fogging, and registered 8,711 individuals belonging to 60 families, of which 3,181 individuals from 45 families were collected using canopy fogging. Tovar-Sánchez et al. (2003) analyzed insect communities from an oak canopy in sites with varying degrees of disturbance and fragmentation in the municipalities of Mineral del Chico, in Hidalgo, and Cahuacán and Juchitepec in state of Mexico. These authors examined 54 trees during the dry and rainy seasons and found 831 morphospecies in total, belonging to 20 different arthropod orders. The cloud forest in Mexico is one of the most diverse, yet restricted vegetation types. It is characterized by frequent clouds at the vegetation level, and, hence, it is commonly known as “cloud forest” (Toledo-Aceves 2010). It is estimated that less than 1% of the national territory is occupied by primary vegetation of mountain cloud forest (8,809 km2; III series, INEGI 2005), and approximately 50% of the original cloud forest area has been replaced by other coverage types (Challenger 1998). Mountain cloud forests is found in several states of Mexico, mainly in the mountain systems that include the Sierra Madre Oriental, Sierra Madre Occidental, Sierra Madre del Sur and Sierra Madre de Chiapas, in an altitudinal gradient of 1000 to 2000 m. (CONABIO 2010). In Mexico, mountain cloud forests are subject to severe changes in structure and composition because of natural processes or anthropogenic disturbance, the latter being the most important factor shaping the forest distribution, restricting it to sites with difficult access and making the current distribution much smaller than the one estimated in past decades (CONABIO 2010). These changes in the structure and composition of cloud forests can potentially affect the distribution of Coleoptera caused by changes in the landscape configuration, particularly for canopy coleopterans, since the canopy cover transforms from continuous and complex to isolated tree fragments with a much simpler vertical structure and with more open areas exposed to direct sunlight (Müller et al. 2018). The effect of these open areas within the canopy has been studied on coleopteran biodiversity (Seibold et al. 2016) and the complexity of canopy vegetation in the composition of arthropods (Seibold et al. 2016). In addition, the results show either positive or negative effects depending on the guild studied. The canopy spaces, which expose sunlight, can provide edge effects because the discontinuity in the canopy provides a change in light, temperature, and arboreal species composition. This may influence the coleopteran species composition as it provides the conditions needed for species that either avoid or prefer forest edges. The response of coleopterans to edges has been extensively studied, particularly in dung beetles (Martello et al. 2016, Villada-Bedoya et al. 2017), and the results showed beetles can either respond positively or negatively to edges. There are no studies yet, however, on edge effects and the biodiversity of Coleoptera in mountain cloud forest canopy. In this study, we analyze the biodiversity of coleopterans inhabiting the mountain cloud forest canopy in Tlanchinol, Hidalgo. The importance of this study lies in the fact that we include two of the most diverse biotic elements of the country, which so far have not been analyzed together: coleopterans and the mountain cloud forest. In particular, we analyze the morphospecies richness, abundance, biodiversity, and community structure, according to seasons (dry and rainy) and sampling sites (forest edge, an intermediate, and an internal site). Materials and Methods Study Area The municipality of Tlanchinol belongs to the state of Hidalgo and is embedded in the Sierra Madre Oriental, at an altitude of 1,590 m. Its geographic coordinates are 19°59′21″N and 98°40′43″W. Tlanchinol borders the state of San Luis Potosí to the north, the municipality of Calnali to the south, Huazalingo and Huejutla to the east, and Lolotla to the west (CEEMH 1998). It is located within the region of the Huasteca Alta of Hidalgo, mesophilic subregion of the northeast from Hidalgo to Huayacocotla, and it is a dense forest, with two or three tree strata, reaching heights of 30 to 35 m. The highest trees found are Liquidambar macrophylla L., Pinus greggii Engelm, P. patula Schltdl & Cham., Quercus eugeniifolia Liembmann, Q. sapotifolia Liebmann, 1854 y Q. sartorii Liebmann (Luna et al. 1994). Some cycad species (Zamiaceae) of the genera Dioon Lindl., Zamia L., and Ceratozamia Brongn. inhabit the area, as well as many other species of phanerogams (Luna et al. 2001, León y Paniagua et al. 2010). The study site is called “La Cabaña,” located 2 km northeast of Tlanchinol at 21°01′N, 98°38′W and an altitude of 1,485 m, with a mountain cloud forest that maintained a good conservation status during the sampling years (2004 to 2005). Sampling Procedure The sampling was conducted during July, August, and September 2004 in the rainy season, and in March, April, and May 2005 in the dry season. On each sampling survey, we set up two transects separated by 500 m. Each transect was considered a replicate and inside each one, we selected three sampling sites (Fig. 1). The first site was the forest edge (hereby referred to as “edge,” Fig. 1B), the second was 100 m from the edge in a straight line towards the forest (“intermediate,” Fig. 1C), and the third was 200 m from the edge in a straight line towards the forest (“internal,” Fig. 1D; Fig. 1). Each site covered an area of 10 m2, in which 25 plastic surfaces were laid out and distributed in four lines, each with five surfaces (Figs. 1D and 2). During the early morning hours (4:00 to 5:00 a.m., with the lowest amount of wind affecting the vertical displacement of the insecticide cloud), the canopy of the six sites was fumigated. For each fumigation, a SuperHawk thermo-nebulizer sprayer of the Dyna-Fog brand (Fig. 1A), which contained 1 liter of solution consisting of 5% biodegradable insecticide brand ULD BP-300 based on pyrethrins and 95% mineral oil, was used. The fumigation (fogging) stopped when this liter of insecticide with mineral oil was finished. A couple of hours after fogging, the specimens were collected using brushes and 70% ethanol. The organisms were collected in each sampling site; all organisms from the 20 sampling surfaces were pooled to have one unique sample per site (Fig. 1D). We used the same pyrethrums and procedure reported by Erwin (1989). This biodegradable insectide only knocks out the insects but does not kill them (Adis et al., 1997, 1998a, b). Furthermore, the effectiveness of the insecticide only persists 2 or 3 h after fogging. We only collected the insects that fell down into a bottle with ethanol into the sampling surfaces (Fig. 1D). The rest of the insects regained consciousness after approximately 4 h, and we saw flying insects while we were removing the sampling traps. Fig. 1. View largeDownload slide Collection sites of canopy beetles in the cloud forest of Tlanchinol, Hidalgo. (A) Fogging machine used for sampling in a test near the edge of the forest. (B) Edge of the forest with some plants of alcatraz sown. (C) Panoramic view of the intermediate site of the forest. (D) Internal site of the forest showing the arrangement of the collecting surfaces, with two authors and two collaborators in the project (photos A–C: J. Asiain, D: J. Márquez). Fig. 1. View largeDownload slide Collection sites of canopy beetles in the cloud forest of Tlanchinol, Hidalgo. (A) Fogging machine used for sampling in a test near the edge of the forest. (B) Edge of the forest with some plants of alcatraz sown. (C) Panoramic view of the intermediate site of the forest. (D) Internal site of the forest showing the arrangement of the collecting surfaces, with two authors and two collaborators in the project (photos A–C: J. Asiain, D: J. Márquez). Fig. 2. View largeDownload slide Sampling design of Coleoptera in the canopy of the cloud forest in Tlanchinol, Hidalgo, Mexico. Fig. 2. View largeDownload slide Sampling design of Coleoptera in the canopy of the cloud forest in Tlanchinol, Hidalgo, Mexico. Identification of Specimens The collected specimens were preserved in either 70% ethanol or mounted with entomological pins to facilitate species identification, which was performed using specialized literature (White 1983, Arnett and Thomas 2001, Triplehorn and Johnson 2005). Specimens were identified with help from specialists (included in the acknowledgements) and comparing specimens previously identified from the Coleoptera Collection in Universidad Autónoma del Estado de Hidalgo (CC-UAEH), in which all of the collected specimens from this study are currently deposited. The classification criteria followed was that proposed by Bouchard et al. (2011). Data Analyses The data were analyzed according to seasons (dry and rainy) and to the sampling site (edge, intermediate, internal). First, the completeness of morphospecies inventory was calculated using the sample coverage (Chao and Jost 2012). This calculation was performed to compare seasons and sampling sites. We also compared species richness and abundance according to seasons and sampling sites using generalized linear models (GLMs; Crawley 2007) with a quasi-Poisson distribution. We used each transect separated 500 m as a replicate. Overdispersion was estimated and revised per model. Hill numbers were also calculated (Jost 2006) to compare biodiversity using the indices q = 0 representing the species richness, q = 1 representing the exponential value of the Shannon index and considering the species and their abundances, and q = 2 representing the inverse value of the Simpson index and giving higher values to dominant species. These values were compared using 95% confidence intervals. The inventory completeness, generalized linear models, and biodiversity estimations were calculated using R software 3.3.1 (R Development Core Team 2015). The species composition was compared using the Bray–Curtis index, which takes into account the species abundance in each sample. These values were compared using a PERMANOVA analysis with square-root transformed data to decrease the influence of highly abundant taxa and represented in a MDS (multidimensional scaling) with Bootstrap using the PRIMER v7 program (Clarke and Gorley 2015). This type of graph hierarchically organizes the similarity values among community pairs for locating each community in a two-dimensional space that maintains distances using the values, in this case, of the Bray–Curtis indices among communities. Results The taxonomic list including the number of specimens collected per replicate, month, and sampling site is available in Suppl Table (online only). In addition, in Suppl Table (online only), graphics of richness and abundance per month, replicate, and sampling site were included to show that was not possible to detect negative effects in these parameters after each sampling event that affected the results. In total, 3,587 coleopteran specimens were collected, belonging to 325 morphospecies and 52 families (Sensu Bouchard et al. 2011). The level of taxonomic identification was the following: 174 morphospecies at the family level, 72 to subfamily, 58 to genus, 13 to species or similar, 6 to tribe, and 2 to subtribe. Staphylinidae was the family with the most morphospecies (68), followed by Curculionidae (57) and Chrysomelidae (21). Another five families presented between 11 and 20 morphospecies, whereas 19 families were represented by only 1 morphospecies, and the rest of the families had between 2 and 10 morphospecies (Table 1). Table 1. No. of species and specimens collected for each Coleoptera family (arranged alphabetically) with highlighted in bold the 10 families with the highest number of morphospecies and/or the 10 families with the greatest abundance Families No. of species No. of specimens Aderidae 5 10 Anthribidae 5 6 Attelabidae 1 17 Biphyllidae 1 1 Brentidae 2 143 Buprestidae 1 1 Cantharidae 3 15 Carabidae 9 145 Cerambycidae 11 45 Cerylonidae 1 1 Chrysomelidae 21 695 Ciidae 2 2 Cleridae 3 11 Coccinelidae 2 8 Corylophidae 3 28 Cryptophagidae 4 12 Curculionidae 57 439 Disteniidae 1 3 Elateridae 11 87 Endomychidae 1 1 Eucinetidae 1 1 Hybosoridae 1 2 Hydrophilidae 1 3 Laemophloeidae 2 71 Lampyridae 3 11 Lathridiidae 1 86 Leiodidae 3 10 Lutrochidae 1 10 Lycidae 6 16 Melandryidae 2 11 Melyridae 3 6 Monotomidae 3 6 Mordellidae 12 55 Mycetophagidae 3 33 Nemonychidae 1 2 Nitidulidae 6 9 Passalidae 1 1 Phalacridae 2 3 Phengodidae 1 5 Ptiliidae 1 10 Ptilodactylidae 6 36 Ptinidae 7 38 Salpigidae 1 3 Scarabaeidae 5 34 Scirtidae 1 36 Scraptiidae 7 185 Silvanidae 1 6 Staphylinidae 68 1011 Tenebrionidae 15 75 Throscidae 1 3 Trogossitidae 2 3 Zopheridae 13 136 Total: 52 families Total of species: 325 Total of specimens: 3,587 Families No. of species No. of specimens Aderidae 5 10 Anthribidae 5 6 Attelabidae 1 17 Biphyllidae 1 1 Brentidae 2 143 Buprestidae 1 1 Cantharidae 3 15 Carabidae 9 145 Cerambycidae 11 45 Cerylonidae 1 1 Chrysomelidae 21 695 Ciidae 2 2 Cleridae 3 11 Coccinelidae 2 8 Corylophidae 3 28 Cryptophagidae 4 12 Curculionidae 57 439 Disteniidae 1 3 Elateridae 11 87 Endomychidae 1 1 Eucinetidae 1 1 Hybosoridae 1 2 Hydrophilidae 1 3 Laemophloeidae 2 71 Lampyridae 3 11 Lathridiidae 1 86 Leiodidae 3 10 Lutrochidae 1 10 Lycidae 6 16 Melandryidae 2 11 Melyridae 3 6 Monotomidae 3 6 Mordellidae 12 55 Mycetophagidae 3 33 Nemonychidae 1 2 Nitidulidae 6 9 Passalidae 1 1 Phalacridae 2 3 Phengodidae 1 5 Ptiliidae 1 10 Ptilodactylidae 6 36 Ptinidae 7 38 Salpigidae 1 3 Scarabaeidae 5 34 Scirtidae 1 36 Scraptiidae 7 185 Silvanidae 1 6 Staphylinidae 68 1011 Tenebrionidae 15 75 Throscidae 1 3 Trogossitidae 2 3 Zopheridae 13 136 Total: 52 families Total of species: 325 Total of specimens: 3,587 View Large Table 1. No. of species and specimens collected for each Coleoptera family (arranged alphabetically) with highlighted in bold the 10 families with the highest number of morphospecies and/or the 10 families with the greatest abundance Families No. of species No. of specimens Aderidae 5 10 Anthribidae 5 6 Attelabidae 1 17 Biphyllidae 1 1 Brentidae 2 143 Buprestidae 1 1 Cantharidae 3 15 Carabidae 9 145 Cerambycidae 11 45 Cerylonidae 1 1 Chrysomelidae 21 695 Ciidae 2 2 Cleridae 3 11 Coccinelidae 2 8 Corylophidae 3 28 Cryptophagidae 4 12 Curculionidae 57 439 Disteniidae 1 3 Elateridae 11 87 Endomychidae 1 1 Eucinetidae 1 1 Hybosoridae 1 2 Hydrophilidae 1 3 Laemophloeidae 2 71 Lampyridae 3 11 Lathridiidae 1 86 Leiodidae 3 10 Lutrochidae 1 10 Lycidae 6 16 Melandryidae 2 11 Melyridae 3 6 Monotomidae 3 6 Mordellidae 12 55 Mycetophagidae 3 33 Nemonychidae 1 2 Nitidulidae 6 9 Passalidae 1 1 Phalacridae 2 3 Phengodidae 1 5 Ptiliidae 1 10 Ptilodactylidae 6 36 Ptinidae 7 38 Salpigidae 1 3 Scarabaeidae 5 34 Scirtidae 1 36 Scraptiidae 7 185 Silvanidae 1 6 Staphylinidae 68 1011 Tenebrionidae 15 75 Throscidae 1 3 Trogossitidae 2 3 Zopheridae 13 136 Total: 52 families Total of species: 325 Total of specimens: 3,587 Families No. of species No. of specimens Aderidae 5 10 Anthribidae 5 6 Attelabidae 1 17 Biphyllidae 1 1 Brentidae 2 143 Buprestidae 1 1 Cantharidae 3 15 Carabidae 9 145 Cerambycidae 11 45 Cerylonidae 1 1 Chrysomelidae 21 695 Ciidae 2 2 Cleridae 3 11 Coccinelidae 2 8 Corylophidae 3 28 Cryptophagidae 4 12 Curculionidae 57 439 Disteniidae 1 3 Elateridae 11 87 Endomychidae 1 1 Eucinetidae 1 1 Hybosoridae 1 2 Hydrophilidae 1 3 Laemophloeidae 2 71 Lampyridae 3 11 Lathridiidae 1 86 Leiodidae 3 10 Lutrochidae 1 10 Lycidae 6 16 Melandryidae 2 11 Melyridae 3 6 Monotomidae 3 6 Mordellidae 12 55 Mycetophagidae 3 33 Nemonychidae 1 2 Nitidulidae 6 9 Passalidae 1 1 Phalacridae 2 3 Phengodidae 1 5 Ptiliidae 1 10 Ptilodactylidae 6 36 Ptinidae 7 38 Salpigidae 1 3 Scarabaeidae 5 34 Scirtidae 1 36 Scraptiidae 7 185 Silvanidae 1 6 Staphylinidae 68 1011 Tenebrionidae 15 75 Throscidae 1 3 Trogossitidae 2 3 Zopheridae 13 136 Total: 52 families Total of species: 325 Total of specimens: 3,587 View Large In addition, Staphylinidae had the largest organism abundance (1,011 specimens), whereas Chrysomelidae had the second largest abundance (695 specimens), followed by Curculionidae (439 specimens). The relative abundance of these three families corresponds to 60% of the overall abundance. Most of the collected species were represented by only one specimen (116), which represented 35.7% of the overall abundance. On the other hand, 102 species (31.4%) were represented by 3 to 10 organisms; 51 species (15.7%) were represented by 2 specimens; 50 species (15.4%) were represented by 11 to 100 specimens, and 5 species (1.30%) were represented by 101 to 200 specimens. Only one species (0.3%) had over 200 specimens. The latter, Eumolpinae sp. (Chrysomelidae), was the dominant species with 524 specimens collected, which represent 14.6% of all organisms collected. The following species, including Eumolpinae sp., represent the 10 most abundant species (in descending order): Aleocharinae sp. 3 (200 specimens, Staphylinidae), Apion Herbst. sp. 1 (137 specimens, Brentidae), Sepedophilus Gistel. sp. 1 (125 individuals, Staphylinidae), Palaminus Erichson sp. 1 (112 individuals, Staphylinidae), Scraptiidae sp. 2 (105 individuals), Palaminus sp. 3 (96 individuals, Staphylinidae), Curculionidae sp. 2 (94 individuals), Latridiidae sp. (86 individuals), and Colydiinae sp. 4 (83 specimens, Zopheridae). The completeness of the inventory, according to the sample coverage, was higher than 90% considering the seasonality and the forest sites where the sampling was performed. Therefore, all analyses were done using the observed values. Based on the comparisons of the GLMs, the season contributed significantly to species richness (χ2 = 13.96, df = 1, P < 0.001), but not sampling sites (χ2 = 3.65, df = 2, P = 0.16). For the abundance data, there were significant differences among seasons (χ2 = 276.24, df = 1, P < 0.001) and among sampling sites (χ2 = 161.35, df = 2, P < 0.001). During the dry season, the largest abundance of organisms was collected (2288) rather than in the rainy season (1299). For the sampling sites, the internal site showed the highest abundance with 1557 specimens, followed by the intermediate site with 1061 specimens, and the edge with 969 specimens. According to the Hill numbers, there were significant differences in species richness (q = 0) between the rainy season (197 effective number of species) and the dry season (238 effective number of species), the latter showing the greatest richness. For q = 1, however, the community in the rainy season (70.21 effective number of species) had a higher ecological biodiversity than the dry season (54.3 effective number of species) according to the confidence intervals (Fig. 3). The same pattern was observed with q = 2, where 32.67 effective number of species were estimated for the rainy season and 16.32 effective number of species for the dry season; these results show that with 2D the diversity in the rainy season is twice as much as in the dry season. Fig. 3. View largeDownload slide Hill number for the sampling seasons q = 0, q = 1, and q = 2. The confidence intervals are 95%. Fig. 3. View largeDownload slide Hill number for the sampling seasons q = 0, q = 1, and q = 2. The confidence intervals are 95%. Regarding the sampling sites, no significant differences were found for species richness (q = 0), where 189, 190, and 196 effective number of species were found for the edge, intermediate site, and internal site, respectively. The ecological biodiversity q = 1 showed no significant differences among the edge and intermediate sites (71.54 and 71.25 effective number of species, respectively), but we found significant differences for the internal site (54.38 effective number of species), with the latter showing significantly lower diversity compared with the other two sites. This result was consistent with q = 2 in which 30.79 and 33.72 effective number of species were estimated for the edge and intermediate site, as well as 18.65 effective number of species for the internal site (Fig. 4). Fig. 4. View largeDownload slide Hill number for the sampling sites q = 0, q = 1, and q = 2. The confidence intervals are 95%. Fig. 4. View largeDownload slide Hill number for the sampling sites q = 0, q = 1, and q = 2. The confidence intervals are 95%. The results from the PERMANOVA analysis show significant differences in the species composition among samples according to season (pseudo-F = 6.12, df = 1, P < 0.001) and to sampling site (pseudo-F = 1.46, df = 2, P = 0.04). In Fig. 5, the differences among seasons and sampling sites are shown. The latter showed no significant differences among the internal and intermediate sites, although the edge showed a significantly different species composition from the internal and the intermediate site. Fig. 5. View largeDownload slide MDS of the composition of the sampling for seasons (above) and for sampling sites (below) according to the Bray–Curtis index. Fig. 5. View largeDownload slide MDS of the composition of the sampling for seasons (above) and for sampling sites (below) according to the Bray–Curtis index. Discussion The identification of coleopterans even at the family level can be complex, but the effort invested in this activity is relevant because it allows us to know more about the biology of these organisms and even compare similar studies. This, however, is not possible when the identification is only at the order level, as has been done in the main studies performed in Mexico (Pérez García 1996, Tovar-Sánchez et al. 2003, Vaca-Sánchez et al. 2018; Table 2). Some families have highly varied feeding habits (e.g., Staphylinidae), whereas others have more specific habits (e.g., Curculionidae), which underlines the importance of identifying organisms at the lowest taxonomic level possible and segregate specimens into morphs when identification at species level is not possible. Table 2. Main studies about Coleoptera collected by canopy fumigation in Mexico (including the present study) and three of the most relevant studies in the Neotropical region (ordered chronologically) References Study zone No. of species No. of specimens No. of families (the three most diverse) Objetives and sampling effort Erwin and Scott (1980) Panama: Panama Canal More of 940 7,712 56 (Chrysomelidae, Staphylinidae, Cerambycidae) (excluding Curculionidae) Establish the seasonality, size patterns, trophic structure and richness of Coleoptera in the arboreal ecosystem of Luehea seemannii Triana & Planch. Fumigated 19 trees in a humid forest, during the less rainy season (July), rainier season (Oct.) and the drought season (Mar.–April) Erwin (1983a) Brazil: Manaos 1,080 4,845 57 (Curculionidae, Chrysomelidae, Staphylinidae) Comparison of Coleoptera of the canopy of Panama and Peru with those of the Amazon basin. Analysis based on 49% of the samples obtained in 10 transects of 50 m, 3 in each of the different forests (samplings were started at the beginning of the dry season): 1) flooded with black water, 2) flooded with water mixed, 3) on dry land, and 4) flooded with white water. The replica of the transects in each type of forest was no more than 1000 m Pérez García (1996) Mexico: Jalisco No data (specimens identified at family level without distinguish morpho species) 3,181 45 (No data) Analyze the abundance and food guilds of the Coleoptera of the foliage of a low deciduous forest and the comparison of the method of canopy fumigation with respect to the Malaise traps. An area of 100 m2 was fogging by installing 45 funnels of 0.5 m in diameter during 6 samplings carried out between 1992 and 1994 Tovar-Sánchez et al. (2003) Mexico: Hidalgo and Estado de México No data No data Identified to order To analyze the effect of disturbance and fragmentation on the diversity and composition of canopy arthropods of 6 species of oak in 3 localities of central Mexico. Fifty-four oaks were fogged in drought and rainy season, in three oak forests under different conditions of disturbance and fragmentation Araujo et al. (2005) Ecuador: Choco 1,054 4,853 69 (Curculionidae, Chrysomelidae, Staphylinidae) In 5 evergreen forest locations: 1) quantify the species richness and estimate the potential biodiversity, 2) examine the composition and assemblage of the arboreal coleoptera community, 3) determine the degree of variation of the community in a latitudinal gradient, 4) establish the degree of relationship between the complexity of the canopy and the richness of coleoptera. Sampling from April to July, in a transect of 1 km per locality, with 20 points at random, using sheets of 9 m2. The fumigation at each point was 1 min at 20:00 h Vaca-Sánchez et al. (2018) Mexico: Michoacán and Jalisco No data No data Although the specimens were identified to family, data are provided only to order To evaluate the structure and composition of the canopy arthropods in 5 localities with 2 to 4 species of Quercus L., always including Quercus laurina Humb. & Bonpl. Five individuals of Q. laurina were fumigated per site in 3 transects of 100 × 40 m with at least 500 m separation between them. In each transect, oak species were identified, measured, and counted. Funnel-shaped traps placed under the canopy were used Current work Mexico: Hidalgo 325 3,587 52 (Staphylinidae, Curculionidae, Chrysomelidae) Analysis of the richness, abundance, diversity and structure of the community, both by seasons (rain and drought) and by sampling sites (edge, intermediate, and internal), in a mountain cloud forest. Sampling conducted during 3 mo in the rainy season (July–Sept.) and 3 in the dry season (Mar.– May), with 2 replications. Each sampling includes a 200 m transect with 3 collection sites (edge, intermediate and internal). Each sampling point covered 10 m2 with 20 plastic surfaces. The replicates were 500 m apart from each other References Study zone No. of species No. of specimens No. of families (the three most diverse) Objetives and sampling effort Erwin and Scott (1980) Panama: Panama Canal More of 940 7,712 56 (Chrysomelidae, Staphylinidae, Cerambycidae) (excluding Curculionidae) Establish the seasonality, size patterns, trophic structure and richness of Coleoptera in the arboreal ecosystem of Luehea seemannii Triana & Planch. Fumigated 19 trees in a humid forest, during the less rainy season (July), rainier season (Oct.) and the drought season (Mar.–April) Erwin (1983a) Brazil: Manaos 1,080 4,845 57 (Curculionidae, Chrysomelidae, Staphylinidae) Comparison of Coleoptera of the canopy of Panama and Peru with those of the Amazon basin. Analysis based on 49% of the samples obtained in 10 transects of 50 m, 3 in each of the different forests (samplings were started at the beginning of the dry season): 1) flooded with black water, 2) flooded with water mixed, 3) on dry land, and 4) flooded with white water. The replica of the transects in each type of forest was no more than 1000 m Pérez García (1996) Mexico: Jalisco No data (specimens identified at family level without distinguish morpho species) 3,181 45 (No data) Analyze the abundance and food guilds of the Coleoptera of the foliage of a low deciduous forest and the comparison of the method of canopy fumigation with respect to the Malaise traps. An area of 100 m2 was fogging by installing 45 funnels of 0.5 m in diameter during 6 samplings carried out between 1992 and 1994 Tovar-Sánchez et al. (2003) Mexico: Hidalgo and Estado de México No data No data Identified to order To analyze the effect of disturbance and fragmentation on the diversity and composition of canopy arthropods of 6 species of oak in 3 localities of central Mexico. Fifty-four oaks were fogged in drought and rainy season, in three oak forests under different conditions of disturbance and fragmentation Araujo et al. (2005) Ecuador: Choco 1,054 4,853 69 (Curculionidae, Chrysomelidae, Staphylinidae) In 5 evergreen forest locations: 1) quantify the species richness and estimate the potential biodiversity, 2) examine the composition and assemblage of the arboreal coleoptera community, 3) determine the degree of variation of the community in a latitudinal gradient, 4) establish the degree of relationship between the complexity of the canopy and the richness of coleoptera. Sampling from April to July, in a transect of 1 km per locality, with 20 points at random, using sheets of 9 m2. The fumigation at each point was 1 min at 20:00 h Vaca-Sánchez et al. (2018) Mexico: Michoacán and Jalisco No data No data Although the specimens were identified to family, data are provided only to order To evaluate the structure and composition of the canopy arthropods in 5 localities with 2 to 4 species of Quercus L., always including Quercus laurina Humb. & Bonpl. Five individuals of Q. laurina were fumigated per site in 3 transects of 100 × 40 m with at least 500 m separation between them. In each transect, oak species were identified, measured, and counted. Funnel-shaped traps placed under the canopy were used Current work Mexico: Hidalgo 325 3,587 52 (Staphylinidae, Curculionidae, Chrysomelidae) Analysis of the richness, abundance, diversity and structure of the community, both by seasons (rain and drought) and by sampling sites (edge, intermediate, and internal), in a mountain cloud forest. Sampling conducted during 3 mo in the rainy season (July–Sept.) and 3 in the dry season (Mar.– May), with 2 replications. Each sampling includes a 200 m transect with 3 collection sites (edge, intermediate and internal). Each sampling point covered 10 m2 with 20 plastic surfaces. The replicates were 500 m apart from each other View Large Table 2. Main studies about Coleoptera collected by canopy fumigation in Mexico (including the present study) and three of the most relevant studies in the Neotropical region (ordered chronologically) References Study zone No. of species No. of specimens No. of families (the three most diverse) Objetives and sampling effort Erwin and Scott (1980) Panama: Panama Canal More of 940 7,712 56 (Chrysomelidae, Staphylinidae, Cerambycidae) (excluding Curculionidae) Establish the seasonality, size patterns, trophic structure and richness of Coleoptera in the arboreal ecosystem of Luehea seemannii Triana & Planch. Fumigated 19 trees in a humid forest, during the less rainy season (July), rainier season (Oct.) and the drought season (Mar.–April) Erwin (1983a) Brazil: Manaos 1,080 4,845 57 (Curculionidae, Chrysomelidae, Staphylinidae) Comparison of Coleoptera of the canopy of Panama and Peru with those of the Amazon basin. Analysis based on 49% of the samples obtained in 10 transects of 50 m, 3 in each of the different forests (samplings were started at the beginning of the dry season): 1) flooded with black water, 2) flooded with water mixed, 3) on dry land, and 4) flooded with white water. The replica of the transects in each type of forest was no more than 1000 m Pérez García (1996) Mexico: Jalisco No data (specimens identified at family level without distinguish morpho species) 3,181 45 (No data) Analyze the abundance and food guilds of the Coleoptera of the foliage of a low deciduous forest and the comparison of the method of canopy fumigation with respect to the Malaise traps. An area of 100 m2 was fogging by installing 45 funnels of 0.5 m in diameter during 6 samplings carried out between 1992 and 1994 Tovar-Sánchez et al. (2003) Mexico: Hidalgo and Estado de México No data No data Identified to order To analyze the effect of disturbance and fragmentation on the diversity and composition of canopy arthropods of 6 species of oak in 3 localities of central Mexico. Fifty-four oaks were fogged in drought and rainy season, in three oak forests under different conditions of disturbance and fragmentation Araujo et al. (2005) Ecuador: Choco 1,054 4,853 69 (Curculionidae, Chrysomelidae, Staphylinidae) In 5 evergreen forest locations: 1) quantify the species richness and estimate the potential biodiversity, 2) examine the composition and assemblage of the arboreal coleoptera community, 3) determine the degree of variation of the community in a latitudinal gradient, 4) establish the degree of relationship between the complexity of the canopy and the richness of coleoptera. Sampling from April to July, in a transect of 1 km per locality, with 20 points at random, using sheets of 9 m2. The fumigation at each point was 1 min at 20:00 h Vaca-Sánchez et al. (2018) Mexico: Michoacán and Jalisco No data No data Although the specimens were identified to family, data are provided only to order To evaluate the structure and composition of the canopy arthropods in 5 localities with 2 to 4 species of Quercus L., always including Quercus laurina Humb. & Bonpl. Five individuals of Q. laurina were fumigated per site in 3 transects of 100 × 40 m with at least 500 m separation between them. In each transect, oak species were identified, measured, and counted. Funnel-shaped traps placed under the canopy were used Current work Mexico: Hidalgo 325 3,587 52 (Staphylinidae, Curculionidae, Chrysomelidae) Analysis of the richness, abundance, diversity and structure of the community, both by seasons (rain and drought) and by sampling sites (edge, intermediate, and internal), in a mountain cloud forest. Sampling conducted during 3 mo in the rainy season (July–Sept.) and 3 in the dry season (Mar.– May), with 2 replications. Each sampling includes a 200 m transect with 3 collection sites (edge, intermediate and internal). Each sampling point covered 10 m2 with 20 plastic surfaces. The replicates were 500 m apart from each other References Study zone No. of species No. of specimens No. of families (the three most diverse) Objetives and sampling effort Erwin and Scott (1980) Panama: Panama Canal More of 940 7,712 56 (Chrysomelidae, Staphylinidae, Cerambycidae) (excluding Curculionidae) Establish the seasonality, size patterns, trophic structure and richness of Coleoptera in the arboreal ecosystem of Luehea seemannii Triana & Planch. Fumigated 19 trees in a humid forest, during the less rainy season (July), rainier season (Oct.) and the drought season (Mar.–April) Erwin (1983a) Brazil: Manaos 1,080 4,845 57 (Curculionidae, Chrysomelidae, Staphylinidae) Comparison of Coleoptera of the canopy of Panama and Peru with those of the Amazon basin. Analysis based on 49% of the samples obtained in 10 transects of 50 m, 3 in each of the different forests (samplings were started at the beginning of the dry season): 1) flooded with black water, 2) flooded with water mixed, 3) on dry land, and 4) flooded with white water. The replica of the transects in each type of forest was no more than 1000 m Pérez García (1996) Mexico: Jalisco No data (specimens identified at family level without distinguish morpho species) 3,181 45 (No data) Analyze the abundance and food guilds of the Coleoptera of the foliage of a low deciduous forest and the comparison of the method of canopy fumigation with respect to the Malaise traps. An area of 100 m2 was fogging by installing 45 funnels of 0.5 m in diameter during 6 samplings carried out between 1992 and 1994 Tovar-Sánchez et al. (2003) Mexico: Hidalgo and Estado de México No data No data Identified to order To analyze the effect of disturbance and fragmentation on the diversity and composition of canopy arthropods of 6 species of oak in 3 localities of central Mexico. Fifty-four oaks were fogged in drought and rainy season, in three oak forests under different conditions of disturbance and fragmentation Araujo et al. (2005) Ecuador: Choco 1,054 4,853 69 (Curculionidae, Chrysomelidae, Staphylinidae) In 5 evergreen forest locations: 1) quantify the species richness and estimate the potential biodiversity, 2) examine the composition and assemblage of the arboreal coleoptera community, 3) determine the degree of variation of the community in a latitudinal gradient, 4) establish the degree of relationship between the complexity of the canopy and the richness of coleoptera. Sampling from April to July, in a transect of 1 km per locality, with 20 points at random, using sheets of 9 m2. The fumigation at each point was 1 min at 20:00 h Vaca-Sánchez et al. (2018) Mexico: Michoacán and Jalisco No data No data Although the specimens were identified to family, data are provided only to order To evaluate the structure and composition of the canopy arthropods in 5 localities with 2 to 4 species of Quercus L., always including Quercus laurina Humb. & Bonpl. Five individuals of Q. laurina were fumigated per site in 3 transects of 100 × 40 m with at least 500 m separation between them. In each transect, oak species were identified, measured, and counted. Funnel-shaped traps placed under the canopy were used Current work Mexico: Hidalgo 325 3,587 52 (Staphylinidae, Curculionidae, Chrysomelidae) Analysis of the richness, abundance, diversity and structure of the community, both by seasons (rain and drought) and by sampling sites (edge, intermediate, and internal), in a mountain cloud forest. Sampling conducted during 3 mo in the rainy season (July–Sept.) and 3 in the dry season (Mar.– May), with 2 replications. Each sampling includes a 200 m transect with 3 collection sites (edge, intermediate and internal). Each sampling point covered 10 m2 with 20 plastic surfaces. The replicates were 500 m apart from each other View Large The fact that Staphylinidae was the family that showed the highest species richness can be due to their diverse feeding habits (predators, saprophagous insects, fungivores, among others; Navarrete-Heredia et al. 2002) and because this family is represented by 63,000 known species, which is the largest number of species known in all Coleoptera (Chani-Posse et al. 2018), including Scaphidiinae, Pselaphinae, and Scydmaeninae, which have been proposed as subfamilies of Staphylinidae in the past years, although they were considered separate families in previous works on canopy fauna. This result is congruent with the results reported for the same area where flight intercept traps were installed at 1.5 m above ground, which supports the fact that Staphylinidae has high species richness in this location (Pedraza et al. 2010). Curculionidae was the second most numerous family, probably because species from this family are mostly phytophagous and the study area had diverse and abundant vegetation. Additionally, it is the second most diverse family of all Coleoptera (Anderson and O’Brien 1996). Chrysomelidae, the third most numerous family collected in this study, is also one of the most diverse families with approximately 35,000 described species worldwide and with mainly phytophagous habits (Riley et al. 2002, Dial et al. 2006). The other families registered in this study showed lower species richness, probably because their feeding habits are more specific and the families themselves show lower diversity than Staphylinidae, Curculionidae, and Chrysomelidae. The results of this study are congruent with three of the most relevant studies performed in the Neotropical region (Table 2) given that Staphylinidae, Curculionidae, and Chrysomelidae were also the most abundant (Erwin and Scott 1980, Araujo et al. 2005), except in Panama (Erwin and Scott 1980), where individuals from the Curculionidae family were not examined. Among other studies, the families with the highest species richness in Uganda were also Staphylinidae, Curculionidae, and Chrysomelidae (Wagner 2000). Regarding the abundances by families, a consistent pattern of species richness was found. Staphylinidae was the most abundant family in this study, although Chrysomelidae showed higher abundance than Curculionidae mostly because of the high abundance have of Eumolpinae sp. We expected greater diversity and abundance of phytophagous insects given the large amount of vegetation cover, even though Staphylinidae was the family with the highest species richness. Staphilinids have a wide range of feeding behaviors, with only a limited number of feeding on plants (Navarrete-Heredia et al. 2002), so it was not expected to be the most abundant group, whereas Curculionidae and Chrysomelidae are generally phytophagous (Anderson and O’Brien 1996, Riley et al. 2002). A few dominant species such as Eumolpinae sp. were detected on the forest canopy maybe because it is rich in potential food plants. Only a few phytophagous species, however, were dominant and did not outnumber the staphylinid abundance. A study from Pedraza et al. (2010) using flight intercept traps also found that Staphylinidae was the most abundant family. Morphospecies richness (q = 0) was significantly higher during the dry season compared with the rainy season, which may be related to the fact that water (and several resources such as food) in the study area is never completely lacking, since even in the driest season there is fog that provides water in the form of dew in these forests (Luna et al. 2001, León y Paniagua et al. 2010, Toledo-Aceves 2010). It is possible that small organisms (less than 1 cm), which represent most of the morphospecies collected, were able to find shelter from the intense rain in sites where the insecticide cannot reach (such as nodes and epiphytic plants), unlike medium- and large-sized coleopterans (although we assume the latter may be able to escape once the fumigation began) that may have been less affected by the rain (Adis et al. 1997). Erwin and Scott (1980) also found that there were more small-sized species during the dry season than the rainy season. Similar results were found using flight intercept traps in the same location (Pedraza et al. 2010), which suggests there may be a negative impact from the rain on the activity of small coleopterans. Unlike the result of q = 0, the ecological biodiversity indices (q = 1 and q = 2) indicate that there is higher biodiversity during the rainy season than in the dry season. This result is mainly because the proportion of abundance is more evenly distributed among species despite having a reduced species richness in the rainy season, whereas the opposite was found in the dry season where more species were found. Some of the species were, however, dominant, and the distribution of abundance among species was uneven. Several studies have reported that diversity increases during the rainy season because in this season there is a greater availability of food resources for insects to feed on and there may be less competition, which leads to more evenly distributed populations (Martínez-Falcón et al. 2011, Ramírez-Hernández et al. 2014, García-López et al. 2016). On the other hand, resources are scarcer in the dry season, and competition for these resources increases. This process leads to the dominance of some species over others. There seemed to be a less even diversity of canopy coleopterans during the dry season compared with the rainy season. The resources in each season may be different, but the resources from the dry season likely benefit only a few species (the dominant species), whereas the resources from the rainy season benefit fewer species but those with more even populations. In this study, we did not analyze the type of resources in each season and what type of beetles consume them, but we encourage further studies to investigate the relationship between resource variation and canopy coleopteran biodiversity. According to sampling sites, significant differences were only observed in q = 1 and q = 2 in the internal site compared with the intermediate and edge sites. Despite the internal site showing a higher species richness, it also showed the lowest ecological diversity because the number of specimens per species was more heterogeneous. For example, 5 of the 10 most abundant species were also the most dominant in this site (Eumolpinae sp., Aleocharinae sp. 3, Apion sp. 1, Palaminus sp. 3, and Latridiidae sp.). This could be a result of having more species specific to areas shaded by the canopy and in higher numbers, which lead to unevenness and decreased diversity. In the edge and intermediate sites, however, there may be a combination of species that tolerate more variable conditions, thus showing a higher diversity and evenness than in the internal site. The former has been observed by Benítez-Malvido et al. (2016), who studied open areas in the forest and found that coleopteran species located in closed vegetation tend to be more specialized and the coleopterans from the open areas are more generalist. One aspect to consider is that even though the fumigation cloud elevated vertically, the insects collected may not have been from one single tree but from other surrounding trees of various canopy levels and microhabitats, thus forming a structurally complex system (Ashton et al. 2016), which is shown by the different diversity scores estimated for each sampling site. The forest canopy provides different resources for species, such as leaves, flowers, and fruits for the phytophagous species, but it also provides space and food for predators, parasites, and parasitoids (Gossner et al. 2014, Nakamura et al. 2017). According to Müller et al. (2018), the species richness in the canopy is favored by the habitat heterogeneity that is provided by a more complex vertical structure of the canopy; therefore, a combination of elements such as trees of different species and sizes, as well as the presence of epiphytes within the canopy, form more heterogeneous environments that increase species richness and abundance in the canopy. The fact that species composition differs from the rainy season to the dry season is in line with the differences observed in the diversity scores, since there are changes in morphospecies according to the season, which may be related to the changes in resource availability, such as buds, flowers, and fruits from the plants in the cloud forest, and possibly also to climatic factors, such as temperature and humidity. Given that Coleoptera represents such a vast community and the identification level here was often far from species level, it is difficult to ascertain which species are univoltine or multivoltine. It can be hard to find natural communities where coeopteran species composition does not change significantly across seasons, but, relevantly, the coleopteran diversity in the studied cloud forest remained high in both seasons, in agreement with Pedraza et al. (2010) who used flight intercept traps. Regarding composition of canopy coleopterans composition, significative differences were detected between edge and both the internal and intermediate sites. Although the forest edge showed less effective number of species and reduced abundance than the internal and intermediate sites, the diversity was higher than in the internal site, but it was not different from the intermediate site. The species collected at the edge, however, were different from the other sites. Differences in canopy coleopterans between the edge and more internal sites were somehow expected, although it was difficult to predict whether this difference would result in higher or lower diversity, or in higher or lower abundance. What we found is that the edge, with more light exposure, less canopy cover and possibly less plant species than in the internal and intermediate sites, showed different coleopteran species from the other sites. The former can be considered a positive aspect for the degree of conservation in the site because it is not losing biodiversity with the disturbance in the edge. These results, however, must be viewed with precaution given that the forest edge sampled can be an open space modified by human activities but of smaller dimensions compared with the surrounding forest. The area was not calculated without forest or the forest extension; therefore, we suggest that more replicates with different forest sizes are needed to unveil the effect of forest size and edge on biodiversity. Considering the recommendations from Adis et al. (1998a,b), another factor limiting the certainty of the results is not selecting a particular tree species to fumigate or at least identifying the tree species in every sampling site. Other studies suggest that the greater tree diversity in an ecosystem the greater the canopy coleopteran diversity, and tree diversity loss is also reflected in the reduction of canopy coleopteran diversity. This has been observed in oak forests in Mexico (Tovar-Sánchez et al. 2003, Vaca-Sánchez et al. 2018), in coffee plantations in Costa Rica under three different levels of shading (Perfecto et al. 1997), and in primary and secondary forests of Uganda (Wagner 2000). Therefore, it is possible that the observed edge effect in this study is due to a similar tree diversity among intermediate and internal sites, with a different tree species diversity at the edge sites, thus resulting in a similar coleopteran diversity but significantly different coleopteran species composition. The species richness found in this study is not comparable to any other study performed in cloud forests in Mexico because not only are these studies scarce, but also the identification level does not go beyond family level. We also need to consider that this study is complemented by another study using flight intercept traps (Pedraza et al. 2010), which found a slightly higher diversity than this study (352 morphospecies). Without a meticulous comparison of the species found in both studies, it is difficult to ascertain exactly how many species are shared among studies, but by mere observation based on the identification work (J.M., personal observations), it is estimated that between 50% and 75% of morphospecies are shared among these studies. In contrast with the study using flight intercept traps, which found the highest species diversity compared with the canopy fogging in Tlanchinol, Kitching et al. (2001) and Müller et al. (2018) have concluded that flight intercept traps do not collect all the canopy beetles since many of these species are not efficiently captured. On the other hand, the fogging technique offers a method for collecting most residents at different canopy levels. Therefore, we suggest continuing comparing both methods in different types of forests and at different canopy levels (in the case of intercept traps). Despite the results obtained, it is unlikely that the species richness in our study is similar to that registered in other sites with tropical evergreen rain forests (Erwin and Scott 1980, Erwin 1983a, Araujo et al. 2005) or other tropical parts of the world (Wagner 2000), not only because the vegetation type is different (cloud forest versus tropical forest) but also because this study had a lower sampling effort compared with those previous studies (Table 2). Moreover, Tlanchinol is located further north from the equator than the other sites studied, and insect species richness is reduced when further from the equator. Araujo et al. (2005) determined that the number of coleopteran species of evergreen forests in the Ecuadorian Chocó region is one of the highest worldwide. The authors, however, based their study on five locations. If we consider only one of these sampling sites (for example, in the Santiago sector at the location “La Tabla,” with 324 morphospecies), the results are similar with those reported here for Tlanchinol. Hence, we can conclude that the mountain cloud forest in this site can also be considered an ecosystem with high coleopteran diversity. Acknowledgments We thank these former students with a BSc in biology from the UAEH for their help during fieldwork: G. A. Canizal Ordaz, I. A. Rodríguez Márquez, and J. Islas Villaseñor. We would also like to thank these specialists for the identification of some specimens collected in this study: L. Delgado (Scarabaeoidea, Instituto de Ecología, A.C.), S. Zaragoza (Cantharoidea, Instituto de Biología, UNAM), N. Gutiérrez (Cerambycidae and Disteniidae, PhD student of the American Museum of Natural History, United States), D. K. Young (Scraptiidae and Tenebrionidae: Lagriini, University of Wisconsin, United States), M. Zurita (Elateridae, Instituto de Biología, UNAM), and E. Arriaga-Varela (Endomychidae, Department of Zoology, Faculty of Science, Charles University, Prague, Czech Republic). We thank Mary-Ann Hall for her English revision of the text and two anonymous reviewers for their useful comments made to the paper. References Cited Adis , J. , W. Parman , C. V. R. da Fonseca , and J. A. Rafael . 1997 . Knockdown efficiency of natural pyrethrum and survival rate of living arthropods obtained by canopy fogging in Central Amazonia, pp. 67 – 81 . In N. E. Stork , J. 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TI - Coleoptera in the Canopy of the Cloud Forest From Tlanchinol in the State of Hidalgo, Mexico
JF - Environmental Entomology
DO - 10.1093/ee/nvz059
DA - 2019-08-05
UR - https://www.deepdyve.com/lp/oxford-university-press/coleoptera-in-the-canopy-of-the-cloud-forest-from-tlanchinol-in-the-gNc7dmKOJa
SP - 1012
VL - 48
IS - 4
DP - DeepDyve
ER -