Neotrop Entomol DOI 10.1007/s13744-016-0367-0

ECOLOGY, BEHAVIOR AND BIONOMICS

Coleoptera Associated with Decaying Wood in a Tropical Deciduous Forest NZ MUÑOZ-LÓPEZ, AR ANDRÉS-HERNÁNDEZ, H CARRILLO-RUIZ, SP RIVAS-ARANCIBIA Escuela de Biología, Univ Autónoma de Puebla, Puebla, Mexico

Keywords Beetles, interactions, recycling, succession, xylem Correspondence AR Andrés-Hernández, Escuela de Biología, Univ Autónoma de Puebla, Boulevard. Valsequillo y Avenida San Claudio Edificio 112 A, Ciudad Universitaria Colonia Jardines de San Manuel, C. P. 72570 Puebla, Mexico; [email protected] Edited by Marcelo N Rossi – UNIFESP Received 18 February 2015 and accepted 17 January 2016 * Sociedade Entomológica do Brasil 2016

Abstract Coleoptera is the largest and diverse group of organisms, but few studies are dedicated to determine the diversity and feeding guilds of saproxylic Coleoptera. We demonstrate the diversity, abundance, feeding guilds, and succession process of Coleoptera associated with decaying wood in a tropical deciduous forest in the Mixteca Poblana, Mexico. Decaying wood was sampled and classified into four stages of decay, and the associated Coleoptera. The wood was identified according to their anatomy. Diversity was estimated using the Simpson index, while abundance was estimated using a KruskalWallis test; the association of Coleoptera with wood species and decay was assessed using canonical correspondence analysis. Decay wood stage I is the most abundant (51%), followed by stage III (21%). We collected 93 Coleoptera belonging to 14 families, 41 genera, and 44 species. The family Cerambycidae was the most abundant, with 29% of individuals, followed by Tenebrionidae with 27% and Carabidae with 13%. We recognized six feeding guilds. The greatest diversity of Coleoptera was recorded in decaying Acacia farnesiana and Bursera linanoe. Kruskal-Wallis analysis indicated that the abundance of Coleoptera varied according to the species and stage of decay of the wood. The canonical analysis showed that the species and stage of decay of wood determined the composition and community structure of Coleoptera.

Introduction Tropical deciduous forest habitat has been deteriorated in the last years causing a decrease in the number of woody plants and affecting many species that depend on them (Harmon et al 1995, Micó et al 2008). Although wood is not a widely available resource for living organisms, when it dies, it returns to the environment, passing through various stages of decay in which nutrients become available to different organisms. Thus, from a standing or freshly dead tree until its total disintegration, wood becomes a place and space for hundreds or thousands of species that succeed each other (primary and secondary succession; Maser & Trappe

1984, Grove 2002). Some species of Coleoptera depend on wood to complete their life cycle; they occupy different ecological niches through their life: at their larval stage, they can be saproxylophagous, while at their adult stage, they can be phyllophagous, anthophagous, or carpophagous, among others (Dajoz 1978, 2000, Beaver et al 1989, Dunn et al 1990, Morón 1985, 1986). Few studies have focused on this association. For example, Castillo & Morón (1992) recognized four stages of wood decay in a tropical rain forest of “Los Tuxtlas,” Veracruz, Mexico. She identified 4136 specimens (adults, larvae, teneral adults, and pupae) of Passalidae, recording a higher percentage in stages II and III of wood decay. The most abundant botanical families were Fabaceae, Moraceae,

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Tiliaceae, Boraginaceae, and Lauraceae. Furthermore, in a tropical rain forest of Cuetzalan del Progreso, Puebla, De la Piedra (unpublished observations 2004) recognized a total of 307 individuals of adult Coleoptera belonging to 14 families of Coleoptera, mostly associated with wood in stage of decay IV. He also recognized six feeding guilds: saproxylic, mycetophagous, phytophagous, predators, necrophagous, and detritivores. Some studies have reported an association between certain Coleoptera guilds according to the stage of wood decay. Lanuza-Garay & Vargas-Cusatti (2011) mentioned that when wood decay started (stage I), they observed Coleoptera with chewing mouthparts that allowed them to gnaw very hard pieces of wood, which also possess enzymatic material or associated microorganisms in their digestive tracts to degrade cellulose. They also reported that these species favored the decaying wood colonization by secondary saproxylic organisms. These organisms continue to thrive in later stages of decay and wood exploitation (stages II, III, and IV); at the last stage, they are often progressively replaced by other species of Coleoptera (Morón 1986, Beaver et al 1989, Castillo & Morón 1992, Castillo & Reyes-Castillo 2003, Méndez 2009). Furthermore, Míss & Deloya (2007) reported that as wood decay progressed, they found larvae and adults of Coleoptera of the families Curculionidae and Carabidae, but especially of Passalidae, Tenebrionidae, and Cerambycidae. In addition, it is known that the diversity of xylophagous Coleoptera depends mainly on the abundance of dead trees in some stage of decay, since the phloem stores starches and sugars (Savely 1939, Stevens 1986). The association of Coleoptera with decayed wood is so intense that nearly 90 species from the known 166 families of Coleoptera were recorded exploiting dead wood (Lawrence 1991, Delgado & Pedraza 2002). Therefore, Coleoptera and dead wood are two elements that perform vital functions in jungles and forests, contributing to the flow of energy through the different trophic chains (Price 1997, Camero 1999). In Mexico, the tropical deciduous forest is a very rich ecosystem suffering from significant deforestation, in which there are few studies of saproxylic Coleoptera despite their importance to these ecosystems. In this study, we aimed to determine the diversity, abundance, feeding guilds, and the succession process showed by Coleoptera associated with decaying wood in a tropical deciduous forest of the Mixteca Poblana, Mexico, under the hypothesis that these attributes will change according to the species and stage of wood decay, and this two conditions will determine the composition and Coleoptera community structure.

Material and Methods Study area This work was carried out in the “Rancho El Salado” community, which corresponds to the municipality of Jolalpan, Puebla, Mexico, located at the following orthogonal coordinates: long. −98°95′80″N and lat. 18°33′72″O. It has an area of 3125 ha of properties, under a land tenure regime, and is included in the region called Mixteca Poblana (INEGI 2010, Fig 1). The region has a warm subhumid climate with summer rains, with an average annual temperature of 25.6°C and annual rainfall of 852.2 mm, concentrated in the summer. The predominant vegetation is tropical deciduous forest, located between 1000 and 1800 m asl. Collection and identification of species In order to obtain wood and Coleoptera, samples were collected for 3 days every month from February to November 2010. Sampling was carried out from 8:00 am to 8:00 pm following 10 trails of 2.5-km long (La mina, La presa, El rincón, Mal paso, El bordo, Guacamayas, Agua Zarca, Las golondrinas, La Tirolesa, and Alseseca). We examined stumps and fallen trees (in the field) and established stages of wood decay according to Castillo & Reyes-Castillo (2003) and classified the successional stage of exploitation of Coleoptera within the logs and under the bark as stages of decay I, II, III, and IV. The stage IV represents the most advanced stage of wood decay. Taxonomic wood determination was made using samples of 4 cm3; wood samples in stages of decay I, II, and III were fixed in glycerin-ethanol-water solution (1:1:1) and subjected to conventional microtechniques for performing histological sections using a sliding microtome (Brand pfm; Ruzin 1999). Wood samples in the most advanced stage of decay (stage IV) were embedded in paraffin for cutting with a rotary microtome (Leica RM2125 RT at 25 μm). We made transversal, longitudinal, and radial cuts of all samples and stained them with safranin and fast green. All sections were mounted in Hycel synthetic resin, and wood samples were determined to species level following the recommendations and criteria of the IAWA Committee database (2006). Only adult Coleoptera were collected directly from decaying wood and placed in a lethal camera with ethyl acetate (Márquez-Luna 2005). The collected Coleoptera were mounted and identified using dichotomous keys (Dillon & Dillon 1972, Morón & Terrón 1988, Yanega 1996, Ross et al 2002, Lingafelter 2007, Bousquet 2010, Morón et al 2013). The Coleoptera were deposited in the scientific collection of the Escuela de Biología de la Benemérita Universidad Autónoma de Puebla, México (Supplementary Online Material S1).

Coleoptera Associated with Decaying Wood

Fig 1 Geographical location of the UMA Rancho El Salado, Jolalpan, Puebla.

Data analysis The Simpson diversity index was obtained for each wood species and for each stage of decay. Kruskal-Wallis analysis was used to compare the diversities and relative abundances of Coleoptera (Zar 1999) among wood species and among stages of wood decay. This analysis was performed using the statistical package NCSS 2000 (Hintze 2008). To analyze the dynamics of the community of Coleoptera for each stage of decay and species of wood, we performed a canonical correspondence analysis (CCA) using the statistical software MVSP v. 3.12c (Kovach 2004).

Results Identification of Coleoptera, stages of decay, and wood species We found 27 logs in different stages of decay (I, II, III, and IV). We found a total of 93 adult specimens belonging to 14 families, 41 genera, and 44 species. The family Cerambycidae was the best one represented with 29%; the least abundant families were Staphylinidae, Bostrichidae, Coccinellidae, and Dermestidae with 1% each (Table 1). The most abundant species were Aethecerinus sp., Trachyderes mandibularis Dupont, and Stenapsis verticalis Audinet-Serville (Table 1). Most species (45%) were saproxylophagous (Cerambycidae, Brentidae, Buprestidae, Elateridae, Trogossitidae, Bostrichidae), while detritivorous species (Staphylinidae) were the least abundant with 1% (Table 1). We identified six botanical species belonging to three families. The Burseraceae Bursera linanoe (two

samples) and Bursera bipinnata, the Fabaceae Acacia farnesiana, Leucaena esculenta, and Prosopis juliflora, and the Moraceae Ficus sp. B. linanoe were found in stage of decay II, with low humidity and retaining the bark in all cases, and were exploited by Nothopleurus madericus (Skiles) (collected in heartwood), Brentus anchorago (Linnaeus), Geropa sp. (saproxylophagous), Zopherus sp., Neatus tenebroides (Beauvois) (mycophagous), collected in the sapwood, and Phileurus sp. (predator) in the outermost part of the sapwood (Figs 2a and 3a). Logs of B. bipinnata were in stage of decay III (no bark available and very little moisture if any) were associated with Aethecerinus sp., Chrysobothris sexsignata (Say) (saproxylophagous), Lobometopon sp., and Hymenorus sp. (mycophagous) found in holes near the surface of the logs, and Poecilus lucublandus (Say) in the sapwood (predator; Figs 2b and 3b). Logs of A. farnesiana were found in stage I of decay (bark still available, with a high humidity and an intense aroma of resin) and were associated with the saproxylophages Aethecerinus sp., S. verticalis Audinet-Serville, T. mandibularis Dupont, Placosterus difficilis (Chevrolat), Chalcolepidius limbatus (Eschsch), and the mycophagous Lobometopon sp. (Figs 2c and 3c). Leucaena esculenta logs were in stage of decay II (bark easily comes off) and were exploited by the mycophage Platydema sp. and the predator Myzia sp. (Figs 2d and 3d). Prosopis juliflora was in stage of decay III (absence of bark, with soft wood, no moisture, and with galleries in the heartwood) and associated with the mycophage Platydema ruficorne (Sturm), the predators Lebia sp. and Saprinus sp., and the saproxylophages Airora cylindrica (Serville), Tenebroides sp., and B. anchorago (Figs 2e and 3e). Ficus sp. samples were in stage of decay IV (logs had no bark, with very soft and rotten wood of spongy consistency and saturated with water) and associated with the predators Chlaenius dajuensis Kirschenhofer, Tetracha carolina (Linnaeus), and Calosoma sp. and the detritivorous Homaeotarsus parallelus (Casey) (Figs 2f and 3f).

Association between Coleoptera and stages of wood decay The Kruskal-Wallis analysis showed that the abundance of insects was significantly different (p < 0.05) among stages of decay I, II, and IV (Fig 4a), and their diversity differed from that of stage III (p < 0.05) compared with stage III (Fig 4b). Furthermore, the CCA showed that stages of decay I and III were associated with a greater number of species of Coleoptera compared with stages II and IV (Fig 4c). The first ordination axis explained 59.3% of the total variation, while the second axis 32.9%.

Muñoz-López et al. Table 1

Families, species, and feeding guilds of adult Coleoptera.

Families

Species

Feeding guilds

Families

Brentidae

Brentus anchorago (Linnaeus) (2)

Saproxylophagous Cerambycidae Aethecerinus sp. (10)

Feeding guilds Saproxylophagous

Geropa sp.(1)

Saproxylophagous

Nothopleurus madericus (Skiles) (3)

Saproxylophagous Saproxylophagous

Bostrichidae

Amphicerus cornutus (Pallas) (2)

Buprestidae

Chrysobothris sexsignata (Say) (1)

Saproxylophagous

Placosternus difficilis (Chevrolat) (1)

Dicerca lurida (Fabricius) (3)

Saproxylophagous

Stenapsis verticalis Audinet-Serville (8) Saproxylophagous

Anisodactylus sp. (2)

Predator

Trachyderes mandibularis Dupont (10)

Saproxylophagous

Bembidion sp. (2)

Predator

Bradycellus sp. (1)

Predator

Calosoma sp. (1)

Predator

Predator

Carabidae

Carabidae

Saproxylophagous

Species

Coccinelidae

Myzia sp. (1)

Dermestidae

Attagenus sp. (1)

Phytophagous

Elateridae

Chalcolepidius limbatus

Phytophagous

Chlaenius dajuensis Kirschenhofer (1)

Predator

Harpalus sp. (2)

Predator

Chalcolepidius viridipilis

Lebia sp. (1)

Predator

(Say) (1)

Poecilus lucublandus

Predator

(Eschsch) (2)

Histeridae

(Say) (1)

Melolonthinae Cotinis mutabilis Gory & Percheron (1) Diplotaxis simplex Blanchard (2)

Predator

(Palisot de Beauvois) (2)

Tetracha carolina (Linnaeus) (1)

Epierus regularis

Phytophagous

Saprinus sp. (1) Predator

Predator

Tenebrionidae Neatus tenebroides (Beauvois) (2)

Mycophagous

Platydema sp. (1)

Mycophagous

Platydema ruficorne

Mycophagous

Melliphagous Phytophagous

(Sturm) (2) Hologymnetis cinerea Gory & Percheron (2) Melliphagous Phileurus sp. (2)

Predator

Nitidulidae

Pocadius sp. (1)

Phytophagous

Staphylinidae

Homaeotarsus parallelus (Casey) (1)

Detritivorous

Tenebrionidae Bitoma sp. (1)

Mycophagous

Glyptasida sp. (1)

Mycophagous

Hymenorus sp. (1)

Mycophagous

Liodema sp. (2)

Mycophagous

Lobometopon sp. (4)

Mycophagous

Trogossitidae

Philolithus sp. (2)

Mycophagous

Tenebrionini sp. (1)

Phytophagous

Zopherus sp. (1)

Mycophagous

Airora cylindrica (Serville) (1)

Saproxylophagous

Tenebroides sp. (3)

Saproxylophagous

Tenebroides corticalis (Melsheimer) (2) Saproxylophagous

In parenthesis are the number of individuals of each species.

Comparison of the community of Coleoptera among wood species Estimated abundances of Coleoptera were significantly different (Kruskal-Wallis test, p < 0.05) only between A. farnesiana and B. linanoe (Fig 5a). When comparing the diversity of Coleoptera between wood species (Fig 5b), both species of wood had the highest diversity of Coleoptera (p < 0.05). The CCA used to compare the association of Coleoptera with wood species explained 40.9% of the total variation in the first axis, while and 35.5% in the second axis. Thus, wood samples from B. linanoe were associated with nine species, while B. bipinnata with three species of Coleoptera. For samples from Fabaceae, A. farnesiana was associated with 11

species, Ficus with six species, L. esculenta with two species, and P. juliflora with a single coleopteran, B. anchorago (Fig 5c).

Fig 2 a Bursera linanoe stage of wood decay II: (a1) diffuse porosity, (a2)„ ray of 1–3 cells wide, and (a3) heterogeneous ray. b Bursera bipinnata stage of decay III: (b1) diffuse porosity, (b2) ray of 1–4 cells wide, and (b3) heterogeneous ray, quadratic cells. c Acacia farnesiana stage of decay I: (c1) diffuse porosity, confluent parenchyma, (c2) ray of 4–10 cells wide, and (c3) heterogeneous ray, prismatic crystals. d Leucaena esculenta stage of decay II: (d1) diffuse porosity, (d2) ray of 4–10 cells wide, and (d3) heterogeneous ray, prismatic crystals. e Prosopis juliflora stage of decay III: (e1) diffuse porosity, (e2) ray of 1–3 cells wide, and (e3) heterogeneous ray, confluent parenchyma. f Ficus stage of decay IV: (f1) semi-ring porosity, (f2) ray of 1–4 cells wide, and (f3) heterogeneous ray, banded parenchyma, parenchyma with mucilage.

Coleoptera Associated with Decaying Wood

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Fig 3 Some species of Coleoptera found in different species of wood.

Coleoptera Associated with Decaying Wood

Fig 4 a Comparison (Kruskal-Wallis) between the stages of wood decay according to the abundance of associated Coleoptera. Values greater than 1.9600 were considered significant. b Multiple comparison (Simpson index) of wood species with respect to the abundance of Coleoptera that benefit from them. c Canonical correspondence analysis (CCA). Preferences of Coleoptera for stages of wood decay. The triangles represent species of Coleoptera. The arrows are environmental variables (stages of decay).

Discussion Stages of wood decay We report significant differences in the abundance of Coleoptera among stages of wood in stages of decay I, II, and IV probably because each stage decay wood has

different conditions of moisture and nutrients in the decomposition process. Moreover, the conditions that allowed Coleoptera to use the logs and satisfy their food or shelter needs also changed according to the changes in wood hardness and moisture; these conditions were no longer present in stage of decay III (Fig 6). The stage of decay I was the most exploited

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Fig 5 a Comparison (Kruskal-Wallis) between wood species according to the abundance of associated Coleoptera. Values greater than 1.9600 were considered significant. b Multiple comparison (Simpson index) of wood species and abundance of Coleoptera. c Canonical correspondence analysis (CCA). Preferences of Coleoptera for different wood species. The triangles represent species of Coleoptera. The arrows are environmental variables (species of wood).

according to the abundance of Coleoptera associated, but is contradictory to other reports in which higher abundances were reported in more advanced stages of decay (Castillo & Morón 1992). These discrepancies may be related with the stage of colonization of the decaying wood, the influence of the climate, the type of vegetation, moisture content, and the conservation of the study area. All other studies were conducted in a tropical rain forest, an environment with different

characteristics from the tropical deciduous forest in which our study took place. In our case, logs in stage of decay I demonstrated to be more suitable for larva and adult coleopterans, as logs still had bark and the wood was consistent and moist. These are important characteristics because wood bark helps in maintaining moisture inside the logs, and at this stage, the wood is still healthy, which favors the attack by xylophagous species (Lanuza-Garay & Vargas-Cusatti 2011).

Coleoptera Associated with Decaying Wood

Fig 6 Succession of Coleoptera during exploitation of wood. The bars indicate the abundance of each species. Primary and secondary successions are indicated, as well as the stage of wood decay.

Abundance and diversity of Coleoptera We did not find Passalidae among the most abundant families of coleopterans exploiting decaying wood as reported by others (Míss & Deloya 2007), and differences in the most abundant families may result from an effect of the sampling period. Our samplings identified six feeding guilds, with saproxylophages as the most abundant as consistently reported in the literature of De la Piedra (unpublished observations 2004) and Míss & Deloya (2007). Very few studies have identified species according to their presence in the successive stages of the decay process. Méndez (2009) suggested wood decay starts with the colonization with primary saproxylics, and we reported several primary saproxylic species, such as Aethecerinus sp., T. mandibularis, S. verticalis, and N. madericus with the stage I of wood decay. We were able to establish a sequence of succession (Table 1, Fig 6), having the secondary saproxylic species Geropa sp., P. difficilis, Amphicerus cornutus (Pallas), B. anchorago, Tenebroides sp., A. cylindrica, Tenebroides corticalis (Melsheimer), and Homaeotarsus parallelus (Casey). The secondary saproxylics were followed by phytophages, as C. limbatus and Attagenus sp., which were in turn succeeded by the mycophages Lobometopon sp.,

Liodema sp., Philolithus sp., P. ruficorne (Sturm), Zopherus sp., Glyptasida sp., Hymenorus sp., Neatus tenebrioides (Beauvois), Platydema sp., and Bitoma sp. And at the end of the process of exploitation of decaying wood, predatory coleopterans become available, such as Anisodactylus sp., Harpalus sp., Lebia sp., Calosoma sp., T. carolina (Linnaeus), C. dajuensis Kirschenhofer, Saprinus sp., Epierus regularis (Palisot de Beauvois), and Myzia sp., and finally followed by scavenger species (Phileurus sp. and Pocadius sp.). These coleopterans were eventually replaced by soil organisms (collembola, earthworms, nematodes, isoptera, and acari). We found two species Melliphagous. However, they are not related with wood. According to the Kruskal-Wallis test and canonical correspondence analysis (CCA), the species A. farnesiana in stage of decay I and B. linanoe in stage II were the only ones that had significant differences in the abundance and diversity of associated Coleoptera. According to Dunn et al. (1990), some larvae and adult of Coleoptera have a marked preference for certain tree species. We observed that A. farnesiana and B. linanoe had a resin with a very intense aroma, which might have functioned as an attractant. Our analysis confirmed that the composition and structure of the Coleoptera community varied according to the

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species and stage of decay of the wood in studied ecosystem. However, the level of conservation of the study area can modify the structure of the coleopteran community. Acknowledgments The development of this work was possible thanks to the facilities provided by Dr. Jorge Alejandro Cebada Ruiz, who arranged transportation for field trips to the study site; we thank also the support and facilities provided by the members of UMA of Rancho El Salado and also the Laboratorio de Biología Vegetal y Micología and the Laboratorio de Entomología de la Escuela de Biología of the Benemérita Universidad Autónoma de Puebla. We thank BecaNet Superior for the social service scholarship through the Programa de Fortalecimiento al Programa de Becas 2010 (N2U588) CCP1_20101208 459. Electronic supplementary material The online version of this article (doi:10.1007/s13744-016-0367-0) contains supplementary material, which is available to authorized users.

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