DECOMPOSITION AND BEETLES IN THE MAULINOR FeOvRisEtaS TChilena de Historia Nat1u0ra7l 77: 107-120, 2004 Dung decomposition and associated beetles in a fragmented temperate forest Descomposición de heces y sus coleópteros asociados en un bosque templado fragmentado MARCELA A. BUSTAMANTE-SÁNCHEZ1, AUDREY A. GREZ2 & JAVIER A. SIMONETTI1 1Departamento de Ciencias Ecológicas, Facultad de Ciencias, Universidad de Chile, Casilla 653, Santiago, Chile; e-mail: [email protected] 2Facultad de Ciencias Veterinarias y Pecuarias, Universidad de Chile, Casilla 2, Correo 15, La Granja, Santiago, Chile ABSTRACT Habitat fragmentation may result in changes in species number and population abundance among habitats that differ in area, structure, or edge characteristics. These changes, in turn, may result in alterations in ecosystem process such as decomposition of organic matter. Through an experimental approach, we compared the beetles assemblages associated with dung and decomposition of cow feces in a continuous portion of Maulino forest, forest fragments and in pine plantations that surround this forest and forest remnants. Abundance and richness of dung-associated beetles were lower in forest fragments compared to the continuous forest and pine plantations. However, dung decomposition was similar in these three habitats. Beetle abundance, species richness and decomposition did not vary along edges of forest fragments and pine plantations, but beetle abundance and decomposition rate varied on the border compared to the interior of the continuous forest. Thus, although beetle assemblage changes across the fragmented landscape, these variations in species richness and abundance did not translate into alterations of an ecosystem process such as dung-decomposition, as occurs in tropical forests. The beetle assemblage at pine plantations comprises only native species and dung decomposition was similar in both fragments and continuous forest. Therefore, pine plantations maintain at least partially the structural and functional biodiversity of the native fauna, connecting the native remnants throughout the landscape, a crucial factor in biodiversity conservation. Key words: temperate forest, fragmentation, insects, decomposition. RESUMEN La fragmentación del hábitat puede cambiar el número de especies y la abundancia poblacional entre hábitats que difieren en área, estructura o en las características del borde. Estos cambios, a su vez, pueden alterar procesos ecosistémicos como la descomposición de la materia orgánica. A través de una aproximación experi- mental, comparamos un ensamble de coleópteros asociados a heces y la descomposición de estas en una porción continua de bosque Maulino, fragmentos de bosque y en la matriz de plantaciones de pino que rodean estos remanentes de bosque. La abundancia y riqueza de coleópteros asociados a las heces fueron más bajas en los fragmentos de bosque que en el bosque continuo y en las plantaciones de pino. Sin embargo, la descomposición de las heces fue similar entre los tres hábitats. La abundancia de coleópteros, riqueza de especies y descomposición no variaron en los bordes de los fragmentos ni en los bordes de las plantaciones de pino, sin embargo, la abundancia y descomposición variaron en el borde en comparación al centro del bosque continuo. Así, aunque el ensamble de coleópteros cambia a través de este paisaje fragmentado, estos cambios no se tradujeron en alteraciones en procesos ecosistémicos como la descomposición de heces, como ocurre en bosques tropicales. El ensamble de coleópteros en las plantaciones de pino solo tuvo especies nativas y la descomposición de heces fue similar a la de los fragmentos y a la del bosque continuo. Por lo tanto, estas plantaciones de pino mantienen por lo menos parcialmente la biodiversidad estructural y funcional de la fauna nativa, conectando remanentes de bosque nativo a través del paisaje, un factor crucial en la conservación de la biodiversidad. Palabras clave: bosque templado, fragmentación, insectos, descomposición. 108 BUSTAMANTE-SÁNCHEZ ET AL. INTRODUCTION pine plantations (Pinus radiata D. Don) (Bustamante & Castor 1998, Grez et al. 1998). Land use changes are a major threat to In this forest, ground-dwelling beetles are more biodiversity, particularly in temperate forests. diverse and abundant in small than in large In fact, deforestation and forest fragmentation forest fragments, sharply contrasting with the have increased worldwide, and are a significant effects of fragmentation in tropical forests (Grez menace to the compositional, structural and in press). Some of these beetles might be functional biodiversity (Chapin et al. 2000, associated with the decomposition of dead Sala et al. 2000). Coupled to a reduction and organic matter. Therefore, dung decomposition isolation of the remnant forest area, could be higher in forest fragments, similar to an fragmentation also increases the proportion of increased granivory and nest predation rate due edge habitat with decreasing fragment area, to a more abundant consumer assemblages modifying the microclimatic conditions in the thriving in these forest remnants (Donoso et al. borders and the dispersal of organisms between 2003, Vergara & Simonetti 2003). Here, we used neighboring fragments and among isolated an experimental approach to analyze changes in fragments. These changes might modify the ecological processes in the Maulino forest distribution, abundance, and species richness of brought about by forest fragmentation, focusing several groups of insects at both within each on dung decomposition. Regarding beetles fragment and the landscape level (Didham et al. associated with dung and the decomposition 1998, Golden & Crist 2000). In turn, these process, we addressed the four following compositional and structural biodiversity questions: (1) How does species composition of changes might translate into altered ecological these beetles change with forest fragmentation? processes such as reduced rates of organic (2) Do the species richness and abundance of matter decomposition (Didham et al. 1996). these beetles and dung decomposition increase Decomposition of dead organic matter, such in forest fragments? (3) Is there an edge effect as carcasses, leaf litter or dung, is a dynamic on the beetles associated with dung and on dung process that involves a complex array of decomposition? (4) Are the changes in the physical, chemical and biological interactions beetles community structure associated with that complete the biogeochemical nutrient changes in dung decomposition? Furthermore, in cycles. This process is largely performed by order to analyze changes in a broader microbes, but soil fauna have an important perspective, we determine if the responses of the stimulatory role. Insects participate in the beetles and dung decomposition are similar in decomposition processes, breaking apart or tropical and temperate fragmented forest. consuming organic matter, or through the consumption of other organisms associated with such organic matter. Animal consumption MATERIAL AND METHODS enhances decomposition rates (Peterson & Luxton 1982, Packham et al. 1992, Robertson Study area & Paul 2000). In tropical forests, species richness and abundance of beetles associated The study was carried out in the Maulino forest, with dung decomposition are generally which harbors a suite of endemic tree species, depressed in small forest fragments (Klein including Gomortega keule (Mol.) Baillon, the 1989, Estrada 2002, Andresen 2003). Such a single representative of the primitive family decrease translates into reduced decomposition Gomortegaceae. The dominant species is rates (Klein 1989, Andresen 2003). However, Nothofagus glauca (Phil.) Krasser (Fagaceae), despite the paramount significance of dung which coexists with many endangered endemic decomposition to nutrient cycling and species such as Nothofagus alessandrii Esp. associated biogeochemical processes, few (Fagaceae), Pitavia punctata (R. et P.) Mol. studies have addressed the effect of habitat (Rutaceae) and G. keule. This forest has been fragmentation on this process and none of them intensively deforested and fragmented, initially have been carried out in temperate forests. due to increased fuel wood production and land Like tropical ones, temperate forests in clearing for cultivation, and more recently, due southern Chile have been extensively to its replacement by plantations of commercial fragmented (San Martín & Donoso 1997). The P. radiata, associated to the expansion of timber Maulino forest, a unique temperate ecosystem production and exports (Lara et al. 1996). harboring several distinctive and endangered The study was conducted in a continuous species, is currently reduced to a mosaic of forest located in the coast of central Chile, in isolated fragments surrounded by Monterrey three adjacent forest fragments and in three DECOMPOSITION AND BEETLES IN THE MAULINO FOREST 109 pine plantations that surround the native forest. experimental area. One of these piles was The continuous forest includes the Reserva removed from each group after nine (t ), 30 (t ) 1 2 Nacional Los Queules (35º59’19’’S, and 58 (t ) days after the beginning of the 3 72º41’15”W), one of the few areas allocated to experiment. Following Klein (1989), we used preserve the Maulino forest in Chile. This cow dung as experimental substrate. This reserve covers 145 ha but is embedded in 600 experimental design used here allows us to ha of continuous forest. Forest fragments are compare our results with those of Klein (1989) remnants of native forest of 3.4, 3.0 and 2.3 ha. regarding beetle abundance and dung Both continuous forest and forest fragments decomposition in a tropical forest. have a similar vegetation dominated by N. glauca, N. obliqua (Mirb.) Oerst, Cryptocarya Laboratory work alba (Mol.) Looser, Gevuina avellana Mol. (San Martín & Donoso 1997). Pine plantations Beetles were manually removed from the dung are 20 years old, with an abundant understory piles, preserved in alcohol and identified of native trees dominated by N. glauca and following taxonomic keys or by comparison Aristotelia chilensis (Mol.) Stuntz and exotic with reference collections from the Museo shrubs as Teline monspessulana (L.) K. Koch Nacional de Historia Natural, Santiago. After and Rosa moschata Hermm. removing all beetle fauna, disintegrated dung piles were dried at 100ºC for five days and Experimental design weighted to estimate dung decomposition. Decomposition involves the active or passive Fieldwork was carried out during the summer remove of dead organic matter, performed by from 14 November 2001 to 11 January 2002. biotic and abiotic agents. Typically, it is Species richness and abundance of ground- measured as weight loss; the usual strategy for dwelling beetles are higher in summer assessing weight loss is to set a known quantity (December-March) than in spring (September- of material at a specific location and then December, Grez et al. 2003). periodically evaluate the weight loss (Robertson We placed fresh dung piles in six different & Paul 2000). Consequently, we evaluated dung locations: the border and interior of continuous decomposition as the dry weight loss of the dung forest, forest fragments and pine plantations. piles in every sampling time (t , t and t ). As an 1 2 3 The dung piles consisted of cow dung collected initial dry weight, we used the average initial one day before the beginning of the experiment dry weight of 30 intact dung piles. from a farm where animals were treated neither with antibiotics nor with antiparasites, avoiding Data analysis possible toxic effects on the insects associated with dung (Floate 1998). We used 100 ml We calculated the Morisita’s index of similarity metallic containers to obtain dung piles of and built a phenogram to compare the beetle equal shape and size. Piles were 2 cm high, 8 species assemblages among the six locations: cm in diameter with an initial dry weight of the interior and borders of the three kinds of 17.6 ± 0.18 mg (n = 30, mean ± 1 SE). Each habitats. This index considers both the species fresh dung pile was set up on the ground over a composition and the proportional abundance of 20 x 20 cm plastic mesh (9 mm2 of sieve) to the species in each location. The phenogram avoid the loss of dung and an eventual was built using the UPGMA clustering overestimation of dung decomposition. algorithm (Sneath & Sokal 1973). The We considered the first 10 m from the edge statistical significance of the observed clusters toward the interior of the forest or toward the was determined through a randomization test interior of pine plantations as their borders. We (Manly 1998). also considered as the interior of the continuous Differences in the number of beetle species, forest a place located at least 100 m from the number of individuals and dung decomposition nearest edge, because the most striking edge were tested using a two-way repeated measures effects do not penetrate more than 50-100 m ANOVA, with habitat (i.e., continuous forest, inward (Laurance et al. 2002). In the forest forest fragments and pine plantations) and fragments, the dung piles were installed in its location (i.e., interior and border) as the factors geometric center and on the borders. and sampling time as the repeated factor. Given Groups of three dung piles (1 m apart) were that the continuous forest is not replicable, we spaced at least 10 m apart in linear transects on considered each dung pile as the experimental the border and in the interior of each habitat. In unit. Species richness, abundance and total, we distributed 540 dung piles in the decomposition rate at contiguous dung pile 110 BUSTAMANTE-SÁNCHEZ ET AL. groups are statistically independent at all times RESULTS (t -t ) and settings (border-interior, continuous 1 3 forest, forest fragments, and pine plantations; The beetle fauna Mantel test critical value > 0.105, P < 0.05 for all cases). Therefore, we can use each dung pile as a We collected 1,730 beetles belonging to 15 legitimate replicate. We used the Greenhouse- families and 36 species, all of them natives. Of Geisser adjusted probabilities given that data did these, 832 individuals of 19 species were not satisfy the sphericity assumption (Scheiner & recorded in the continuous forest, 639 Gurevitch 1993). Statistical analyses were done individuals of 16 species in the pine plantations using Statistica (StatSoft, Inc. 2000), and Pop and 259 individuals of 22 species in the forest Tools software (Hood 2003). fragments (Table 1). Staphylinidae was the TABLE 1 Total number of beetles found in the continuous forest (CF), pine plantation (PP) and forest fragments (FF). The trophic level is indicated at family level (Fam): C = coprophagous, D = detritivore, F = fungivore, H = herbivore, P = predator (Strong et al. 1984, Borror et al. 1989, Saiz et al. 1989, Lawrence 1991, Lawrence & Britton 1991, Peña 1992, Artigas 1994) Número total de coleópteros encontrados en el bosque continuo (CF), plantaciones de pino (PP) y fragmentos de bosque (FF). Se indica el nivel trófico a nivel de familia (Fam): C = coprófago, D = detritívoro, F = fungívoro, H = herbívoro, P = depredador (Strong et al. 1984, Borror et al. 1989, Saiz et al. 1989, Lawrence 1991, Lawrence & Britton 1991, Peña 1992, Artigas 1994) Family Species Total number of individuals CF PP FF Trophic level Acanthoceridae Martinezostes asper (Phil.) 3 0 0 Fam: D-F Biphyllidae Diplocoelus sp. 0 0 2 ¿? Carabidae Cyanotarus andinus (Germ.) 0 0 1 Fam: P Carabidae Euproctinus fasciatus (Solier) 1 0 0 Fam: P Ciidae Cis sp. 23 0 5 Fam: F Coleoptera Coleoptera sp.1 0 1 0 - Coleoptera Coleoptera sp. 2 1 3 1 - Crysomelidae Crysomelidae sp. 1 0 0 7 Fam: H Crysomelidae Psathyrocerus sp. 0 0 1 Fam: H Histeridae Phelister vibius (Marseul) 1 0 0 Fam: D-P Lathridiidae Aridius sp. 0 1 1 Fam: F Leiodidae Eupelates sp. 0 0 1 Fam: F-D Leiodidae Leiodidae sp.1 1 1 0 Fam: F-D Leiodidae Leiodidae sp.2 2 0 0 Fam: F-D Melyridae Arthrobachus sp. 60 99 25 Fam: P-H Nitidulidae Carpophilus sp. 1 0 0 Fam: D Ptiliidae Acrotrichis chilensis (F. & G.) 181 86 37 Fam: F Ptinidae Ptinus sp. 1 162 46 31 Fam: D Ptinidae Ptinus sp. 2 0 0 1 Fam: D Staphylinidae Atheta obscuripennis (Solier) 343 174 41 Fam: P-C Staphylinidae Baeocera sp. 0 1 0 Fam: P-C Staphylinidae Bolitobius unicolor (F. & G.) 0 1 0 Fam: P-C Staphylinidae Conosomus sp. 1 0 1 0 Fam: P-C Staphylinidae Conosomus sp. 2 1 0 0 Fam: P-C Staphylinidae Conosomus sp. 3 0 1 0 Fam: P-C Staphylinidae Dasymera sp. 0 70 2 Fam: P-C Staphylinidae Kainolinus socius (Ful.) 0 0 2 Fam: P-C Staphylinidae Leptoglossula sculpticollis (Flauvel) 1 0 15 Fam: P-C Staphylinidae Loncovilius discoideus (F. & G.) 1 0 1 Fam: P-C Staphylinidae Omaliopsis russata (F. & G.) 0 0 1 Fam: P-C Staphylinidae Plesiomalota merula (Flauvel) 39 21 73 Fam: P-C Staphylinidae Spanioda spectrum (Flauvel) 7 0 1 Fam: P-C Staphylinidae Spanioda sp. 0 10 0 Fam: P-C Tenebrionidae Allecula sp. 1 0 0 Fam: H Tenebrionidae Apocrypha sp. 0 0 1 Fam: H Zopheridae Namunaria angustata (Solier) 3 123 9 Fam: F Total number of individuals 832 639 259 Total number of species 19 16 22 DECOMPOSITION AND BEETLES IN THE MAULINO FOREST 111 most speciose family (13 species), whereas the border of the continuous forest than its average other families were represented by only one to abundance in all other habitats, while N. three species (Table 1). The most abundant angustata was 7.5 times more abundant in the families (i.e., with species with more than 40 border of the pine plantations. individuals) were Staphylinidae, Ptiliidae, Species richness (number of species mg-1 of Ptinidae, Zopheridae and Melyridae. Two of dry dung) varied through habitat and time. At these families, Staphylinidae and Ptiliidae, t , species richness was 2.5 times higher in the 1 were more abundant at t , decreasing continuous forest than in the forest fragments 1 progressively until their disappearance at t . (0.15 ± 0.01 versus 0.06 ± 0.01 species; mean ± 3 Ptinidae, Zopheridae and Melyridae presented 1 SE), whereas pine plantations had an the opposite trend, with scarce or no abundance intermediate species richness (0.11 ± 0.01 at t but increasing numbers through time. species; mean ± 1 SE). These differences 1 disappeared over time (Fig. 2). Species richness Species similarity and species richness of beetles was statistically similar in the edges and interior of the three habitats (Table 2). Beetle assemblages were statistically dissimilar only on the borders of both of the continuous Abundance of beetles forest and pine plantations (Fig. 1). These differences were accounted for two species that The highest number of individuals occurred dominated each one of these habitats. Ptinus after nine days (t ). At t , the most abundant 1 1 sp. 1 was nine times more abundant on the species were Atheta obscuripennis (n = 539) Fig. 1: Phenogram resulting from application of UPGMA clustering algorithm (Sneath & Sokal 1973) to the similitary values of Morisita’s index among the six locations (CF = continuous forest, PP = pine plantations and FF = forest fragments, b = border, i = interior). The perpendicular dotted line on the similarity axis represents the critical value (for α = 0.05) obtained from the null distribution (n = 15,000 iterations). Dendrograma resultante de la aplicación del algoritmo de agrupación UPGMA (Sneath & Sokal 1973) a los valores de similitud calculados con el índice de Morisita entre los seis sitios (CF = bosque continuo, PP = plantaciones de pino, FF = fragmentos de bosque, b = borde y i = centro). La línea punteada perpendicular a eje de similitud representa el valor crítico (para un α = 0,05) obtenido a partir de la distribución nula (n = 15.000 iteraciones). 112 BUSTAMANTE-SÁNCHEZ ET AL. Fig. 2: Species richness of beetles associated with dung on the border and interior of each habitat in every sampling time (mean ± 1 SE). Different letters represent significant statistical differences (P < 0.05) (CF = continuous forest, PP = pine plantations, and FF = forest fragments). Riqueza de especies de coleópteros asociados a las heces en los bordes y centros de cada hábitat para cada una de las fechas de muestreo (media ± 1 EE). Letras distintas representan diferencias estadísticamente significativas (P < 0,05) (CF = bosque continuo, PP = plantaciones de pino y FF = fragmentos de bosque). TABLE 2 Results of repeated measures ANOVA for the effect of habitat (continuous forest, forest fragments and pine plantations), location within each habitat (border, interior) and sampling time (9, 30 and 58 days) on beetle species richness (number of species /mg of dry dung). Letter P* is the non adjusted probability, P adj. is the adjusted probability based on the epsilon value of the Greenhouse-Geisser estimator Resultados del ANDEVA de medidas repetidas para el efecto del hábitat (bosque continuo, fragmentos de bosque y plantaciones de pino), ubicación dentro de cada hábitat (borde, centro) y fecha de muestreo (9, 30 y 58 días) sobre la riqueza de especies de coleópteros (número de especies/mg de hez seca). P* corresponde a la probabilidad no ajustada, P adj. es la probabilidad ajustada basada en el valor de epsilon del estimador Greenhouse-Geisser Source of variation Degree of freedom Mean square F-value P*-value P adj-value Habitat 2 0.07 7.62 < 0.01 Location 1 0.00 0.04 0.84 Habitat*location 2 0.04 3.87 0.02 Error 170 0.01 Sampling time 2 0.17 20.98 < 0.01 < 0.01 Habitat*sampling time 4 0.05 6.18 < 0.01 < 0.01 Location*sampling time 2 0.02 1.97 0.14 0.14 Habitat*location*sampling time 4 0.02 2.12 0.07 0.08 Error 340 0.01 Greenhouse-Geisser e = 0.903 and Acrotrichis chilensis (n = 276), which individuals. At t , the most abundant species 3 accounted for 87 % of the 933 individuals were Ptinus sp. 1 (n = 194), Arthrobrachus sp. collected. At t , the most abundant species (n = 89) and N. angustata (n = 52) being 91 % 2 were Plesiomalota merula (n= 99), of the 368 individuals. Arthrobrachus sp. (n = 95), Namunaria Abundance (number of beetles mg dry dung- angustata (n = 76) and Dasymera sp. (n = 53), 1) was significantly higher in the continuous which accounted for 75 % of the 429 forest than in the pine plantations and forest DECOMPOSITION AND BEETLES IN THE MAULINO FOREST 113 fragments; however, this pattern varied through continuous forest was 16 times higher than in time (Table 3). At t , abundance in the the forest fragments (0.48 ± 0.12 versus 0.03 ± 1 continuous forest was three and six times 0.01 beetles mg dry dung-1, mean ± 1 SE), higher than in the pine plantations and forest whereas the abundance at the pine plantations fragments, respectively (0.90 ± 0.12 versus was intermediate (0.16 ± 0.04 beetles, mean ± 1 0.34 ± 0.10 and 0.14 ± 0.02 beetles mg dry SE). Nevertheless, at t , abundance was similar 2 dung-1, mean ± 1 SE). At t , abundance in the among habitats (Table 3, Fig. 3). 3 TABLE 3 Results of repeated measures ANOVA for the effect of habitat (continuous forest, forest fragments and pine plantations), location within each habitat (border, interior) and sampling time (9, 30 and 58 days) on beetle abundance (number of individuals/mg of dry dung). Letter P* is the non adjusted probability, P adj. is the adjusted probability based on the epsilon value of the Greenhouse-Geisser estimator Resultados del ANDEVA de medidas repetidas para el efecto del hábitat (bosque continuo, fragmentos de bosque y plantaciones de pino), ubicación dentro de cada hábitat (borde, centro) y fecha de muestreo (9, 30 y 58 días), sobre la abundancia de coleópteros (número de individuos/mg de hez seca). El valor de P* indica la probabilidad no ajustada, P adj., es la probabilidad ajustada basada en el valor de epsilon del estimador Greenhouse-Geisser Source of variation Degree of freedom Mean square F-value P*-value P adj-value Habitat 2 8.06 22.48 < 0.01 Location 1 0.02 0.07 0.78 Habitat*location 2 0.41 1.16 0.31 Error 170 0.35 Sampling time 2 4.32 13.14 < 0.01 < 0.01 Habitat*sampling time 4 2.87 8.72 < 0.01 < 0.01 Location*sampling time 2 5.01 15.23 < 0.01 < 0.01 Habitat*location*sampling time 4 2.21 6.72 < 0.01 < 0.01 Error 340 0.32 Greenhouse-Geisser e = 0.952 Fig. 3: Abundance of beetles associated with dung on the border and interior of each habitat in every sampling time (mean ± 1 SE). Different letters represent significant statistical differences (P < 0.05) (CF = continuous forest, PP = pine plantations, and FF = forest fragments). Abundancia de coleópteros asociados a las heces en los bordes y centros de cada hábitat para cada una de las fechas de muestreo (media ± 1 EE). Letras distintas representan diferencias estadísticamente significativas (P < 0,05) (CF = bosque continuo, PP = plantaciones de pino y FF = fragmentos de bosque). 114 BUSTAMANTE-SÁNCHEZ ET AL. Regarding edge effects, after nine days (t1), DISCUSSION beetles were twice more abundant in the interior than in the border of the continuous Forest fragmentation generally has profound forest, whereas at t , they were eight times effects upon the composition, structure and 3 more abundant on the border. In none of the functioning of biodiversity (Didham et al. sampling time, there was an edge effect upon 1996, Chapin et al. 2000). Although in the total beetles abundance in the forest fragments Maulino forest, species richness and abundance and pine plantations (Fig. 3). were depressed in the forest fragments, the Abundance of the five most frequent structure of beetle assemblages only changed in families was significantly different among the borders of both the continuous forest and habitats (Table 4). Four of these families were pine plantations, and dung decomposition did more abundant in the continuous forest than in not change across the fragmented landscape, the forest fragments, while one of them except between the border and the interior of (Zopheridae) was more abundant in the pine the continuous forest. Thus, although the beetle plantations than in the other two habitats (Fig. assemblage varies across the fragmented 4). There was an edge effect in the abundance landscape, these changes do not translate into of two families: Staphylinidae (t ) had more alterations of an ecosystem process such as 1 individuals in the interior of the continuous dung-decomposition, as occurs in tropical forest and pine plantations, whereas Ptinidae forests (Klein 1989). (t ) was more abundant on the border of the The differences in the beetle assemblages 3 continuous forest (Fig. 4, Table 4). on the borders of the continuous forest and pine plantations are accounted for the increase in the Dung decomposition abundance of only two species, Ptinus sp. 1 (Ptinidae) and N. angustata (Zopheridae). Most Dung decomposition did not differ significantly of the species of Ptinidae are detritivores, and among the three habitats (Table 5). Zopheridae are fungivores (Table 1). Thus, the Additionally, decomposition did not differ increased abundance of these species on the between the interior and border of the forest borders of these habitats may have some effects fragments and pine plantations, but in the upon important ecological processes associated continuous forest, dung decomposition was 2.3 with decomposition. However, little is known and 1.8 times higher in the border than in the about the natural history of insects in Chile, interior at t and t , respectively (Fig. 5). and nothing is known about the specific 2 3 TABLE 4 Results of repeated measures ANOVA for the effect of habitat (continuous forest, forest fragments and pine plantations), location within each habitat (border, interior) and sampling time (9, 30 and 58 days) on the abundance of the most frequent beetle families Resultados del ANDEVA de medidas repetidas para el efecto del hábitat (bosque continuo, fragmentos de bosque y plantaciones de pino), ubicación dentro de cada hábitat (borde, centro) y fecha de muestreo (9, 30 y 58 días), sobre la abundancia de las cinco familias de coleópteros más numerosas Family Melyridae Zopheridae Ptiliidae Ptinidae Staphylinidae Source of variation df MS F MS F MS F MS F MS F Habitat 2 0.02 3.36* 0.23 10.21** 0.36 5.05* 0.21 5.85** 0.72 3.21* Location 1 0.02 3.41 0.03 1.53 0.16 2.25 0.29 8.14** 2.12 9.43** Habitat*location 2 0.05 9.75** 0.04 2.02 0.10 1.46 0.34 9.49** 1.08 4.82** Error 170 0.01 0.02 0.07 0.04 0.22 Sampling time 2 0.07 16.01** 0.07 4.47* 1.43 20.22** 0.43 11.41** 4.86 19.63** Habitat*sampling time 4 0.03 5.77** 0.05 2.92 0.46 6.41** 0.28 7.26** 0.62 2.49* Location*sampling time 2 0.00 0.04 0.03 1.69 0.38 5.48* 0.20 5.33** 2.65 10.71** Habitat*location*sampling time 4 0.00 0.73 0.03 1.69 0.09 1.36 0.38 9.89** 0.53 2.14 Error 340 0.00 0.02 0.07 0.04 0.25 *P < 0.05; **P < 0.01; adjusted probabilities based on the epsilon value of the Greenhouse-Geisser estimator DECOMPOSITION AND BEETLES IN THE MAULINO FOREST 115 ) 1 - g n u d g m d n I ( e c n a d n u b A Habitat Fig. 4: The most abundant families of beetles associated with dung, on the border and interior of each habitat in every sampling time (mean ± 1 SE). Different letters represent significant statistical differences (P < 0.05) (CF = continuous forest, PP = pine plantations, and FF = forest fragments). Familias más abundantes de coleópteros asociados a las heces, en los bordes y centros de cada hábitat en cada fecha de muestreo (media ± 1 EE). Letras distintas representan diferencias estadísticamente significativas (P < 0,05) (CF = bosque continuo, PP = plantaciones de pino y FF = fragmentos de bosque). 116 BUSTAMANTE-SÁNCHEZ ET AL. TABLE 5 Results of repeated measures ANOVA for the effect of habitat (continuous forest, forest fragments and pine plantations), location (borders and interiors) and sampling time (9, 30 and 58 days) on dung decomposition (% weight loss). Letter P* is the non adjusted probability, P adj. is the adjusted probability based on the epsilon value of the Greenhouse-Geisser estimator Resultados del ANDEVA de medidas repetidas para el efecto de el hábitat (bosque continuo, fragmentos de bosque y plantaciones de pino), ubicación dentro de cada hábitat (borde, centro) y fecha de muestreo (9, 30 y 58 días), sobre la descomposición de heces (% de peso perdido). El valor de P* corresponde a la probabilidad no ajustada, P adj., es la probabilidad ajustada basada en el valor de epsilon del estimador Greenhouse-Geisser Source of variation Degree of freedom Mean square F-value P*-value P adj-value Habitat 2 4.9 0.59 0.55 Location 1 64.9 7.92 0.01 Habitat*location 2 251.9 30.73 < 0.01 Error 171 8.5 Sampling time 2 20.4 4.51 0.01 0.01 Habitat*sampling time 4 13.1 2.91 0.02 0.03 Location*sampling time 2 47.4 10.51 < 0.01 < 0.01 Habitat*location*sampling time 4 6.3 1.40 0.23 0.20 Error 342 4.5 Greenhouse-Geisser e = 0.988 Fig. 5: Dung decomposition (% weight loss) on the border and interior of each habitat in every sampling time (mean ± 1 SE). Different letters represent significant statistical differences (P < 0.05) (CF = continuous forest, PP = pine plantations, and FF = forest fragments). Descomposición de heces (% de peso perdido) en los bordes y centros de cada hábitat para cada fecha de muestreo (media ± 1 EE). Letras distintas representan diferencias estadísticamente significativas (P < 0,05) (CF = bosque continuo, PP = plantaciones de pino y FF = fragmentos de bosque). biology of these two species. The paucity of Contrary to our initial prediction, species this kind of knowledge is regarded as one of richness and abundance of dung beetles were the major threats to biodiversity conservation in depressed in the Maulino forest fragments, in South America (Mares 1992, Barbosa & agreement with the effects observed in tropical Marquet 2002) and makes it difficult to explain forests. Notwithstanding, the mechanisms the possible consequences of these changes in explaining these effects seem to be different. In beetle assemblages upon ecosystem processes. tropical forests, this decrease is associated with