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Effects of pine invasion on land planarian communities in an area covered by Araucaria moist forest



Cultivation of exotic pine species has increased in areas of Araucaria moist forest, which is an ecosystem with high biological diversity. Land planarians are generally susceptible to replacement of natural habitat by exotic tree species plantations. However, how planarian communities respond to the invasion of exotic species in natural habitats is unknown: (1) Are there differences in richness and abundance of land planarians between sites of Araucaria moist forest with (AMF-P) and without (AMF) pine trees and between these areas and pine plantations (P)? (2) Does the species composition of land planarians vary among AMF, AMF-P, and P?


This study shows that mean richness and abundance of land planarians per sample unit are higher in AMF sites than AMF-P sites. In addition, AMF sites have a higher estimated richness per sample unit than pine plantations and AMF-P sites. In AMF-P sites, mean richness and abundance are higher in sample units not influenced by pine trees than in those with pine needles. An ordination analysis indicated that the communities of each site are distinct, especially the communities of the AMF and P sites.


The present work demonstrated negative impacts from a recent invasion of an exotic species of pine on the richness and abundance of land planarians in a site of Araucaria moist forest and significant variation in the planarian community composition between sites of Araucaria moist forest and pine plantation.


Until the beginning of the 20th century, Araucaria moist forest was listed as critically endangered in terms of environmental conservation (MMA [2002]; Guerra et al. [2002]; Castella and Britez [2004]). It covered about 25% of the state of Rio Grande do Sul, Brazil (Guerra et al. [2002]; Koch and Corrêa [2002]). It currently covers an estimated 3.25% of Brazil, for a total of 919,565 ha (SEMA/UFSM-RS [2001]), only 14.9% of the original vegetation remaining (Mähler Junior and Larocca [2009]). One of the causes of this reduced geographic range of Araucaria moist forest is its progressive replacement by extensive areas of exotic monocultures, such as pine species (Pinheiro and Ganade [2009]).

Although they are economically important, monocultures negatively affect native ecosystems due to their low diversity of plant species (Vallejo et al. [1987]). Not only do monocultures potentially negatively affect biodiversity but they also have increased vulnerability to pests and are prone to exotic species invasions (Russel [1989]; Engelmark et al. [2001]; Pinheiro and Ganade, [2009]).

Land planarian communities are highly diverse in areas of Araucaria moist forest (Leal-Zanchet and Carbayo [2000]; Baptista et al. [2006]; Fick et al. [2006]; Leal-Zanchet and Froehlich [2006]; Antunes et al. [2008]; Leal-Zanchet and Baptista [2009]; Leal-Zanchet et al. [2011, 2012]). They are important elements of forest communities and are considered to be top predators in their microhabitats, where they feed on other invertebrates, such as annelids, gastropods, insect larvae, other arthropods, and even other land planarians (Du Bois-Reymond Marcus [1951]; Froehlich [1955]; Ogren [1995]; Jones and Cumming [1998]; Winsor et al. [1998]; Sluys [1999]; Carbayo and Leal-Zanchet [2003]; Prasniski and Leal-Zanchet [2009]). These flatworms do not have any water retention mechanism and have low tolerance to extreme changes in temperature and humidity. Thus, they are considered to be good bioindicators of the degree of impact on the areas where they are found, and they are used in studies on diversity and conservation (Sluys [1998, 1999]; Winsor et al. [1998]).

Previous studies have indicated that land planarians are highly sensitive to the replacement of Araucaria moist forest by monocultures of exotic species (Carbayo et al. [2002]; Fonseca et al. [2009]). However, the response of planarian communities to the invasion of exotic species in their original habitat remains unknown. Considering the high diversity of land planarians in areas of Araucaria moist forest and the increasing impact of pine plantations on these areas, our study attempts to answer the following questions: (1) Is there a difference in richness and abundance of land planarians between sites of Araucaria moist forest with and without pine trees and between these areas and pine plantations? (2) Does species composition of land planarians vary between sites of Araucaria moist forest and pine plantations?


Study area

Sampling took place in São Francisco de Paula National Forest, located in the northeastern region of the state of Rio Grande do Sul, Brazil (29°23′ to 29°27′ S, 50°23′ to 50°25′ W). It consists of a conservation unit of sustainable use included in an area covered by the Atlantic Forest Biosphere Reserve, a core area that has high to very high conservation priority (MMA [2000]). This conservation unit is composed of a heterogeneous mosaic of environments, including remnants of Araucaria moist forest, plantations of exotic species of pine (Pinus spp.) and eucalyptus (Eucalyptus sp.), and plantations of the native species Araucaria angustifolia. It has a total area of 1,606 ha and altitude higher than 900 m, with an altitudinal variation of 300 m. The climate is Cfb (i.e., mesothermic, super humid, with mild summer and cold winter), mean annual temperature is 14.5°C, and mean annual rainfall is 2,252 mm (Backes [1999]; ICMBIO -unpublished data).

Sampling design

Three sites were sampled in São Francisco de Paula National Forest. Two sites were composed of Araucaria moist forest, located on opposite sides (west and east) of a 0.5- to 1-m wide stream, and the third was composed of an exotic pine species plantation. Each site had an area of 0.5 ha and was subdivided into 200 5 m × 5 m plots, from which 50 were randomly selected in each site for sampling land planarians.

Both sites of the Araucaria moist forest slope slightly towards the stream and have different structural features. The western site (AMF) is dominated by plants in the canopy layer and almost completely lacks an understory. The eastern site (AMF-P) is dominated by young plants that form a dense understory and suffers from the invasion of an exotic pine species. Part of the site is directly affected by this impact. The third site (P), a pine plantation, is located about 2.5 km east of the Araucaria moist forest sites, has a well-developed understory, and is surrounded by areas with native forest and Araucaria plantations. Site P differs from AMF-P by lower abundance and richness of tree species associated with pine trees and by a thicker leaf litter layer, due to the amount of pine needles on the soil.

Each site was sampled five times between January and July 2010. In each plot, divided into four quadrants, land planarians were sampled by four previously trained persons by directly searching in the mainland planarian refuges: under stones, logs, fallen branches, and leaf litter. A sampling effort of 10 min was used for each plot in each round of sampling.

The animals were identified in the field, whenever possible, according to characteristics of external morphology, such as color pattern, size, and body form. In the lab, the animals were measured and the analysis of the external morphology was complemented. Specimens were fixed with 10% formalin. For identification at species level, histological preparations of the copulatory apparatus and the pharynx were made. Adult specimens without any of the morphological characteristics required for identification at the genus level, which could be differentiated from specimens of other species occurring in the study area, were placed in the collective group Pseudogeoplana Ogren and Kawakatsu, 1990. Unidentified flatworms were either immature specimens or those lost before fixation. Voucher specimens of each species were deposited in the scientific collection of the laboratory (Instituto de Pesquisas de Planárias, UNISINOS, São Leopoldo, Brazil) in order to do morphologic and/or taxonomic studies.

Data analysis

The analyses were performed at site level (alpha diversity) using the sample units (plots) as repetitions. To verify the existence of significant differences in mean richness and abundance of land planarians by plot in the three study sites, an analysis of variance (ANOVA) was applied, followed by a Tukey test (with SPSS-19; IMB Corporation, Somers, NY, USA). Rarefaction curves based on individuals were built with EcoSim, version 7.72 (Gotelli and Entsminger [2012]), in order to correct richness to the same abundance of specimens, aiming to compare the communities of study sites. The specimens were used as sample units to build the curves, thus more clearly showing richness patterns (Gotelli and Colwell [2001]). The Chao2 method with EstimateS (Colwell [2005]) was used to estimate richness by site. Unidentified specimens were considered only in the calculation of abundance.

An ordination analysis (nonmetric multidimensional scaling (NMDS)), using species abundance data, was applied to explore differences in flatworm assemblage composition. NMDS was carried out with R-software, version 2.15, on a similarity matrix based on the Bray-Curtis dissimilarity measure. Data were logarithmized and relativized. Species with abundance lower than 0.9% of the total of individuals were excluded from the analysis in order to reduce ordination stress. Only stress values lower than 0.20 provide an adequate description of the distance matrix (Legendre and Anderson [1999]). The Berger-Parker dominance index was used to verify the relative importance of the most abundant species of land planarians in the studied sites.


In the three study sites, 316 specimens, distributed over 24 flatworm species, were sampled (Table 1). The mean richness (F (1,2), 3.885; p = 0.017) and mean abundance (F (1,2), 6.698; p = 0.001) of land planarians per sample unit were higher at the site not influenced by pines (AMF) than at the site influenced by pines (AMF-P), and there were no significant differences between the pine plantation site (P) and AMF or AMF-P sites. In AMF-P, mean richness (t test, p = 0.006) and mean abundance (t test, p = 0.007) were higher in plots not influenced by pines than in those with pine needles (Figures 1 and 2).

Table 1 Land planarian richness and abundance at three sites in a southern Brazilian conservation unit
Figure 1
figure 1

Mean richness of land flatworms per sample unit in plots with and without Pinus needles. AMF, Araucaria moist forest; AMF-P, Araucaria moist forest with pine needles. P = 0.006.

Figure 2
figure 2

Mean abundance of land flatworms per sample unit in plots with and without Pinus needles. In a southern Brazilian conservation unit. AMF, Araucaria moist forest; AMF-P, Araucaria moist forest with pine needles. P = 0.007.

Considering total species richness per site, the observed richness at sites AMF-P and P were similar and higher than what was observed in AMF. The rarefaction curve, with corrected richness under the same abundance, supported these results (Figure 3). However, taking into account the results per sample unit in each studied site, AMF showed a higher estimated richness. Thus, a larger species increment was estimated for AMF, followed by P and AMF-P (Table 2).

Figure 3
figure 3

Species accumulation curves with confidence intervals for three sites in a southern Brazilian conservation unit. AMF, Araucaria moist forest; AMF-P, Araucaria moist forest with pine needles; P, pine plantation.

Table 2 Species richness and abundance of land planarians in a southern Brazilian conservation unit

Composition of the communities

The recorded species are distributed among 13 genera and a collective group. Obama and Luteostriata were the richest genera (Table 1). The three sites had ten species in common, but the dominant species were different for each site. In AMF, Paraba franciscana (n = 28) and Obama ladislavii (n = 26) showed dominance indices of 21% and 19%, respectively, while in AMF-P, O. ladislavii (n = 16) and Obama sp. 1 (n = 11) showed dominance indices of 21% and 14%, respectively. In P, the dominant species was Luteostriata ernesti (n = 26), with a dominance index of 33%, while O. ladislavii was the second most abundant flatworm (n = 11), with 10% dominance.

Some species had very different dominance indices between the sites. P. franciscana had a high dominance in AMF but a dominance index of only 8% in AMF-P; Obama josefi, the third most dominant species in AMF (17%), had only 3% dominance in AMF-P. In pine plantations, both species had dominance lower than 1%, with only one specimen recorded, while L. ernesti was recorded only in P.

The ordination analysis supports these results by revealing a significant separation of land planarian communities between sites of Araucaria moist forest and pine plantation (Figure 4), indicating that the communities from the three sites are distinct. The ordination stress was 0.09, which ensures reliable interpretation of the results.

Figure 4
figure 4

Ordination analysis (NMDS) of three sites in a southern Brazilian conservation unit. 1, Araucaria moist forest with pine needles; 2, Araucaria moist forest; 3, pine plantation.


The results indicate the existence of significant differences in species richness and mean abundance of land planarians per sample unit between the sites of Araucaria moist forest. The alterations in microhabitat caused by the accumulation of pine needles on the soil in AMF-P, which changed the microclimate, probably caused the differences found for these two sites. Similar situations have been found in other studies, where the abundance of several invertebrate groups was reduced in plantations where values of pH, humidity, and C:N ratios were altered by the different leaf litter composition (Bonham et al. [2002]; Robson et al. [2009]; Castro-Díez et al. [2012]).

The impact on the land planarian community was clear in AMF-P plots without pine, which had significantly higher values of richness and abundance than plots with pine. However, total richness per site was probably not influenced since the invasion was recent and the surrounding areas are conserved. In other studies, these characteristics were important for diversity in areas dominated by exotic species (Bonham et al. [2002]). Furthermore, AMF-P has a more developed understory than AMF, which may favor a higher richness in AMF-P.

Mean richness and abundance per sample unit in the pine plantation did not differ significantly from the other sites, probably due to the occurrence of intact native forest in the surrounding area. This intactness is a result of the plantation being about 40 years old and having a well-developed understory. Thus, it seems to be in a secondary stage of ecological succession. In fact, understory diversity is an important factor for diversity conservation in plantations (Humphrey et al. [1999]). Older plantations also support a larger number of native terrestrial invertebrate species (Bonham et al. [2002]). Additionally, the small extension of pine plantations in the study area and the dispersal ability of land planarians (Carbayo et al. [2002]) together with the landscape features of this conservation unit (Fonseca et al. [2009]) facilitate occupation of these sites by planarians. Nevertheless, the land planarian communities are highly sensitive to the replacement of Araucaria moist forest by monocultures of exotic species (Carbayo et al. [2002]; Fonseca et al. [2009]).

With respect to species composition, the community in the pine plantation clearly differed from that of the Araucaria forest. Five species were exclusive to the pine plantation, and L. ernesti was dominant and only recorded in this site. However, previous studies have recorded a low abundance of L. ernesti in Araucaria moist forest (Carbayo et al. [2002]; Antunes et al. [2012]).

Among the dominant species in the Araucaria forest sites, the generalist species O. ladislavii (Carbayo et al. [2002]; Fick et al. [2006]) has a high dominance index at both sites and at the pine plantation. These results suggest that the structural differences between sites did not affect populations of O. ladislavii. Similar results were found in a previous study in the same study area (Carbayo et al. [2002]). In studies at a larger spatial scale, O. ladislavii abundance was low at other sites of Araucaria moist forest (Leal-Zanchet and Baptista [2009]; Leal-Zanchet et al. [2011]).

P. franciscana and O. josefi, the first and third most dominant species in AMF, respectively, are among the five most abundant species in areas of Araucaria moist forest (Leal-Zanchet et al. [2011]). Their low dominance or abundance in AMF-P and P suggest that both may prefer preserved areas, which has already been indicated for P. franciscana (Carbayo et al. [2002]).


This work demonstrated negative impacts of the recent invasion of an exotic pine species on the richness and abundance of land planarians at a site of Araucaria moist forest and also revealed significant variation in community composition between Araucaria moist forest and pine plantations. However, the factors that influence land planarian species composition at sites with different degrees of impact and in areas with exotic tree species are still unknown, in addition to the microhabitat features that may influence occupation by land planarian species.


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We are grateful to the Brazilian Research Council (CNPq), the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), and the Fundação de Amparo à Pesquisa do Rio Grande do Sul (FAPERGS) for grants and fellowships in support of this study. We also thank the Instituto Chico Mendes de Conservação da Biodiversidade for permitting and supporting fieldwork activities in the National Forest and for the permits for sampling biological material. We are indebted to G. Iturralde, I. Rossi, J.A.L. Braccini, and R. Canello for field assistance and data organization. The technicians L. Guterres and R. Canello are thanked for their help in histological preparation. MSc. Emily Toriane is acknowledged for the English review of the text. We also thank two anonymous reviewers for their suggestions.

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Correspondence to Ana Maria Leal-Zanchet.

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Authors’ contributions

SMO participated in the field samplings, made the histological preparations, performed part of the statistical analyses, made the figures, and drafted the manuscript. PKB participated in the field samplings, contributed in the statistical analyses, edited the figures, and reviewed the manuscript. VAB performed part of the statistical analyses and reviewed the manuscript. AMLZ conceived the study, made intellectual contributions, determined the sampling design, coordinated the study, and reviewed the manuscript. All authors read and approved the final manuscript.

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de Oliveira, S.M., Boll, P.K., dos Anjos Baptista, V. et al. Effects of pine invasion on land planarian communities in an area covered by Araucaria moist forest. Zool. Stud. 53, 19 (2014).

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  • Community structure
  • Species composition
  • Flatworms
  • Exotic species
  • Conservation