Ecosystem engineering by Fascicularia bicolor in the canopy of the South-American temperate rainforest

Highlights

• Fascicularia bicolor accumulate litter and reduce temperature variation on trees.

• The mean cover of vascular plants was 44% higher in plots with F. bicolor.

• Fascicularia bicolor support a high number of invertebrate species.

• Results could be relevant to improve biodiversity conservation in degraded forests.

Abstract

Ecosystem engineers are organisms that modify habitats and resource flows, they therefore could have a disproportionate impact on the diversity of ecological communities. Evidence suggests that trash basket epiphytes (TBE) can be considered ecosystem engineers of forest canopies, due to their relationship with arboreal soil availability and treetop communities. Here we evaluated whether the TBE Fascicularia bicolor (Bromeliaceae), modulates temperature and humidity in the forest canopy. We also investigated if this bromeliad is related with greater arboreal soil accumulation and is associated to higher diversity of other epiphytic plants and invertebrates in the canopy of the South-American temperate rainforest (SATR), in Chile. We measured temperature and humidity in ten trees within the forest before and after the experimental addition of F. bicolor. We also related the presence of F. bicolor with occurrence of soil macro-fauna and other canopy dwelling plants in a comparative field survey.

Temperature variability in the canopy was reduced by F. bicolor. Soil availability was higher in sites with mats of F. bicolor. The richness of vascular epiphytes was unaltered by the presence of F. bicolor, but species composition differed between sites with and without mats on each tree. At the group level, the cover of lichens and bryophytes was greater in sites without F. bicolor, while vascular epiphytes show a larger cover in sites with F. bicolor. The species richness of invertebrates increased in treetop sites colonized by F. bicolor but species composition was not different from soil in branch bifurcations. Our results show that F. bicolor must be considered in forest management practices to determine which trees must be logged, in order to preserve the viability of populations of these key organisms in the treetops of South-American temperate rainforests.

Introduction

Ecosystem engineers are species that transform their habitat by creating new structures (e.g., beaver dams; Jones et al., 1994, Wright et al., 2002), or by changing the environmental conditions with their mere presence (e.g., shading trees; Jones et al., 1994, Jones et al., 1997). In both cases engineers are able to directly or indirectly regulate the flow of resources in the environment, thus greatly impacting the landscape architecture and the community’s structure and composition.

Ecosystem engineers have such a great effect on their environment that they help to determine the inclusion or exclusion of species in the transformed area, depending on the attributes of the former habitat and organisms’ ability to take advantage of the new environmental conditions created by the engineer species (Crain and Bertness, 2006, Jones et al., 1997). Therefore, species distribution and diversity patterns across different landscapes can be partially explained due to the presence and effects of ecosystem engineers. Identifying engineer species in different ecosystems could provide insightful information to understand the mechanisms that structure ecological communities, and contribute to the improvement of current resource management and biodiversity conservation protocols (Crain and Bertness, 2005).

The importance of ecosystem engineers in less explored habitats such as forest canopies is little known, despite the existence of clear examples of canopy dwelling organisms that are able to alter arboreal communities (Angelini and Silliman, 2014, Ellwood et al., 2002, Gonçalves-Souza et al., 2010, Karasawa and Hijii, 2006, Mccracken and Forstner, 2014, Richardson, 1999, Stuntz et al., 2002, Yanoviak et al., 2004). Forest canopies are considered one of the last biotic frontiers of terrestrial ecosystems (Nadkarni et al., 2011) and hold a large portion of forest biodiversity (Ozanne et al., 2003). One of the most conspicuous structural components of forest canopies are “epiphytes”, i.e. vascular and non-vascular plants that use trees as substrates for support without extracting nutrients from their host. Epiphytes represent a significant percentage of forest biodiversity in tropical and temperate forests (Gentry and Dodson, 1987, Kelly et al., 1994, Zotz, 2005). In South-American temperate rainforests seven trees of Fitzroya cupressoides (Cupressaceae) can hold up to 48 species of vascular epiphytes, non-vascular epiphytes and vines (Clement et al., 2001). Hofstede et al. (2001) reported at least 40 vascular canopy dwelling plants in a Lowland temperate forest in New Zealand. Epiphytes support a carpet-like layer of arboreal soil along the vertical profile of their host-trees (Nadkarni, 1984a, Nadkarni, 1984b, Nadkarni and Longino, 1990) and can harbor an enormous diversity of invertebrates (Ellwood and Foster, 2004, Stuntz et al., 2002). Thus, epiphytes enhance structural diversity throughout trees’ vertical profiles by creating new habitat conditions quite different from bare trunks and branches.

Several studies have documented the ecological importance of epiphytes as drivers of forest biodiversity. For instance, Cruz-Angón et al. (2009) found that abundance of bird individuals in coffee plantation plots with epiphytes increase by 90% and the number of species is 22% higher when compared with plots where epiphytes were removed. The epiphytic bromeliad Tillandsia usneoides increase invertebrate richness by 70% by offering a more suitable environment for invertebrates, reducing the risk of predation and modulating temperature and humidity stress (Angelini and Silliman, 2014). Tank bromeliads are particularly known for supporting several species within the forest canopy, including a specialized aquatic community (Armbruster et al., 2002, Richardson, 1999). Gonçalves-Souza et al. (2010) found that tank bromeliads act as “biodiversity amplifiers”, increasing in 40% spider diversity. Armbruster et al. (2002) reported 11,219 individuals of 354 morphospecies inhabiting 209 bromeliads in the Yasuni Reserve (Ecuador), while Richardson (1999) found 15,599 individuals of 282 morphospecies from 120 tank bromeliads sampled in the Luquillo Forest (Puerto Rico). In tropical South East Asian rainforests, the presence of Asplenium ferns practically doubles the invertebrate biomass in the canopy (Ellwood and Foster, 2004). Besides their impact on forest diversity, epiphytes also support essential functional groups in the treetops, such as soil decomposers (Díaz et al., 2012). Thus, epiphytes can directly or indirectly modify their surroundings, influencing the amount of resources available and therefore change the number of species and functional groups inhabiting the canopy.

Epiphytic species which affect the canopy’s habitat due to their accumulation of organic matter in focal points of trees are called trash-basket epiphytes (TBE; sensu Benzing, 1990). Most of these epiphytes are characterized by their funnel-like shape, where litter is collected, accumulated and decomposed (Benzing, 1990, Ingrouille, 1995). The importance of TBE in the structure of canopy communities has been overlooked in most forest ecosystems; however, their relationship with the occurrence of soil invertebrates in the canopy has been widely recognized in ecological literature (Beaulieu et al., 2010, Ellwood et al., 2002, Ellwood and Foster, 2004, Gibernau et al., 2007, Karasawa and Hijii, 2006, Wardle et al., 2003). Existing evidence suggests that TBE could be considered as ecosystem engineers since TBE: (i) contribute to accumulate organic matter in the treetops (Benzing, 1990, Díaz et al., 2010, Ellwood and Foster, 2004), (ii) modulate micro-environmental conditions by reducing air temperature oscillations (Turner and Foster, 2006), (iii) create a more stable habitat for canopy dwelling invertebrates (Turner and Foster, 2006).

South-American temperate rainforests (SATRs) are distributed along the west side of the Andes, in southern Chile and western-most Argentina. These forests are a vanishing ecosystem, threatened by the expansion of exotic tree monocultures, agriculture, grazing, and logging (Armesto et al., 1998, Echeverria et al., 2006). Most taxa of the SATRs share floristic and faunistic relationships with tropical forests due to their common origin during the Tertiary (Villagrán and Hinojosa, 1997). During the Quaternary drastic climatic and geological changes depauperated the existing flora and fauna, causing these forests to become a simplified ecosystem, rich in families and genera but poor in number of species (Hinojosa and Villagran, 1997, Villagrán and Hinojosa, 1997). This ecosystem represents an opportunity to understand general ecological processes while avoiding the high complexity and diversity of most tropical forests.

In the SATRs the only TBE is the endemic Fascicularia bicolor (Bromeliaceae). This species has long leaves arranged in a rosette form with an extremely short stem or no stem at all while mats are generally formed by multiple rosettes growing together (Zizka et al., 1999). According to Zizka et al. (1999) there are two subspecies of F. bicolor: F. bicolor ssp. bicolor, a mostly saxicolous plant associated with coastal lands, and F. bicolor ssp. canaliculata, which is a frequent epiphyte in lowland old-growth forests. Fascicularia bicolor becomes more abundant in large old trees, where it is associated with around 50% of the arboreal soil along the vertical profile of their hosts (Díaz et al., 2010). Furthermore, the rosette shape of this plant acts like a natural littertrap, where debris from epiphytes and the host tree accumulates and decomposes, fostering a focal accumulation of canopy soils. By promoting the accumulation of arboreal soils, this TBE could influence a large part of the SATR canopy’s community, including functional groups such as decomposers and predators. However, traditional foresters and rural people tend to see this large epiphyte as a “parasitic plant” and a “sign of forest decay”. Therefore, trees colonized by F. bicolor are frequently targeted for selective logging in management plans of native forest in Chile (G. Ortega, personal observation). In addition, F. bicolor has been cultivated as an ornamental plant and introduced to Europe where it has been reported naturalized (Marchante et al., 2008, Nelson and Zizka, 1997).

By understanding the links between F. bicolor, the habitat provided by its host-trees and the other species inhabiting the vertical profile of trees, it is possible to visualize consequences of the loss of this TBE in a forest stand in the SATR. This information could be useful to improve forest management plans in the SATR and also to predict potential effects of F. bicolor in its non-native range. In this context, we evaluated the importance of F. bicolor within the canopy community, following four specific predictions: (i) F. bicolor modulates both the air temperature and humidity in the forest canopy, (ii) The presence and abundance of F. bicolor in focal points of trees is associated with higher diversity and abundance of other epiphytic plants, (iii) F. bicolor provides accumulation sites for organic matter and arboreal soil, and (iv) The arboreal soils associated with F. bicolor enhances the diversity and abundance of soil invertebrate macro-fauna. We therefore explored variations within the canopy habitat related to the occurrence of F. bicolor in order to provide insights about the links between this TBE and forest biodiversity.