Fontúrbel, F.E. and J.E. Jiménez. 2011. Environmental and ecological architects: Guidelines for...

CONSERVATION-DERIVED TEMPERATE FOREST MANAGEMENT 203

Revista Chilena de Historia Natural 84: 203-211, 2011 © Sociedad de Biología de Chile

REVISTA CHILENA DE HISTORIA NATURAL

Environmental and ecological architects: Guidelines for the Chileantemperate rainforest management derived from the monito del monte

(Dromiciops gliroides) conservationArquitectos ambientales y ecológicos: Pautas para la gestión ambiental del bosque

templado lluvioso de Chile derivadas de la conservación del monito del monte(Dromiciops gliroides)

FRANCISCO E. FONTÚRBEL1, * & JAIME E. JIMÉNEZ2, 3

1 Departamento de Ciencias Ecológicas, Facultad de Ciencias, Universidad de Chile, Casilla 653, Santiago, Chile2 Laboratorio de Vida Silvestre, Universidad de Los Lagos, Osorno, Chile

3 Present address: Department of Biology and Department of Philosophy and Religion Studies, University of North Texas,Denton, TX 76203-5017, USA

*Corresponding author: [email protected]

ABSTRACT

Land use change is one of the main biodiversity threats. Due to this change, natural habitats such as the SouthAmerican temperate rainforests have been rapidly degraded, fragmented, and lost. Consequently, the managementand conservation of the remaining forest is a priority and having an appropriate environmental policy is mandatoryfor this purpose. Conservation actions in the temperate rainforest have been addressed from an individual speciesperspective, giving less attention to the ecosystem level conservation. Moreover, conservation-related informationhas not reflected yet on environmental policy development. We used the case study of the monito del monte(Dromiciops gliroides) to illustrate how our current ecological and conservation knowledge of a species could beused to generate a new environmental policy. Dromiciops gliroides is a forest-dependent species with an importantecological role and quite unique evolutionary status. In order to guarantee the persistence of D. gliroides, wepropose two habitat management components to be incorporated in management plans: structure and connectivity.Structure refers to spatial arrangement and key structural elements that determine habitat quality and connectivityrefers to functional connectivity at the landscape level. The conservation of the monito del monte might alsocontribute to the conservation of many other forest-dependent species. By conserving such species it will bepossible to conserve the ecological interactions and the eco-evolutionary processes, which ultimately determine theconservation of the temperate rainforest.

Key words: environmental policy, management plan, natural regeneration, plant-animal mutualism, rainforest.

RESUMEN

El cambio de uso de la tierra es una de las principales amenazas a la biodiversidad. Hábitats naturales como elbosque templado lluvioso de Sudamérica han sido degradados, fragmentados y eliminados rápidamente. Enconsecuencia, es prioritario el manejo y conservación de los remanentes, para lo que es necesario contar con unapolítica ambiental acorde. Las acciones de conservación referentes al bosque lluvioso templado se han abordadomayormente desde una perspectiva de especies individuales, con poco énfasis en la conservación a nivel deecosistema. Más aún, la información generada en este ámbito tampoco ha permeado en el desarrollo de políticasambientales. Utilizamos el estudio de caso del monito del monte (Dromiciops gliroides) para ilustrar cómo elconocimiento actual en ecología y conservación de una especie puede ser utilizado para generar una nueva políticaambiental. Dromiciops gliroides es una especie dependiente del bosque, con un importante rol ecológico y un graninterés evolutivo y de conservación. Para garantizar su persistencia, proponemos dos componentes de gestión delhábitat, a incorporarse en los planes de manejo: la estructura y la conectividad. La estructura hace referencia alarreglo espacial y la presencia de elementos estructurales clave que influyen en la calidad del hábitat, mientras queconectividad se refiere a la conectividad funcional del paisaje. Conservando al monito del monte, se conservaríantambién otras especies dependientes del bosque y así las interacciones ecológicas y los procesos ecoevolutivos, quedeterminan finalmente la conservación del bosque lluvioso templado.

Palabras clave: bosque lluvioso, mutualismo planta-animal, plan de manejo, política ambiental, regeneraciónnatural.

SPECIAL FEATURE: APPLYING ECOLOGY

204 FONTÚRBEL & JIMÉNEZ

INTRODUCTION

Human activities have modified natural habitatssince prehistoric times, with a remarkableintensification after the arrival of the industrialera (Armesto et al. 2010). As a result, there iscurrently a biodiversity loss crisis. Even thoughthis situation has been acknowledged in the lastdecades, the environmental policies andconservation actions have only been developedquite recently (Butchart et al. 2010). Land usechange is one of the most worrisome threats tobiodiversity worldwide (Sala et al. 2000) and itis closely related to habitat loss, fragmentation,and transformation (Chapin III et al. 2000). Allthese factors might compromise the long-termpersistence of many species, given that theirlife history traits determine their sensitivity tohabitat modifications (Vásquez & Simonetti1999, Vergara & Armesto 2009).

Special attention has been given to hot-spotsites around the world (Myers et al. 2000,Mittermeier et al. 2005) in order to preserveecosystems with high biodiversity andendemism levels, currently threatened byhuman actions. Among them, high endemismin temperate ecosystems, such as the SouthAmerican temperate rainforest (SATR) hasbeen less studied than tropical ecosystems.This particular forest is facing rapidfragmentation and loss (Echeverria et al. 2006,2007), because of the expansion of urbancenters and farming activities (Armesto et al.2010). The remaining SATR stands are highlyfragmented, immersed in a complex mosaic ofanthropogenic matrices. Such matrices rangefrom plain grasslands to commercial forestplantations, increasing edge effects (Bentley2008) and reducing habitat quality.

Conservation issues at the SATR have beenmostly handled species-by-species, focused onspecies with critical conservation status.However, the conservation of functionality ofthese forests has not been taken intoconsideration. Few studies have addressed theimpact of human disturbances on ecologicalinteractions (e.g., Valdivia et al . 2006,Simonetti et al. 2007, Valdivia & Simonetti2007, Martinez-Harms & Gajardo 2008).Moreover, habitat degradation, loss, andfragmentation could disrupt key mutualisms(e.g., Rodríguez-Cabal et al . 2007) andnegatively affect natural regeneration. As the

SATR has a highly endemic biota, plant-animalmutualisms (such as pollination and seeddispersal) are remarkably important inmaintaining biodiversity (Aizen et al. 2002).Therefore, an ecosystem conservationapproach would be preferred, rather thansingle species-based conservation actions.

For a successful habitat conservationapproach, appropriate environmental policiesare necessary, aiming to create a nationalframework for management and conservation.However, environmental policy and biodiversityconservation studies are commonly treatedseparately (e.g., Margalida et al. 2010), eachfocusing on resolving their particular problemswithout an explicit connection. Environmentalmanagement and conservation sciences sharemany ecological elements, even if they usuallyoperate at different spatial scales. In this shortessay, we aim to use the case study of anendemic South American ancient marsupial, toshow an example of an explicit connectionbetween research conducted on the ecologyand conservation of a particular species. Wepropose the development of environmentalpolicies intended to successfully manage theSATR, considering its functional and structuralaspects.

DROMICIOPS GLIROIDES AS A MODEL SPECIES

The monito del monte (Dromiciops gliroidesThomas) is considered a conservation priorityfor being the only extant species of theMicrobiotheria Order (Marshall 1978), andbecause of i ts ecological role as seeddisperser of many native species (Amico et al.2009). Thus, D. gliroides can help significantlyto the natural regeneration of the nativevegetation (García et al. 2009, Carmona et al.2010). This species has not been studied indetail until the last decade. Recent researchhas shown that D. gliroides is not as scarce asit was assumed to be, when specific samplingmethods were developed (Fontúrbel &Jimenez 2009, Fontúrbel 2010). We also havea much better understanding of this species’tolerance to habitat degradation, emphasizingits role as a regeneration agent. In spite ofsuch tolerance, studies regarding spatialecology have shown that D. gliroides candisperse through riparian corridors (Smith-


Ramírez et al. 2010), but cannot move acrossopen habitats, such as prairies (Fontúrbel etal . 2010). Such behavior precludes i tsdispersal among forest remnants immersedinto non-forested matrices, experimenting a“fence effect” (Lindenmayer et al. 1999).

Dromiciops gliroides is an endemic marsupialof the Chilean and Argentinean SATRdistributed from Los Queules National Reserve(35º S) to Chiloé island (44º S), comprising bothCoastal and Andes ranges and the interveninglowlands (Kelt & Martínez 1989, Lobos et al.2006). This species is morphologically andphysiologically adapted to cold and moistforests (Hershkovitz 1999, Bozinovic et al.2004). It was thought to be restricted to old-growth native stands dominated by Nothofagusspp. and Araucaria araucana (Hershkovitz1999). However, recent research has shownthat D. gliroides is also found in small (< 5 ha)Myrtaceae-dominated second-growth forestfragments (Fontúrbel et al. 2010), in which ithas shown similar population densities thanthose found in old-growth fragments (see alsoCelis-Diez 2010, Smith-Ramírez et al. 2010), aslong as these fragments retain key structuralelements such as fallen logs, stumps, leaf litter,snags, shrubs, and a dense bamboo cover. InArgentina, nevertheless, forest fragmentationhas shown a negative effect on D. gliroides’densities (Rodríguez-Cabal et al. 2007).

Small-bodied species like this marsupial areusually associated to structurally complexhabitats. In that sense, structural complexitydetermines habitat texture, which alsoinfluences mobility and shelter-provisioning(Bro-Jørgensen 2008, Fischer et al. 2008).However, human disturbance can significantlyalter habitat complexity for D. gliroides .Anthropic pressures can change canopy heightand cover, branch diameter and density, leafl itter abundance, vine abundance, mossabundance, shrub cover, bamboo cover, aswell as the presence of fallen logs, stumps, andsnags (Jaña-Prado et al. 2006). Such changescan dramatically reduce cavity availability (i.e.,nesting sites) by removing coarse woodydebris (usually used as firewood), as has beenshown for forest cavity nesting birds(Cornelius et al. 2008, Cockle et al. 2010) andmarsupials (Lindenmayer et al. 1999, Gibbonset al. 2002). Despite this, there is no formalstudy on cavity limitation for D. gliroides. The

use of nest boxes and its increasing occupancytrend over time (Franco 2009) suggest thatnatural cavities might in fact be a limitingresource for this species in second-growthstands. Nesting boxes occupancy increasedfrom 20 % to 40 % in three years (LM Franco,personal communication, 2010).

The reduction of branch, shrub, and bamboodensity might diminish shelter sites and intra-fragment dispersal paths. Such habitat structureseems essential in order to attain long-termpersistence (Vergara & Schlatter 2008). Thoseaspects are well documented for forest-dependent birds. Forest bird richness,abundance, and guild composition has shownsignificant changes as a function of habitatstructure (Diaz et al. 2005). Specifically,structural simplification would cause a declineon forest bird diversity. Moreover, structuralcomponents such as understory density mightdetermine movement possibilities for dispersal-limited species, such as rhynocriptids (e.g.,Scelorchilus rubecula, Pteroptochos tarnii)(Castellón & Sieving 2006a, 2007).

In summary, habitat degradation couldnegatively affect D. gliroides in two mainaspects: shelter and food provisioning. Shelterwould be a limiting resource when cavities onlive trees and fallen logs are reduced byhuman action. Also nesting materials (mossesand bamboo leaves; Jiménez & Rageot 1979)could be a limiting resource on degradedforests (Diaz et al. 2006). On the other hand,the reduction of vines and understoryvegetation would reduce food (i.e., fleshy fruitsand insects) availability, as well as potentialdispersal paths needed to search for food(Jaña-Prado et al. 2006, LM Franco, personalcommunication, 2010) and compromisemobility (Gallardo-Santis et al . 2005).Consequently, habitat structure could limithabitat use possibilities (Vergara & Schlatter2008, Vergara & Armesto 2009), as reportedfor other forest-dependent species (e.g.,Sieving et al. 2000, Reid et al. 2004).

STRUCTURE AND CONNECTIVITY: LINKINGCONSERVATION RESULTS WITH

ENVIRONMENTAL POLICY

A sound environmental policy should be basedon hard ecological knowledge (Lindenmayer


1999). Ecological and conservation knowledgeshould be used to design forest conservationand management plans at the scale of thebiome. Maintaining ecosystem functionalityand its evolutionary trajectory depends onpreserving the ecological interactions.Previous works highlighted understory birdsas umbrella species for SATR conservation(e.g., Castellón & Sieving 2007). Here, we gofurther by proposing the use of an endemicmammal, with an exceptional ecological role.Our current ecological knowledge on D.gliroides points to its outstanding rolemaintaining pollination and dispersal services(Aizen 2003), on which the ecosystempersistence and identity relies, and supports itas a model species for conservation andmanagement (Lindenmayer et al. 2002). Beingthe sole disperser of the native mistletoeTristerix corymbosus (Amico & Aizen 2000,Amico et al. 2011), this marsupial guaranteesthe food supply for many other species,especially for the hummingbird Sephanoidessephaniodes, which depends on this mistletoefor feeding in winter (Aizen 2003). Conservingmutualists has an exceptional ecosystemconservation value, considering that about 75% of the SATR plants depend on suchmutualisms (Aizen & Ezcurra 1998).

In order to maintain D. gliroides’ ecologicaldynamics that may serve as a model species tomaintain SATR ecological processes, wepropose two key components that should beconsidered on the environmental policy:habitat structure and connectivity.

Habitat structure

Habitat structure component has two mainaxes: geometry and fine-grain structure. Theformer operates at the landscape scale and isdetermined by the spatial arrangement ofpatches, while the latter does it at the patchscale. Thus, landscape attributes such asfragment size, shape, and its spatialdistribution (randomly, uniformly, oraggregated in patches) determine dispersalpossibilities as well as the amount of suitablehabitat available for a particular species(Fahrig 1997, 2003, Lindenmayer & Fischer2006). Additionally, those landscape attributesalso determine the extent of edge effects (Ries& Sisk 2004). Small and irregular fragments

will experiment larger edge effects than largeand rounded patches. Regular fragments havelarger core areas than irregular ones andhence, larger potential carrying capacities forthe species therein (Castellón & Sieving 2007).

Additionally, metapopulation dynamicscould be achieved if patches are large andclose enough to maintain local populations,and would allow inter-patch dispersal (Wiens1997). Despite the fact that D. gliroidesmetapopulation dynamics has not beenassessed yet, telemetry (Franco 2009,Fontúrbel et al . 2010) and corridor-useevidence (Smith-Ramírez et al. 2010) suggestthat it would be similar to Castellón &Sieving’s (2007) model for S. rubecula. In thatsense, spatially-explicit scenarios should beused in order to estimate the proportion ofSATR remnants that would constitute suitablehabitat for forest-dependent species. If thisconsideration is taken into account whenmanaging forest remnants, the amount ofsuitable habitat for D. gliroides and otherforest species could be maximized.

On the other hand, fine-grain structureaxis refers to the presence and quantity ofkey structural elements in each forest patch.Structural elements such as canopy heightand cover, cavities, branches, vines, mosses,and others determine that microhabitatconditions could be seen as niche axes(Vásquez 2005). The presence and abundanceof those structural elements determine thehabitat quality of each forest remnant (Beyeret al. 2008, Vergara & Armesto 2009) andcould be lost due to human action: directly,through its removal for firewood or otheruses, and indirectly, by livestock grazing.Recent work (Rodríguez-Cabal 2008, García etal. 2009) has shown that, in Argentina, thepresence of D. gliroides is related to T.corymbosus abundance at a smaller scale.However, this pattern was not detected inChile (Smith-Ramírez et al . 2010). At abroader scale, D. gl iroides presence isassociated with bamboo cover (see alsoPatterson et al. 1990). Bamboo cover is also amajor factor for understory birds (e.g. ,Sylviorthorhynchus desmursii), influencingabundance of invertebrates as food resource(Reid et al. 2004). An abundant understorymay also have a positive effect on D. gliroides,by providing invertebrates that constitute an


important item of its diet (Jiménez & Rageot1979, Quijano 2008).

Connectivity

Two axes determine the connectivitycomponent: landscape composition and thenature of the surrounding matrix. Forestcomposition relies on how forest patches ofdifferent size classes are distributed along aheterogeneous landscape. This aspect, closelyrelated with the f irst structural axis, isfundamental to determine functionalconnectivity (e.g., Castellón & Sieving 2007).Castellón & Sieving (2006b) determined that >25 % of non-open habitat surrounding forestpatches could have a significant effect on S.rubecula occupancy even in small (< 10 ha)fragments. A similar situation could beexpected for D. gliroides, which is known to beable to disperse through dense scrublands(Fontúrbel et al. 2010). Considering thelimited dispersal abilities of D. gliroides (shortdistances of 100 to 200 m), its movementthrough the landscape requires closer patchesand forested corridors, with some verticalstructural complexity (Fontúrbel et al. 2010,Smith-Ramírez et al. 2010). Empirical evidencehas shown that corridors > 25 m wide canallow D. gliroides movement and thuspersistence (Smith-Ramírez et al. 2010), whichis very similar to the value estimated bySieving et al. (2000) for S. rubecula.

Because of the positive relationshipbetween landscape connectivity and ecologicalconnectivity (Lindenmayer & Fischer 2006), adiminished D. gliroides landscape dispersalwould result in less ecological connectivity.Losing ecological connectivity would representless inter-fragment dispersal for many nativeplants, and hence less gene flow. Thepermeability of the surrounding matrix(Ricketts 2001), ultimately determines whetherthis species would be capable to dispersethroughout, as well as the species abundanceand composition in each fragment (Ewers &Didham 2006). A non-forested matrix willpreclude D. gliroides dispersal, even thoughforest remnants are close to each other(Fontúrbel et al . 2010), confining localpopulations to isolated patches with nochances of gene flow or rescue effects. Theamount and quality of vegetation cover would

ultimately determine the willingness of forestspecies to enter potential corridors (Sieving etal. 2000).

Molecular evidence has shown minimum D.gliroides genetic differentiation levels, becauseof the unrestricted gene flow along itsdistributional range (Himes et al. 2008).Therefore, the movement restrictions thathuman disturbance impose could severelyaffect the evolutionary trajectory of thismarsupial. Increasing genetic differentiationamong forest remnants and causing allelicdiversity loss could also change its eco-evolutionary dynamics (Kinnison & Hairston2007), modifying the local ecologicalinteractions, and its role as a selection agent.

Joining structure and connectivity with environ-mental policy

The current Chilean legislation (Native ForestLaw 20283, approved in 2008) considers theformulation of native forests managementplans. However, the spatial configuration ofthe SATR is not taken into consideration underthis legal framework, overlooking corehabitats, key structural elements (Vergara &Schlatter 2008), and functional connectivity.Moreover, cutting methods prescribed in theChilean law (i.e., heavy shelter-wood and stripcutting) for forest regeneration does notconsider forest-dependent species, whichwould decrease as a result of structuralchanges (Vergara & Schlatter 2008).Consequently, the whole ecological andevolutionary dynamics of the SATR has beenoverlooked. On the contrary, if structure andconnectivity were taken into account for theelaboration of environmental policies, a morerealistic ecosystem conservation programwould be achieved (Fig. 1).

Considering the current habitat loss trend(Echeverria et al. 2006), it is imperative tomanage the remaining rainforest fragmentsappropriately, contemplating integralmanagement plans. The absence ofmanagement of timber stocks will cause itscollapse within one or two decades (Armestoet al. 2010). Consequently, forest recoveryshould be included in the legal framework.Future land policy should also incorporatesocial values and ecological factors instead ofbeing based mostly on economic reasoning


(Armesto et al. 2010). Our proposal may helpto incorporate the ecological factors into thisnew policy, but socio-economic drivers of landuse change should also being considered.

In the same sense as the monito del montewas proposed here as a model species, birdsalso were used as conservation umbrellas. Inthat case, Willson & Armesto (2003) proposedfive key management recommendations: (1)maintaining the extant forest patches, (2)using wooded windshields, (3) harvestingplanning, (4) education, and (5) research.Although such general recommendations areextremely valuable for incorporating theecological dimension into environmentalpolicy, they ignore the spatial component. Aspatially-explicit approach as the one wepropose here might complement theserecommendations and hence help developingbetter and more functional and sustainablepolicies.

Integrating these structural andconnectivity components derived fromstudying the monito del monte would allowimproving the current environmental policy infour main aspects:

(1) Promoting preservation of the extantremnants and restoring previously degradedor deforested areas, in order to increaselandscape connectivity. Connecting severalforest patches of different size classes wouldhave a larger positive effect than preserving afew large and isolated remnants (Prugh et al.2008). This scenario would allow inter-patchconnectivity, benefiting D. gliroides and manyother forest-dependent species that cannotdisperse through a non-forested matrix(Castellón & Sieving 2006b). This outcomewould help maintain the ecosystemfunctional i ty, incorporat ing trophiccomplexity (Duffy et al. 2007). Additionally,preserving such animal species also would

Fig. 1: Summary chart. Regular lines represent the current situation. Dashed lines represent what wouldhappen if no actions were taken. Bold lines represent what would happen if the proposal were implemented.Circles present the final result for the native forest.

Esquema resumen. Las líneas normales muestran la situación actual. Las líneas punteadas ilustran lo que pasaría si no setoman acciones. Las líneas gruesas muestran lo que pasaría si se implementa la propuesta. Los círculos representan elresultado final para el bosque nativo.


have a posit ive ef fect on plant speciesconservation, particularly specialist speciesthat rely on mutualistic interactions (Aguilaret al. 2006).

(2) Regulating human activities over theextant forest remnants, in order to maintainthe habitat quality (Jaña-Prado et al. 2006), onwhich also many understory bird speciesdepend (Reid et al. 2004, Diaz et al. 2005).Those regulations should avoid the loss of keystructural elements to firewood extraction orlivestock grazing, aiming to maintain habitatquality and to promote natural regeneration ofdisturbed areas.

(3) Maintaining the ecosystem value,through services and goods (Martinez-Harms& Gajardo 2008). This could be achieved byconserving the habitat, the species, and theecological interactions. Regulation and habitatprocesses are essential for the maintenance ofall natural processes (Martinez-Harms &Gajardo 2008). Particularly, conserving D.gliroides would allow maintaining the naturalregeneration services.

(4) Generating a new environmental policyfor the SATR, considering the heuristic valueof the current ecological knowledge as thecornerstone of management plans.

In summary, conservation knowledge andenvironmental policies are closely related toeach other, which is why they should not betreated separately. The case study of D.gliroides has i l lustrated this importantinteraction between scientific and policy-making processes. Following these simplerecommendations would help conserve manyother native species, which also rely onhabitat quality, structure, and connectivity fori ts long-term persistence, as wel l asmaintaining their eco-evolutionary dynamics(Kinnison & Hairston 2007). With an openmind, our “environmental architects” mightfind the essential benefits of learning fromthe “ecological architects”, such as themonito del monte, for the management andconservation outcomes to show significantimprovement.

ACKNOWLEDGEMENTS: We thank P. Camus forinviting us to contribute to this Special Featurenumber. We also thank F. Barbieri, M. Franco, S.Luque, and two anonymous reviewers for their insightson our manuscript. FEF was supported by a ComisiónNacional de Investigación Científica y Tecnológica

(CONICYT) doctoral fellowship. The authors thank theCentro Nacional del Medio Ambiente CENMA, Chile,for funding the publication cost of the article.

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Associate Editor: Rodrigo Ramos-JilibertoReceived January 2, 2011; accepted May 9, 2011

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