Small mammal assemblages in fragmented shrublandsof urban areas of Central Chile

Ignacio C. Fernández & Javier A. Simonetti

Published online: 25 October 2012# Springer Science+Business Media New York 2012

Abstract Mediterranean-type ecosystems are one of the most affected environments byhabitat loss and fragmentation due to urban development, however only few studies haveevaluated the effects of urbanization on the biodiversity of remnant fragments in theseecosystems. This study aims to evaluate the effects of urban development over smallmammal assemblages inhabiting isolated forest fragments of an urban area of ChileanMediterranean zone. We compared abundance and richness of small mammal assemblagesof six remnant fragments within an urban matrix, and six fragments similar in area andhabitat characteristics with those of urban area, but surrounded by a rural matrix. We foundthat small mammal assemblages differ considerably among fragments types (urban vs rural),with lack of endemic species from urban fragments and with high proportion of introducedrodents in urban fragments. Furthermore abundance of small mammals was higher in ruralthan in urban fragments. In urban areas small mammal abundance and richness were notcorrelated with any of the explanatory variables assessed (woody cover, flora heterogeneity,fragment area, perimeter/area ratio). However in rural fragments small mammal richness wasnegatively correlated with flora heterogeneity and the abundance of small mammals waspositively correlated with perimeter/area ratio. These results reveal important differenceswithin the effects of fragmentation over small mammal assemblages among the two types offragments assessed. Our findings suggest that in forest fragments isolated by urbanization,larger areas with good quality habitats are not sufficient to maintain native small mammalpopulation.

Keywords Habitat fragmentation . Urbanization . Vegetation remnants . Mediterraneanecosystems . Species invasion . Urban ecology

Urban Ecosyst (2013) 16:377–387DOI 10.1007/s11252-012-0272-1

I. C. Fernández (*)Departamento de Ecosistemas y Medio Ambiente, Pontificia Universidad Católica de Chile, VicuñaMackenna 4860, Casilla 306, Santiago, Chilee-mail: ifernanc@uc.cl

J. A. SimonettiDepartamento de Ciencias Ecológicas, Universidad de Chile, Las Palmeras 3425, Casilla 653, Santiago,Chile

Introduction

Loss and fragmentation of natural habitats are one of the most important drivers of thecurrent rate of species extinction (Tilman et al. 1994). The expansion of land use thataccompanies human population growth, including urban development, has led to a steadyloss and fragmentation of natural habitats throughout the world (Ellis et al. 2010). In 1900,only 9 % of the world’s human population lived in urban areas, increasing to 50 % by 2000,and is expected to be greater than 66 % by 2025 (McIntyre et al. 2000). The conversion ofland for urban development has divided wild habitats into small fragments, isolated by amatrix of inhospitable land uses such as paved roads and housing facilities. This negativelyimpinges biodiversity by decreasing connectivity and increasing mortality rate, among otherfactors (Sauvajot et al. 1998; Cavia et al. 2009).

Urban development and related human activities have significantly affectedMediterranean-type ecosystems, which are regarded as one of the five most disturbedbiomes in the world (Hannah et al. 1995). These ecosystems occur between 31° and 40°north and south of the Equator, and are characterized by warm wet winters and hot drysummers (Vogiatzakis et al. 2006). The five Mediterranean-climate regions of the world(Mediterranean Basin, Central Chile, the Cape Region of South Africa, SouthwesternAustralia, and parts of California) collectively cover less than 5 % of the Earth's landsurface, yet they harbor 20 % of the world’s flora and have exceptionality high rates ofendemic flora and fauna (Cowling et al. 1996).

Despite their importance for world biodiversity conservation, few studies have evaluatedthe effects of urbanization and related habitat fragmentation upon the biodiversity ofMediterranean-type ecosystems (Klausmeyer and Shaw 2009). These studies have largelyfocused on California, the Mediterranean Basin, and south-western Australia (e.g. Soulé etal. 1992; Bolger et al. 1997; Gibb and Hochuli 2002; Crooks et al. 2004), but the impacts ofurbanization upon the biota in Mediterranean ecosystems of South Africa and Chile havescarcely been addressed.

The Chilean Mediterranean zone harbors more than 80 % of the country’s urbanresidents. This ecosystem covers around 16 % of the Chilean continental territory, but ishome to approximately 50 % of Chile’s vertebrate species, 50 % of the Chilean endemicsand over 50 % of the endangered vertebrates, and is regarded as one of the 34 Biodiversityhot-spots of the world (Simonetti 1999; Arroyo et al. 2004). Urban sprawl has fragmentedvast expanses of natural habitats, and remnant fragments are threatened by current urbangrowth rates (Romero and Vásquez 2005). However, no studies have evaluated biodiversityin forest remnants of urban areas of the Mediterranean-type ecosystems in Chile, generatinga crucial information gap for developing management strategies for the biota associated withthese habitats fragments.

Small mammal assemblages may be particularly important in elucidating changes inbiodiversity in fragmented forests. Small mammals can play a key role influencingvegetation dynamics (e.g. Gutierrez et al. 1997), and may have strong influences on thepresence of a wide array of wildlife, either through competitive interactions or byserving as the prey base for carnivorous species, which are often of greater conservationconcern (e.g., Ekernas and Mertes 2006). The persistence of small mammals withinfragments will depend on factors such as the area and shape of the remaining fragmentsand the quality of the surrounding matrix as dispersal habitat (Bierwagen 2007).Furthermore the presence of small mammals in urban remnants might also haveimplications for human health, as many diseases (such as Hantavirus) are associatedwith their presence (Torres-Perez et al. 2004). Therefore, understanding changes in

378 Urban Ecosyst (2013) 16:377–387

richness and abundance of small mammals in urban remnants may contribute to thedevelopment of management strategies for biodiversity conservation in urban areas, aswell as to develop plans to avoid potential zoonotic risks.

In this study we assessed the small mammal assemblages in forest remnants in urbansettings of Santiago de Chile. We compared the richness and abundance of smallmammals between remnant fragments surrounded by an urban matrix, and fragmentssimilar in area and habitat characteristics surrounded by a rural matrix. First, todetermine whether the effects of fragmentation over small mammal assemblages aredependent on the surrounding matrix, we tested two hypotheses: (1) fragments locatedin a rural matrix will contain higher richness and abundance of small mammal speciesthan fragments surrounded by urban settings; (2) the proportion of invasive species willbe higher in fragments surrounded by urban matrix than those located in a rural setting.Second, we evaluated if (1) abundance and richness of small mammals is positivelyrelated to woody vegetation cover and floristic heterogeneity and, (2) if abundance andrichness of small mammals is positively related to fragment area and negatively relatedto perimeter/area ratio (fragment shape index).

Materials and methods

Study area

The study was carried out on the northeast area of Santiago de Chile (33°20′S-70°32′W), in aresidential zone named “La Dehesa” and in a contiguous rural area located at 10 km. to thenorthwest (Fig. 1). The climate is Mediterranean (with a long dry season) with a meanannual temperature of 13.9 °C, ranging from 22.1 °C in January to 7.7 °C in July. The meanannual precipitation is 356.2 mm. with approximately 80 % of the precipitation taking placein winter months (Rojas et al. 2004). La Dehesa is a relatively new residential zone (less than30 years old) composed mainly of low density housing, parks, golf courses and forestfragments embedded in the urban landscape. The rural landscape is mainly composed ofremnant fragments located in hill tops and riparian areas immersed in a shrub matrixdegraded by historical clearance for timber, charcoal and pastures. Currently these fragmentsare threatened by high development rates of new residential zones (Romero and Vásquez2005). The original vegetation in both areas is sclerophyllous vegetation, with a predomi-nance of shrub individuals in east, west and equatorial slopes, and a mixture of shrubs andtrees in polar-facing slopes (Arroyo et al. 2004).

Selection of fragments

Small mammal sampling was carried out in 12 fragments, all of them located on polar-facingslopes, half of them in urban areas and the other half in rural ones. Fragments were selectedusing satellite images on the basis of their area and vegetation cover, in order to havefragments of similar characteristic (Table 1). Two types of fragments were distinguisheddepending on the surrounding matrix: (1) urban: remnant fragments of native vegetationsurrounded in their entire perimeter by urban infrastructure (roads, housing, commercialfacilities), and (2) rural: fragments of native vegetation surrounded in all their perimeter byhighly degraded shrub community conformed almost entirely by sparse Acacia caven(espino) individuals, and that are at least at one km from an urbanized area. All fragmentswere at least at 0.5 km from a non-fragmented habitat.

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Table 1 Habitat attributes of fragments. Urban and Rural represent the matrix type surrounding the fragment.The four variables shown represent respectively: log. area in hectares; perimeter/area ratio; percentage offragment area covered by woody vegetation; average number of woody species present in vegetation transects

Fragment Log area Perimeter/area Vegetation cover Flora heterogeneity

Urban 1 0.155 0.038 0.830 6.250

Urban 2 0.609 0.027 0.938 5.750

Urban 3 0.766 0.033 0.849 4.750

Urban 4 1.135 0.021 0.754 4.750

Urban 5 1.754 0.009 0.742 4.500

Urban 6 1.758 0.008 0.556 4.000

mean (S.E.) 1.029 (0.263) 0.023 (0.005) 0.778 (0.053) 5.000 (0.342)

Rural 1 0.093 0.042 0.898 5.250

Rural 2 0.635 0.034 0.561 3.750

Rural 3 0.863 0.037 0.700 4.750

Rural 4 1.061 0.015 0.579 2.250

Rural 5 1.625 0.009 0.634 4.250

Rural 6 1.732 0.019 0.838 5.500

mean (S.E.) 1.001 (0.252) 0.026 (0.005) 0.702 (0.057) 4.292 (0.485)

Fig. 1 Study area in Central Chile. Grey surface is the current urban area of Santiago de Chile

380 Urban Ecosyst (2013) 16:377–387

Explanatory variables

We assessed four explanatory variables: area, perimeter/area ratio, woody cover (percent ofsurface covered by the canopy of trees and/or shrubs), and floristic heterogeneity of forestremnants (Table 1). The fragment’s area and perimeter were calculated from satellite images viaGoogle-Earth-Pro™ GIS tools (available at http://www.google.com/intl/en/earth/businesses).Woody vegetation cover was estimated through line interception method (Eberhardt 1978),with four 50 m’s transects randomly placed in each fragment. Floristic heterogeneity wasestimated as the mean number of tree and shrub species present in transects.

Small mammal sampling

Small mammal richness and abundance were assessed through live captures using Shermantraps. Traps were placed in one transect per fragment. Each transect consisted of 18 doublestations (pair of traps) separated by 10 m. Transects were positioned in a disposition thatmaximizes the distance to the fragment borders.

In 2007, three capture sessions (September, October–November and December) of fournights, were conducted for each site, totaling 5,184 trap/nights throughout the study.Captured individuals were identified to species level, individually marked and released atthe capture site. We used direct enumeration estimates of small mammal abundance as noassumption of homogeneity of recapture probabilities is required (Simonetti 1986)

Results

Fragment vegetation

Total woody cover was similar in the two habitat types (two tailed t-test; p00.35).Vegetation cover ranged from 56.1 % to 89.8 % in rural fragments, and from 55.6 % to93.8 % in urban fragments (Table 1). The most frequent species in both fragment types wereone endemic tree, Quillaja saponaria (quillay), and two endemic shrub, Lithrea caustica(litre) and Colliguaja odorifera (colliguay). These three species accounted for 68.74 % ofrelative cover in urban sites, and 72.03 % in rural sites (Table 2).

Urban remnants presented higher vegetation richness than rural fragments. While urbanfragments harbored a total of 26 species, 16 were found in rural sites. More than half of theplant species recorded in urban fragments were present only in one fragment, and in mostcases were represented by only one individual (Table 2). A total of five exotic plant specieswere found, all of them in urban fragments. The exotic species accounted for 11.85 % ofvegetation cover in urban fragments. Rubus ulmifolius (zarzamora) was the most frequentand abundant exotic species, occurring at three out of six urban fragments and accounting for9.11 % of vegetation cover.

Small mammal composition

A total of eight small mammal species were recorded, including five species of nativerodents, two of them endemics, two introduced rodent species and one endemic marsupial.Six out of these eight species occurred in rural fragments and five were present in urbanfragments. Assemblage richness ranged from 1 to 6 species in rural fragments, and from 0 to4 species in urban fragments, with no captures in two urban fragments (Table 3).

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Small mammal composition differed between rural and urban fragments (Morista–Hornindex 0 0.35). Only three species were present in both fragment types: the two native rodentsAbrothrix olivaceus (olive grass mouse) andPhyllotis darwini (Darwin’s leaf eared mouse), andthe introduced Rattus rattus (black rat). Furthermore, the three endemic species present in ruralfragments, Abrocoma benetti (Bennett’s chinchilla rat), Octodon degus (degu) and Thylamyselegans (mouse opposum), were absent from urban fragments, and the introduced Musmusculus (house mouse) was found only in urban fragments. The native rodentOligoryzomys longicaudatus (long tailed mouse), which is the principal Hantavirus vector,was absent in rural fragments, but two individuals were captured in an urban fragment (Table 3).

Table 2 Presence and relative coverage of woody species in urban and rural fragments

Urban Rural

NFS Coverage NFS Coverage

Lithraea caustica 6 33.05% 6 25.88%

Quillaja saponaria 4 20.52% 5 11.74%

Colliguja odorifera 4 15.17% 5 34.41%

Rubus ulmifoliusa 3 9.11% np 0%

Acacia caven 4 4.84% 4 8.82%

Cestrum palqui 6 4.52% 3 4.33%

Azara dentata 2 4.17% np 0%

Pinus radiataa 1 1.88% np 0%

Baccharis empetrifolia 1 1.80% np 0%

Kageneckia oblonga 3 1.49% 3 2.30%

Baccharis pingraea 2 0.77% 1 2.03%

Salix babylonicaa 1 0.39% np 0%

Tristerix sp. 1 0.27% np 0%

Talguenea quinquinervia 1 0.27% np 0%

Salix humboldtianaa 1 0.26% np 0%

Podanthus mitique 1 0.24% 3 0.67%

Populus nigraa 1 0.21% np 0%

Colletia spinosissima 1 0.21% np 0%

Azara celastrina 1 0.17% np 0%

Trevoa quinquinervia 1 0.17% 1 0.22%

Berberis chilensis 1 0.13% np 0%

Azara integrifolia 1 0.13% np 0%

Porlieria chilensis 1 0.13% 3 3.97%

Proustia cuneifolia 1 0.07% 3 3.08%

Cuscuta sp. 1 0.03% np 0%

Maitenus boaria 1 0.03% 1 0.90%

Cissus striata np 0% 1 1.13%

Aristotelia chilensis np 0% 1 0.24%

Retanilla trinervia np 0% 1 0.21%

Escalonia illinita np 0% 1 0.08%

NFS Number of fragments where the species was present, np not presenta Introduced species

382 Urban Ecosyst (2013) 16:377–387

Small mammal abundance

A total of 83 individuals were captured. Abundance of small mammals was higher inrural than in urban fragments, with 83 % of all captures occurring in rural fragments.Abundance per fragment ranged from 1 to 29 individuals in rural fragments, and from 0to 7 individuals in urban fragments (Table 3). Phyllotis darwini was the most abundantspecies in rural fragments, with 36 individuals, accounting for more than 50 % ofcaptures. In urban fragments, only two species, the native A. olivaceus and theintroduced R. rattus, reached more than three individuals (Table 3). Introduced rodentswere more frequent in urban than rural zones (p<0.05 two sample proportion test).While in urban fragments 50 % of individuals captured were introduced species, in ruralremnants this proportion was only 20 %. All introduced rodents captured in ruralfragments were R. rattus (Table 3).

Small mammal response to vegetation variables

Small mammal richness and abundance were unrelated to vegetation cover or to floristicheterogeneity in urban fragments (Fig. 2). In rural fragments small mammal richness wasunrelated to vegetation cover, but showed a negative relation to floristic heterogeneity(Fig. 2c, d). Small mammal abundance was not related to vegetation cover or to floristicheterogeneity in rural fragments (Fig. 2a, b).

Small mammal response to spatial variables

Richness and abundance of small mammal assemblages were not correlated with spatialvariables in urban fragments. Neither the area (log transformed) nor the perimeter/arearelation of fragments accounted for small mammal abundance and richness in urban frag-ments (Fig. 3). In rural fragments, small mammal abundance and richness were not

Table 3 Small mammal assemblages in assessed fragments. Small mammal numbers represent individualscaptured in each fragment

Small mammals species Distribution Individuals per fragment

Urban Rural

1 2 3 4 5 6 Total 1 2 3 4 5 6 Total

Marsupialia

Thylamys elegans Endemic 0 0 0 0 0 0 0 0 1 0 1 3 0 5

Rodentia

Abrocoma benetti Endemic 0 0 0 0 0 0 0 0 1 0 1 1 0 3

Abrothrix olivaceus Native 0 0 3 1 0 0 4 0 0 0 1 0 0 1

Oligoryzomys longicaudatus Native 0 0 2 0 0 0 2 0 0 0 0 0 0 0

Phyllotis darwini Native 0 0 1 0 0 0 1 0 0 1 17 16 2 36

Octodon degus Endemic 0 0 0 0 0 0 0 0 0 0 5 5 0 10

Rattus rattus Introduced 0 1 0 0 0 3 4 2 6 0 4 0 2 14

Mus musculus Introduced 0 2 1 0 0 0 3 0 0 0 0 0 0 0

Total per fragment 0 3 7 1 0 3 14 2 8 1 29 25 4 69

Urban Ecosyst (2013) 16:377–387 383

correlated with fragment area (Fig. 3a, c). Species richness is not correlated to the perimeter/area ratio of rural fragments, but abundance is negatively correlated to it (Fig. 3b).

a) b)

c) d)

smal

l mam

mal

s re

spon

se

vegetation cover florístic heterogeneityindependent variables

abun

danc

eri

chne

ss

Rural: R2 = 0.40 (p=0.17)

Urban: R2 = 0.03 (p=0.76)

0

5

10

15

20

25

30

50% 60% 70% 80% 90% 100%

Rural: R2 = 0.51 (p=0.11)

Urban: R2 = 0.13 (p=0.48)

0

1

2

3

4

5

6

7

50% 60% 70% 80% 90% 100%

Rural: R2 = 0.62 (p=0.06)

Urban: R2 = 0.06 (p=0.64)

0

5

10

15

20

25

30

2 3 4 5 6 7

Rural: R2 = 0.79 (p= 0.02)

Urban: R2 = 0.01 (p=0.80)

0

1

2

3

4

5

6

7

2 3 4 5 6 7

Fig. 2 Scatterplots showing relationship between small mammal abundance and richness, and vegetationcover and floristic heterogeneity. (white circle) rural, (black up-pointing triangle) urban. Linear regressioncoefficient (R2), p-value, and regression lines are shown. Dotted line; rural, dashed line; urban

a) b)

c) d)

independent variables

smal

l mam

mal

s re

spon

se

perimeter/area

abun

danc

eri

chne

ss

log. area

Rural: R2 = 0.16 (p=0.43)

Urban: R2 = 0.01 (p=0.86)

0

5

10

15

20

25

30

4 5 6

Rural: R2 = 0.13 (p=0.48)

Urban: R2 = 0.05 (p=0.68)

0

1

2

3

4

5

6

7

4 5 6

Rural: R2 = 0.65 (p<0.05)

Urban: R2 = 0.06 (p=0.65)

0

5

10

15

20

25

30

0,00 0,01 0,02 0,03 0,04

Rural: R2 = 0.56 (p=0.09)

Urban: R2 = 0.13 (p=0.48)

0

1

2

3

4

5

6

7

0,00 0,01 0,02 0,03 0,04

Fig. 3 Scatterplots showing relationship between small mammal abundance and richness, and log. area andperimeter/area ratio. (white circle) rural, (black up-pointing triangle) urban. Linear regression coefficient (R2),p-value, and regression lines are shown. Dotted line; rural, dashed line; urban

384 Urban Ecosyst (2013) 16:377–387

Discussion

Small mammal assemblages persisting in remnant fragments of central Chile differ depend-ing if the surrounding matrix is urban or rural. Compared with the fragments immersed in arural matrix, small mammal assemblages of urban fragments have smaller abundance andrichness, lack endemic species, and have a significantly high proportion of invading rodents.This reveals the multiple effects that urbanization might have for wildlife habiting inremnant fragments. In fact habitat loss and fragmentation due to urban development mighthave significant consequences to wildlife because it results in permanent changes to theenvironment for which there is little chance for recovery. Furthermore, habitat loss andfragmentation due to urbanization brings with it myriad other threats to remnant habitatfragments that exacerbate impacts on biodiversity (Markovchick-Nicholls et al. 2008).

The abundance of small mammals in continuous natural shrublands near to the study area(~0.05 individual/trap-night) is higher than that recorded at rural and urban fragmentedlandscapes (see Jaksic et al. 1981; Iriarte et al. 1989). That is twice the capture rate of ruralfragments (0.026 individual/trap-night), and 10-fold higher of urban fragments (0.005individual/trap-night). This pinpoint to a consistent reduction of small mammal populationin fragmented habitats, also strengthening the difference of fragmentation effects amongrural and urban fragments. Factors that may account for a lower abundance in urbanfragments include higher predation pressures by pets (Soulé et al. 1992), competitiveexclusion by introduced rodents (Tikhonova et al. 2006), and a hard-to-disperse matrix(Verbeylen et al. 2003; Umetsu and Pardini 2007).

The abundance of native small mammals is positively correlated with shrub vegetationcoverage in central Chile (Meserve 1981; Simonetti 1989; Kelt et al. 1994), however thisrelation did not hold for any of the two habitats assessed. This fact may be explained becauseof differences in the fragment’s vegetation structure. The importance of vegetation structurecould be supported by the finding of a negative relation of small mammal abundance andrichness with floristic heterogeneity in rural fragments. Since higher floristic heterogeneityfragments was related to the presence of shrubs (e.g. C. odorifera, L. caustica and P.chilensis) and trees (e.g. Q. saponaria and A. caven), and lower floristic heterogeneitywas related mainly to the presence of shrub species, it seems that small mammals preferfragments with a high proportion of shrub species that offer protection against predators(Simonetti 1989).

The three most abundant species in urban fragments, R. rattus, A. olivaceus and M.musculus are omnivorous (Silva 2005), suggesting that urban remnants are suitable largelyfor species exhibiting a wide trophic niche. Furthermore, remnant fragments embedded in anurban matrix are invaded by exotic flora, which increases vegetation richness, but decreasescoverage of native vegetation (Guirado et al. 2006). These changes might reduce habitatquality for small mammal composition in urban remnants, as endemic small mammals tendto occupy native vegetation areas, whereas invading rodents are suitable to occupy areas ofnon-native vegetation (Sauvajot et al. 1998; Umetsu and Pardini 2007).

Oligoryzomys longicaudatus, the main reservoir of Hanta-virus in Chile, is normallypresent in natural and rural landscapes of central Chile, but not in urban areas (Torres-Pérezet al. 2004). However our results show their presence only in urban areas. Its absence in ruralareas could be explained because O. longicaudatus have high demographic fluctuations,with high abundance in autumn-winter and near zero in spring-summer (the period of ourcaptures), a time where they could move into more humid habitat, such as creeks (Kelt et al.1994). This yearly habitat shift might also explain its presence in urban settings, wherewatering of residential and park vegetation might create a suitable habitat for them. Indeed,

Urban Ecosyst (2013) 16:377–387 385

the two individuals were recorded next to a residential park, suggesting that urban fragmentscould offer year-round affordable resources for this zoonotic species.

The lack of relationship between small mammal abundance and richness and fragmentarea suggests a “small island effect”, which characterizes some fragmented systems that arefrequently disturbed or have limited habitat diversity (Kelt 2000), and may reflect theprotracted human impacts in this region (Aschmann 1991). Furthermore, fragment shapecould mask area effects, as irregularly shaped fragments have reduced proportion of suitablecore habitat and may be perceived as edge rather than a suitable habitat. Indeed our resultsshow that the perimeter/area ratio was a good predictor for fauna abundance in ruralfragments, suggesting that small mammals attempt to reduce contact with the matrix,preferring simple shape fragments that maximize suitable core habitat.

This is the first work evaluating the effects of fragmentation by urbanization over smallmammals in Chile, so these results might be taken as a first approach to fill the currentlyexisting gap of information in this topic, especially relating to the development of conser-vation strategies for urban remnants. Our work suggests that, at least at our study scale,remnants isolated-by-urbanization might not be able to support viable populations of nativesmall mammals. If attempts are made to protect the native small mammal fauna of urbanremnants, habitat management ought to consider not only fragments with greater sizes, butalso their shape, vegetation structure and patch interconnections.

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