Sharp Altitudinal Gradients in Magellanic Sub-Antarctic Streams: Patterns Along a Fluvial System in the Cape Horn Biosphere

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Contador, T., Kennedy, J.H., Ojeda, J. Rozzi, R. (2015). Sharp altitudinal gradients in Magellanic Sub-Antarctic streams: patterns along a fluvial system in the Cape Horn Biosphere...

Article in Polar Biology · June 2015 Impact Factor: 1.59 · DOI: 10.1007/s00300-015-1746-4

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Available from: Ricardo Rozzi Retrieved on: 14 April 2016 Sharp altitudinal gradients in Magellanic Sub-Antarctic streams: patterns along a fluvial system in the Cape Horn Biosphere Reserve (55°S)

Tamara Contador, James H. Kennedy, Ricardo Rozzi & Jaime Ojeda Villarroel

Polar Biology

ISSN 0722-4060

Polar Biol DOI 10.1007/s00300-015-1746-4

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Polar Biol DOI 10.1007/s00300-015-1746-4

ORIGINAL PAPER

Sharp altitudinal gradients in Magellanic Sub-Antarctic streams: patterns along a ﬂuvial system in the Cape Horn Biosphere Reserve (55°S)

1,2,3,6 1,2,3,4 1,2,3,5,6 Tamara Contador • James H. Kennedy • Ricardo Rozzi • Jaime Ojeda Villarroel1,2,3,6

Received: 17 July 2014 / Revised: 20 June 2015 / Accepted: 22 June 2015 Ó Springer-Verlag Berlin Heidelberg 2015

Abstract Magellanic Sub-Antarctic streams run through Antarctic watershed is characterized by a sharp thermal steep, low-altitude mountainous gradients characterized by gradient, in which cumulative degree-days (°C) per year a topography that supports a mosaic of evergreen, mixed, sharply increase through a relatively short altitudinal gra- and deciduous forests, peat lands, and scrublands. Here, the dient (0–600 m above sea level). With the results from this macroinvertebrate fauna and their ecological interactions study, we can now study thermal tolerances of altitude- are poorly known. This study linked the distribution, restricted species or project changes in their distributions community composition, and functional feeding structure and voltinism patterns according to climate change sce- of benthic macroinvertebrates with physicochemical and narios. Ecosystems at higher latitudes and altitudes are thermal patterns along the altitudinal gradient of a Mag- experiencing some of the fastest rates of warming on the ellanic Sub-Antarctic watershed. Invertebrates were col- planet, and Magellanic Sub-Antarctic watersheds could be lected during the austral summers of 2008, 2009, and 2010 considered as ‘‘sentinel systems,’’ providing early warning at ﬁve different altitudes. Our results indicate that benthic of wider scale change. macroinvertebrate community distributions are predomi- nantly affected by temperature and certain species show Keywords Altitudinal gradient Benthic distribution restrictions through the altitudinal gradient macroinvertebrate Sub-AntarcticÁ Functional feeding Á Á studied. Temperature proﬁles indicate that this Sub- group Climate change Á

Introduction Electronic supplementary material The online version of this article (doi:10.1007/s00300-015-1746-4) contains supplementary The Sub-Antarctic Magellanic ecoregion, immersed within material, which is available to authorized users. the South American temperate forest biome, has been identified as one of the 24 true wilderness areas remaining & Tamara Contador [email protected]; [email protected] on the planet. More than 70 % of the original vegetation cover is still extant, over an area greater than 10,000 km2, 1 Universidad de Magallanes, Avenida Bulnes, which lacks significant industrial and urban development 01855 Punta Arenas, Chile (Mittermeier et al. 2003). It spans a myriad of archipela- 2 Sub-Antarctic Biocultural Conservation Program, goes from 47°S to 56°S unique in the world, in a latitudinal Punta Arenas, Chile range of almost 10° well to the south of the southernmost 3 Omora Ethnobotanical Park, Puerto Williams, Chile forests in New Zealand and Australia (Rozzi et al. 2012). 4 Department of Biological Sciences, University of North Furthermore, South American Sub-Antarctic ecosystems Texas, Denton, TX, USA sharply contrast with their northern hemisphere latitudinal 5 Department of Philosophy and Religion Studies, University counterparts in terms of the land-to-ocean ratio, generating of North Texas, Denton, TX, USA sharp inter-hemispheric climatic and biotic differences in 6 Instituto de Ecologıá y Biodiversidad-Chile, Santiago, Chile temperate and subpolar latitudes (Rozzi et al. 2012).

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Southern South America’s Sub-Antarctic freshwater the heterogeneity in habitats and marked gradients in ecosystems temperature and rainfall over a relatively small land area (Rozzi et al. 2012). Among the freshwater fauna, inverte- South America’s Sub-Antarctic freshwater ecosystems are brates are strongly affected by thermal variation across positioned in a region shaped by the glacial erosion of the latitudinal and altitudinal scales (Sweeney et al. 1990). The continent during the Last Glacial Maximum, between thermal environment directly affects their metabolism and 23,000 and 19,000 BP (Hulton et al. 2002). In contrast with growth rates, and hence their ability to survive when high-latitude environments in the northern hemisphere, temperature variation exceeds their range of thermal tol- these ecosystems present marked changes in microclimate erance (Ward and Stanford 1982). Thus, obtaining basic with small changes in elevation. The modulating effect of information about the diversity, distributions and life his- the ocean drastically diminishes with altitude, and the tree tory of freshwater benthic macroinvertebrates associated line appears at only 600 m above sea level (Rozzi et al. with Magellanic Sub-Antarctic rivers are extremely 2010). These steep altitudinal gradients are characterized important to assess the possible implications of climate by a diverse topography that supports evergreen forests, change in this region of the world. mixed evergreen/deciduous forests, peat lands, grasslands, The goals of this study were to: (1) provide a concise and scrublands over a relatively small area (Pisano 1980). description of the benthic fauna associated to the steep Marked topographic and climatic barriers have isolated this altitudinal gradient of a Sub-Antarctic fluvial system in the austral vegetation from the nearest subtropical forests by Cape Horn Biosphere Reserve, Chile (55°S); (2) to assess 1500–2000 km, generating high levels of endemism and a the relationships between richness, density, and distribution unique biodiversity of vertebrates, invertebrates, and non- of benthic macroinvertebrates with temperature and other vascular and vascular plants (Armesto et al. 1998; Rozzi physicochemical variables along the altitudinal gradient; et al. 2012). For example, close to 90 % of woody plant and (3) to provide the basis for future research regarding species, 33 % of woody genera, and about 60 % of bryo- southern South American Sub-Antarctic freshwater phyte species (mosses and liverworts) are endemic to this ecosystems in the context of climate change. region (Rozzi et al. 2012). Indeed, the Sub-Antarctic ecoregion is a ‘‘hotspot’’ of bryophyte biodiversity, one factor that led UNESCO to declare the territory and its Materials and methods waters the Cape Horn Biosphere Reserve. Overall, though, despite the unique biogeographic setting and the high fre- Study area quency of endemisms encountered to date, the biological richness of the Cape Horn archipelago and the Magellanic The Ro´balo River (54°S, 067°W), with an extension of Sub-Antarctic ecoregion is understudied (Contador et al. approximately 12 km, runs through the altitudinal gradient 2012). Many areas have not been systematically explored, of the Dientes of Navarino mountain range, located on even on small, well-defined, and accessible land masses, Navarino Island (55°S). The river provides drinking water and many of the less charismatic taxa, such as aquatic to the city of Puerto Williams, Capital of the Chilean insects, have barely been surveyed at all (Convey and Antarctic Province and the world’s southernmost town. Stevens 2007; Contador et al. 2012). Navarino Island lies south of the Beagle Channel and north Furthermore, climate change is affecting not only polar of Cape Horn (Fig. 1). The Cape Horn archipelago became regions but also subpolar regions. For example, models of the Cape Horn Biosphere Reserve (CHBR) in 2005, and it temperature change for New Zealand predict the shrinking hosts the world’s southernmost-forested ecosystem, and ultimate disappearance of South Island glaciers, encompassing all of the islands south of the Beagle resulting in the lost of habitats suitable for cold-water Channel, as well as the Chilean portion of Tierra del Fuego specialists (Winterbourn et al. 2008). Additionally, Island located south of the highest peaks in the Darwin although the system of South America’s Sub-Antarctic Mountain Range (Rozzi et al. 2010). The study site lies channels and fjords houses one of the most important ice within this biosphere reserve and the Omora Ethnobotani- fields after Antarctica, the loss of mass and freshwater cal Park, part of Chile’s long-term socio-ecological input has been dramatic in recent years due to global research sites (LTSER) network (Rozzi et al. 2010). It warming (Porter and Santana 2003). In this context, the belongs to the Magellanic Sub-Antarctic ecoregion (Mit- Sub-Antarctic islands of southern South America provide a termeier et al. 2003), which has a strong dominance of unique opportunity for understanding the past and present Austral and also Nearctic and Brasilic elements (Mis- climate change in the southern hemisphere to assess its erendino and Pizzolon 2000). consequences to the biota. Comparative studies of the The forests of this region are composed primarily of responses of the biota to climate change are facilitated by three members of the genus Nothofagus (Pisano 1980) and

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Fig. 1 Map of Navarino Island showing its location within the Cape Horn Biosphere Reserve. The map details the location of the Ro´balo River watershed, located on the north side of the island. Sampling sites along the watershed are shown are part of the South American temperate forest biome, Puerto Williams is 6.0 °C and 467.3 mm, respectively, and occurring along a narrow but latitudinally extensive strip of the warmest months have an average temperature of 9.6 °C land between 35° and 55°S (Armesto et al. 1998). The (January–March), while the coldest months average 1.9 °C north portion of the biome is delimited by the Mediter- (May–August) (Contador 2011). ranean-type scrublands and the hyper-arid Atacama Desert, while to the east lies the Patagonian steppe, and westward Sampling sites and southward, the Pacific Ocean (Rozzi et al. 2012). The regional climate depends on polar weather fronts Five sampling sites, separated by approximately 100 m of from the South Pacific, and it is strongly affected by the altitude, were selected according to visually sharp changes in westerly storm tracks coupled with precipitation induced vegetation, habitat, and landscape (Fig. 2, Table 1) along the by the high western flanks of the Andean Cordillera altitudinal gradient of the Ro´balo River watershed, which (McCulloch et al. 1997). The Ro´balo River watershed is ascends from sea level to 600 m above sea level (m.a.s.l). found within the influence of the trans-Andean with steppe This gradient includes the characteristic habitat types of the degeneration climatic zone. It represents a transition Cape Horn region. From the shoreline upward, these habitats between rain climates of the western coast of Magallanes are: evergreen forests dominated by Nothofagus betuloides; and the steppe climates of the eastern side of the mountain mixed evergreen-deciduous forests dominated by N. betu- range (Rozzi et al. 2010). The uniformity of the seasonal loides and N. pumilio; deciduous forests dominated by N. variation of precipitation as well as its thermal character- pumilio and N. antarctica; alpine tundra dominated at lower istics allow for the growth of deciduous forests. The levels by cushion plants, e.g., Bolax gummifera; and at upper average annual temperature and precipitation recorded for levels by lichens such as Neuropogon sp. (Fig. 2).

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Fig. 2 Detail of altitudinal gradient and sampling sites through the Ro´balo River watershed. Sampling sites are represented with Roman numerals I–V and range from 120 to 586 m.a.s.l. Sampling site V was selected as a permanent sampling site and is being monitored in the long term. Figure modiﬁed from Rozzi et al. (2010)

Table 1 Sampling sites Site Description Altitude (m) GPS location selected along the altitudinal gradient of the Ro´balo River I Headwaters 586.0 S54° 59.6740, W067° 40.8780 watershed to perform characterization of benthic II Laguna del Salto 486.0 S54° 59.5200, W067° 40.8690 macroinvertebrate fauna III Laguna de la Tortuga 380.0 S54° 59.2250, W067° 40.8580

IV Former beaver dam 240.0 S54° 58.2890, W067° 39.9260

V Downstream 120.0 S54° 57.1060, W067° 38.6060 Sites were all located along the river, in lotic habitats. The names given in the description for each site are locally known and do not characterize the type of habitat sampled (i.e., laguna)

Habitat characterization and physicochemical temperature (°C), and conductivity (lS) were recorded characteristics three times at each transect using a YSI 85 m. HOBOÒ data loggers, Model U22 Water Temp Pro version 2, were Physical characteristics were recorded for each sampling permanently installed at each altitudinal location starting site. At each site, a 100-m reach was selected and divided on January of 2009 until the present. Average, maximum, into 10 transects of 10 m each. The riparian environment and minimum daily temperatures (°C) are recorded con- along each reach was evaluated by recording the bank tinuously every 5 h at each sampling site. Average daily slope (°), riparian vegetation composition (%), and percent water temperature (°C) was calculated for each site using tree canopy cover (%), as well as stream depth (m) and the information retrieved from the HoboÒ data loggers. width (m). The bank slope and percent tree canopy cover Cumulative degree-days (CDD) for each site were com- were obtained using a clinometer and a concave spherical puted using the Modified Sine Wave Method with densiometer, respectively. Substrate characterization was HobowareÒ Pro Software, version 3.5.0, following Snyder carried out using Wolman pebble counts to quantify par- et al. (2001). ticle size distribution (Harrelson et al. 1994). At each transect, 100 randomly selected points were chosen and the Benthic macroinvertebrate sampling diameter of the substrate type was measured. These values and identification were then used to determine substrate diversity by applying a Shannon–Wiener Diversity Index to the abundance of Benthic macroinvertebrates were collected during the particular size classes of substrate found during the pebble austral summers (January) of 2008, 2009, and 2010. Three counts (Anderson and Rosemond 2007). samples were taken from riffle habitats at each site using a Water chemistry parameters were recorded at the time Surber sampler (0.09 m2) with a 243-lm mesh net. Each of each sampling event. Dissolved oxygen (mg/L), water sample was stored in 70 % ethanol and transported to the

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Polar Biol laboratory for processing. A malaise net was also set at against violations of the symmetry assumption of repeated- each site to capture adult representatives of the organisms, measures ANOVA. When significance was achieved, a to be used as an aid to identify to the lowest taxonomic Tukey HSD multiple comparisons test was used (Zar level possible. The traps were deployed during the late 2010). Two-way repeated-measures ANOVAs and Tukey evening and left throughout the night at each sampling site HSD tests were also used for community measures and and period, except for site I (586 m.a.s.l), where high FFG density to identify any significant differences between winds and habitat conditions did not allow for the setting of sampling sites and years (altitude, year). the trap. Benthic macroinvertebrates were identified to the A principal components analysis (PCA) was applied to lowest taxonomic level, and functional feeding groups examine the linear combinations of environmental variables (FFG), (collector-gatherer, filterer, predator, shredder, and (substrate diversity H0, temperature, and conductivity) that scraper) were determined using the best available litera- best explained the distributions of benthic macroinverte- ture, including but not limited to, Miserendino and Piz- brates along the altitudinal gradient. Aquatic insect taxa zolon 2000, Merritt and Cummins 2007, Merritt et al. included in PCA were those that made up more than 90 % of (2008), Domıńguez and Fernańdez (2009). Samples col- the total density at each site, which were estimated via lected with the Surber were used to estimate community SIMPER (similarity percentage, software PRIMER-E 5.0, composition and density (organisms m-2), while organisms Ltd. Plymouth, UK). Non-insect benthic macroinvertebrate identified from the malaise traps were used to complement fauna was not included in the analysis. A multiple Max R existing taxonomic lists of benthic macroinvertebrates. stepwise regression procedure was used to identify the best set of environmental variables that explained variation in Community measures benthic macroinvertebrate taxa. Statistical analyses were conducted with Statistica version.7.0 (Statsoft Inc. 2004) The following metrics were measured for each site using software package, R software, version 2.9.2, and JMPÒ sample means to assess benthic macroinvertebrate com- 9.0.1. Autocorrelation of variables was tested before pro- munity structure along the altitudinal gradient: (1) taxo- ceeding with PCA and Max R2 analysis. nomic richness; (2) density (organisms m-2); and (3) Pielou’s evenness index (J). Pielou’s evenness index was calculated using DiversityAS software, version 1.6.2. Results Benthic macroinvertebrate densities (organisms m-2) were graphed using the beanplot method, as described by Habitat characterization Kampstra (2008), using R software, version 2.9.2. This method was preferred over a boxplot, because a boxplot As expected, sites at lower altitudes (120, 240, 380 m.a.s.l) and its variant make use of the median of a group of data had a higher percentage of tree canopy cover than sites at points, while the beanplot method uses the average of the higher altitudes (486 and 586 m.a.s.l). Substrate diversity group and also shows an overall average, giving the (Shannon’s H0) increased toward the mouth of the Ro´balo information in the form of a density trace (Kampstra 2008). River, and it was highest at site V (120 m.a.s.l) (Table 2). Stream width (m), depth (cm), and bank slope (°) Statistical analyses increased with decreasing altitude (Table 2). The yearly water temperature (°C) range was higher for sites at lower All tests to determine statistical significance were set at a altitudes. The highest water temperature (17 °C) was level of 0.05. Before proceeding with parametric analysis, recorded at site V (120 m.a.s.l). Cumulative degree-days normality was tested using Shapiro–Wilks tests and (CDD) significantly decreased with altitude, with CDD at homogeneity of variances was tested using a Hartley’s site V (120 m.a.s.l) being 6 9 higher than the CDD

Fmax ratio test. If assumptions for normality or homo- recorded for site I (586 m.a.s.l, Table 2; Fig. 3). geneity of variances were not met, a log transformation On average, conductivity ranged from 26 lS at high alti- [log10(x ? 1)] was used and data were reexamined for tudes to 60 lS at lower altitudes (Table 2), while dissolved normality (Crawley 2007, Zar 2010). oxygen (mg/L) and pH did not vary significantly throughout Significant trends for physicochemical parameters along the gradient (8.9–12.6 mg/L; 8.3–8.9, respectively, Table 3). the altitudinal gradient were identified with two-way (altitude, year) repeated-measures analysis of variance Benthic macroinvertebrate richness (two-way repeated-measures ANOVA). Mauchly’s test of along the altitudinal gradient of the Ro´balo River sphericity was applied to test for the assumption of sphericity. If sphericity was not met, a Greenhouse-Geisser A total of 45 benthic macroinvertebrate taxa were identi- correction procedure was used to protect significance levels fied along the altitudinal gradient of the Ro´balo River

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Table 2 Description of physical habitat variables along the altitudinal gradient of the Ro´balo River watershed, Navarino Island (55°S) Altitude (m.a.s.l) 120 240 380 486 586

Non-vascular herbaceous cover (%) Left bank 7.6 10.3 2.9 11.4 29.4 Right bank 12.0 4.4 0.0 9.9 38.5 Vascular herbaceous cover (%) Left bank 54.8 36.8 44.9 49.2 12.8 Right bank 26.1 48.5 52.2 29.5 19.4 Dominant vegetation type Evergreen forest Mixed forest Deciduous forest Krummholz Alpine tundra

Substrate diversity (H0) 2.0 1.9 1.9 1.8 1.5 Substrate type (%) Very ﬁne gravel (0.2–0.4 cm) 1.0 0.0 0.0 0.0 0.0 Fine gravel (0.4–0.8 cm) 3.0 0.0 0.0 0.0 0.0 Medium gravel (0.8–1.6 cm) 8.9 1.0 1.0 0.0 0.0 Coarse gravel (1.6–3.2 cm) 25.7 20.4 5.0 11.0 0.0 Very coarse gravel (3.2–6.4 cm) 31.7 33.7 24.0 22.0 0.0 Small cobble (6.4–9.0 cm) 11.9 21.4 17.0 16.0 0.0 Medium cobble (9.0–12.0 cm) 9.9 5.1 15.0 17.0 0.0 Large cobble (12.8–18 cm) 7.9 11.2 10.0 10.0 8.0 Very large cobble (18.0–25.6 cm) 0.0 6.1 2.0 3.0 12.0 Small boulder (25.6–51.2 cm) 0.0 1.0 1.0 0.0 3.0 Large boulder (102.4–204.8 cm) 0.0 0.0 25.0 21.0 77.0 Stream width (m) 8.5 (3.3) 8.8 (2.1) 2.8 (0.9) 2.3 (0.9) 2.6 (0.4) Stream depth (cm) 29.0 (5.2) 28.3 (5.8) 13.4 (2.6) 7.7 (2.8) 6.8 (1.1) Bank slope (°) Left bank 31.7 (6.7) 24.0 (2.0) 12.7 (11.2) 16.1 (4.9) 6.6 (1.3) Right bank 18.6 (12.6) 14.3 (7.9) 22.2 (9.7) 4.8 (4.6) 10.0 (3.7) Yearly average temperature (°C) 5.70 (4.16) 4.59 (3.72) 2.72 (2.04) 1.42 (1.84) 1.02 (0.71) Annual degree-days ([0 °C) 2051.0A 1650.0B 974.0C 508.0D 365.0E Physicochemical parameters Conductivity (lS) 47.5 (14.7) 39.3 (17.1) 36.3 (11.6) 46.3 (16.3) 29.3 (4.5) Dissolved oxygen (mg/L) 12.4 (1.2) 12.3 (1.4) 11.3 (2.3) 10.6 (1.1) 10.6 (1.3) pH 8.5 (0.3) 8.6 (0.2) 8.5 (0.3) 8.6 (0.3) 8.4 (0.2)

Means (±SE) are provided for stream depth and width, bank slope, conductivity (lS), dissolved oxygen (mg/L), and pH. Annual degree-days along the altitudinal gradient were compared with a one-way ANOVA (a = 0.05) and significant differences are shown by the letters A through E watershed. These taxa included 17 genera and nine species, Benthic macroinvertebrate density with the remaining taxa being identified to order or family level (see Online Resource 1). Site III (380 m.a.s.l) had the Mean density (individuals m-2) was not significantly dif- highest total richness (35), while site I (586 m.a.s.l) had the ferent between sampling years, but it was highly signifi- lowest total richness (22) (Online Resource 1). Mean cantly different along the altitudinal gradient (repeated- richness was significantly different between altitudes and measures ANOVA, p \ 0.0001, Mauchly’s test of sampling years (repeated-measures ANOVA, p = 0.0001, sphericity, Mauchly criterion = 0.49, p = 0.04, Green- Mauchly’s test of sphericity, Mauchly criterion = 0.99, house-Geisser correction factor 0.66, corrected df = 5.29, p = 0.98). Benthic macroinvertebrate richness was sepa- p = 0.53), and it was separated into three statistically rated into two significantly different groups through the significant groups: site IV [ site III [ site I [ site altitudinal gradient: site III [ site V [ site IV [ site V [ site II (Tukey HSD multiple comparisons test, II [ site I (Tukey HSD multiple comparisons test, a = 0.05, Fig. 5; Table 4). Density was overall higher at a = 0.05, Fig. 4; Table 4). site IV (240 m.a.s.l), than at any other sites, and lower at

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Polar Biol site II (486 m.a.s.l), with densities varying from 200 to 400 highest density achieved at site IV, with a maximum of 320 organisms m-2. In general, density was more evenly dis- individuals m-2 (Fig. 6). tributed at site V (120 m.a.s.l) than at other sites, while it had a bimodal distribution at site I, varying from 95 to 300 Benthic macroinvertebrate evenness (Pielou’s J) organisms m-2 (Fig. 5). This pattern is also evidenced by Pielou’s evenness index (Fig. 4). Furthermore, the order Pielou’s evenness index (J) was not significantly different Diptera had the highest density of organisms, ranging from between altitudes (repeated-measures ANOVA, p = 0.53, 100 to 1000 individuals m-2, with site IV, accounting for Mauchly’s test of sphericity, Mauchly criterion = 0.051, the highest density reached through the altitudinal gradient p \ 0.0001, Greenhouse-Geisser correction factor 0.51, (Fig. 6). Trichoptera density was the lowest along the corrected df = 4.01, p = 0.38), although it was signifi- gradient, and in general, it remained constant (50–150 cantly lower during 2008 (2008 \ 2010 [ 2009, Tukey individuals/m2) (Fig. 6). The order Ephemeroptera exhibits HSD multiple comparisons test, a = 0.05, Fig. 4, Table 4). distribution similarities with Trichoptera, but it is represented by higher number of individuals m-2, with a max- Benthic macroinvertebrate functional feeding imum of 420 individuals m-2 at site IV. Lastly, the density groups (FFG) of Plecoptera decreases with increasing altitude, with the Mean density (individuals m-2) of collector-gatherer, filterer, predator, and scraper densities were significantly influenced by altitude, while filterer and shredder densities were also significantly influenced by year (repeated-measures ANOVA, p \ 0.0001, Mauchly’s test of sphericity, Mauchly criterion = 0.45, p \ 0.0001, Greenhouse-Geis- ser correction factor 0.65, corrected df = 10.35, Table 5; Fig. 7). Shredder densities were higher at lower altitudes and were separated into two significantly different groups: site V [ site IV [ site III [ site II [ site I (Table 5; Fig. 7). Scrapers, predators, and filterers were significantly higher at site IV than at all other sites and were separated into two or three significantly different groups. Oppositely, collector-gatherers decreased at site IV, reaching their lowest densities (see Table 5 for details, Fig. 7). The most abundant collector-gatherers were Meridialaris chiloeensis (Ephemeroptera: Leptophlebiidae) and Pelurgoperla sp. Fig. 3 Total cumulative degree-days (CDD) obtained for a period of (Plecoptera: Gripopterygidae), which peaked at site V, 12 months from the headwaters to the mouth (sites II–V) of the while the most abundant filterer was Gigantodax rufescens altitudinal gradient of the Ro´balo River watershed (Diptera: Simuliidae), which had the highest densities at

Table 3 Results for two-way repeated-measures ANOVA and Tukey identify signiﬁcant differences between years (2008, 2008, and 2010) HSD (a = 0.05) multiple comparison test for physicochemical and altitude (m.a.s.l) (site I, site II, site III, site IV, and site V = 586, parameters along the altitudinal gradient of the Ro´balo River to 486, 380, 240, and 120 m.a.s.l, respectively) Parameter Factor SS FpTukey results (signiﬁcantly different)

Temperature Year 109.37 6.06 0.07 – Altitude 87.14 2.42 0.01 Site I \ site II \ site III \ site IV \ site V Dissolved oxygen Year 133.17 0.28 0.76 – Altitude 1976.44 2.07 0.11 – Conductivity Year 81.78 630.35 0.00 2010 \ 2008 \ 2009 Altitude 29.48 113.59 0.00 Sites V, IV, III [ sites II, I pH Year 0.26 2.03 0.15 – Altitude 0.15 0.59 0.67 –

Signiﬁcant values in bold (a = 0.05). Groups are underlined

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Polar Biol site IV. Rhechorema magellanicum, endemic to the Mag- three environmental variables selected (substrate diversity ellanic region, was the most abundant predator, reaching its (H0), altitude, and conductivity), showed that 83.7 % of the highest densities at site IV. The most abundant scraper was total explained variance in species density was accounted by Metamonius anceps (Ephemeroptera: Nesameletidae), the ﬁrst two principal components (explained variance reaching its highest densities at site V (Fig. 8). component 1 = 53.6 %; explained variance component 2 = 26.7 %, Table 6). The results indicate that Udamocer- Environmental relationships cia sp. (Notonemouridae: Plecoptera) and Orthocladiinae (Chironomidae: Diptera) have a signiﬁcant positive rela- The results of the PCA analysis for the species that make up tionship with altitude (Pearson’s correlation of 0.41 and 0.54, more than 90 % of the total density of organisms and the respectively, a = 0.05, two-tailed test), while Meridialaris chiloeensis (Leptophlebiidae: Ephemeroptera), Rheo- chorema magellanicum (Hydrobiosidae: Trichoptera), Ed- wardsina sp. (Blephlariceridae: Diptera), Limonia sp.

Fig. 5 Beanplot of altitudinal patterns of density (mean number of ind./m2) for benthic macroinvertebrates along the altitudinal gradient of the Ro´balo River watershed. Each ‘‘bean’’ consists of a density trace, which is mirrored to form a polygon shape (Kampstra 2008), and the individual observations are shown as small white lines, which Fig. 4 Mean richness and evenness (Pielou’s J evenness index) in this case correspond to the years 2008, 2009, and 2010. The dotted (±SE) of benthic macroinvertebrates along the altitudinal gradient of line indicates the general average, while the solid line indicates the the Ro´balo River watershed for the years 2008, 2009, and 2010 average for each group

Table 4 Two-way repeated-measures ANOVA and Tukey HSD altitude (m.a.s.l) (site I, site II, site III, site IV, and site V = 586, 486, multiple comparison test results for community metrics to identify 380, 240, and 120 m.a.s.l, respectively) signiﬁcant differences between years (2008, 2008, and 2010) and Metric Factor DF SS Fp Tukey results

Taxa richness Year 2 118.93 6.10 0.006 2009 [ 2010 [ 2008 Altitude 4 513.87 13.17 0.00 Site III [ site V [ site IV [ site II, site I Density Year 2 23,911 2.34 0.11 Altitude 4 2,132,211 10.41 <0.0001 Site IV [ site III [ site I [ site V [ site II Pielou’s evenness index Year 2 0.13 6.12 0.006 2009, 2010 [ 2008 Altitude 4 0.06 1.36 0.27 –

Signiﬁcant values in bold (a = 0.05). Groups are underlined

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Fig. 6 Beanplots of density patterns (mean number of ind./ m2) for the major aquatic insect orders (Diptera, Ephemeroptera, Plecoptera, Trichoptera) along the altitudinal gradient of the Ro´balo River watershed. The dotted line indicates the general average, while the solid line indicates the average of each group

Table 5 Two-way repeated-measures ANOVA and Tukey HSD macroinvertebrate functional feeding groups (FFG) through the multiple comparison test results for altitude (m.a.s.l) and year altitudinal gradient of the Ro´balo River (2008, 2009, and 2010) on the density (individuals/m2) of benthic FFG Factor df SS Fp Tukey results (signiﬁcantly different)

Shredder Year 2 628 0.52 0.48 – Altitude 4 18,527 5.08 0.006 Site V [ site IV [ site III [ site II [ site I Scraper Year 2 11,430 1.37 0.26 – Altitude 4 75,598 4.53 0.0019 Site IV [ site V [ site I [ site III [ site II Predator Year 2 355,774 0.89 0.41 – Altitude 4 3,142,258 3.96 0.0038 Site IV [ site III [ site I [ site V [ site II Collector-gatherer Year 2 306,425 0.89 0.41 – Altitude 4 2,165,384 3.15 0.02 Site I [ site III [ site II [ site V [ site IV Filterer Year 2 13,812 0.18 0.67 – Altitude 4 4,168,894 17.93 <0.0001 Site IV [ site V [ site III [ site II [ site I

Signiﬁcant values in bold, a = 0.05. Groups are underlined

(Tipulidae: Diptera), Hemerodromia sp. (Empididae: Dip- a = 0.05, two-tailed test). Orthocladiinae (Chironomidae: tera), Gigantodax rufescens (Simuliidae: Diptera), and Lu- Diptera) and Hemerodromia (Empididae: Diptera) are neg- choelmis sp. (Elmidae: Diptera) have a significant negative atively correlated with substrate diversity (Pearson’s corre- relationship with altitude (Pearson’s correlations [-0.40, lations -0.47 and -0.51, respectively), while G. rufescens a = 0.05, two-tailed test) (Fig. 9). Furthermore, Pelurgop- shows a positive relationship with this parameter (Pearson’s erla sp. (Gripopterygidae: Plecoptera) has a significant correlation = 0.40, Fig. 9). Finally, Max R2 analysis further positive relationship with year, conductivity, and altitude showed that most of the taxa included in the analysis are (Pearson’s correlations 0.32, 0.37, and 0.52, respectively, significantly correlated with altitude (Table 7).

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Fig. 7 Mean density (m-2) (±SE) of functional feeding groups along the altitudinal gradient of the Ro´balo River for the years 2008, 2009, and 2010

Discussion contrasted with northern hemisphere streams, where the same accumulation of yearly degree-days is reached at Benthic macroinvertebrate assemblages signiﬁcantly higher altitudes, as has been shown for along the altitudinal gradient of the Ro´balo River streams in the Rocky Mountains, where the same CDD are recorded for altitudinal gradients ranging from 0 to Water temperature is one of the major factors determining 1500 m.a.s.l (Hauer et al. 1997). This steep temperature the distribution and life histories of aquatic insects along gradient provides a perfect natural laboratory for studies gradients of latitude and elevation (Vannote et al. 1980). related to climate change in the short and long term, as Furthermore, temperature is greatly affected by climatic future studies could focus on species distributions, thermal changes along gradients of altitude or latitude. In this tolerances, and effects of climate change on phenologies of study, we found that the Ro´balo River watershed is char- aquatic insects in Magellanic Sub-Antarctic streams. acterized by a sharp altitudinal gradient, in which the Benthic macroinvertebrate distributions are highly cor- cumulative degree-days per year sharply increase by a related with elevation and the thermal characteristics along magnitude of 69 (from 365 to 2051 CDD) from its head- the altitudinal gradient of the Ro´balo River. This pattern is waters to its mouth (Figs. 2, 3), through a relatively short also observed in altitudinal gradients of the northern and altitudinal gradient (12 km, 0–600 m.a.s.l). This is notably southern hemispheres (Rocky Mountains, Andes

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Fig. 8 Mean density (m-2) (±SE) of the most abundant taxa along the altitudinal gradient of the Ro´balo River watershed

Table 6 Results of principal component analysis Axes Principal components 1234

Eigenvalues 6.42 3.66 2.39 2.01 Difference 2.75 1.27 0.39 0.67 Eigenvalues for the ﬁrst four principal components are provided

Cordillera), where similar results are found through gradients reaching 4000 m of elevation (Hauer et al. 2000, Jacobsen 2004). However, compared to the gradients mentioned, the Ro´balo River shows a similar pattern Fig. 9 Principal components analysis (PCA) of species that con- through a short and steep gradient of only 600 m. This tributed to 90 % of the density (ind.m-2) along the altitudinal in short and steep gradient provides the perfect scenario for relation to conductivity (lS), substrate diversity (H0), and altitude long-term comparisons through the representative habitats (m.a.s.l) as supplementary variables. Circles indicate macroinverte- of the Sub-Antarctic Magellanic ecoregion, as each habitat brate taxa: Orth = Orthocladiinae (Diptera:Chironomidae); edwa = Edwardsina sp. (Diptera: Blephariceridae); limn = Limonia is represented throughout the altitudinal gradient of the sp. (Diptera: Limnoiidae); heme = Hemerodromia sp (Diptera:Tip- Ro´balo River watershed (Rozzi et al. 2010). Thus, the ulidae); pelu = Pelurgoperla sp. (Plecoptera: Gripopterygidae); Ro´balo River provides an ideal setting for long-term udam = Udamocercia sp. (Plecoptera: Notonemouridae); monitoring of benthic macroinvertebrate community tipu = Tipulidae unidentiﬁed species (Diptera); rheo = Rheo- chorema magellanicum (Trichoptera: Hydrobiosidae); luch = Lu- dynamics through a sharp Sub-Antarctic altitudinal gradi- choelmis sp. (Coleoptera: Elmidae); giga = Gigantodax rufescens ent. Furthermore, because of the sharp response of benthic (Diptera: Simuliidae); meri = Meridialaris chiloeensis (Ephe- macroinvertebrate communities to altitude and tempera- meroptera: Leptophlebiidae); hexa = Hexatoma sp. (Diptera: Tipul- ture, this study emphasizes the value of macroinvertebrates idae); meta = Metamonius anceps (Ephemeroptera: Nesameletidae). Triangles indicate physicochemical characteristics: alt = Altitude as ideal indicators of thermal modiﬁcations that may be (m.a.s.l); subst = instream substrate type; cond = conductivity (lS) associated with change in land, riparian vegetation, or climate change scenarios (Hauer et al. 2000). The macroinvertebrate assemblages of the Ro´balo River ephemeropterans, and trichopterans are the predominant also resemble that of other Patagonian streams (Mis- groups. The invertebrate faunas of many stony streams in erendino and Pizzolon 2000) as well as some similar New Zealand and Australia are also dominated by these streams in New Zealand (Winterbourn 1978; Miserendino four orders of insects, with many of the same families and Pizzolon 2000) in which dipterans, plecopterans, being prominent (Miserendino and Pizzolon 2003) and

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R with New Zealand and South America having the strongest similarities at the family level. For example, 0.20 0.20 0.10 0.44 0.20 0.20 0.19 0.34 ------many of the families (Leptophlebiidae, Gripopterygidae, Notonemouridae, and Hydrobiosidae) are present at the Ro´balo River, and other Patagonian streams (Mis- erendino and Pizzolon 2000), are also present in New Zealand streams. However, several families of fresh- y) through the altitudinal

3rd variable Partial water invertebrates that are widespread or common in Patagonia and Magellanic Sub-Antarctic streams, are 2

R not found in New Zealand and include the Perlidae, Baetidae, Glossosomatidae, Limnephilidae, and Hyal- 0.49 Conductivity 0.38 Temperature 0.28 0.50 Year 0.48 Temperature - - - - lelidae (Miserendino and Pizzolon 2003). Phylogenetic relationships that show close concordance with the proposed geological sequence for the break-up of Gondwana can provide clear evidence for vicariance as the major mechanism that has driven disjunct distribu-

2nd variable Partial tions (Krosch et al. 2011). Broad ranges of invertebrate taxa with varying dispersal capabilities exhibit phylo- 2

R genies consistent with this pattern, including several groups within the Diptera (Krosch et al. 2011) and 0.42 Substrate 0.33 Year 0.35 Substrate 0.12 Temperature 0.02 0.57 Substrate 0.23 Year 0.50 Substrate 0.20 Temperature 0.20 0.57 Temperature 0.43 Substrate 0.33 0.71 Substrate 0.47 Temperature 0.34 ------Ephemeroptera. Thus, strong similarities between the Patagonian and New Zealand aquatic invertebrate faunas are evidenced by the presence of the same families in both systems (Miserendino and Pizzolon 2003). Although the Cape Horn Biosphere Reserve is one of

1st variable Partial the 24 most pristine areas remaining in the world, it is an

0.30 for each proposed model area replete with exotic invasive species, such as the [ North American beaver (Castor canadensis), which was

value introduced to the area in 1946. Today, the North Ameri- 0.0001 Temperature 0.56 Year 0.39 Altitude 0.0001 Altitude 0.0001 Altitude 2 p \ \ \ R can beaver has invaded almost 100 % of all rivers and streams in Navarino Island. Previous studies carried out

2 by Anderson and Rosemond (2007) in rivers and streams 0.30 0.030 Altitude 0.33 0.010 Altitude 0.50 0.005 Altitude 0.59 Substrate 0.51 0.003 Altitude 0.51 0.002 Temperature 0.47 Conductivity 0.45 Altitude 0.52 0.005 Altitude 0.55 0.010 Year 0.42 Altitude 0.59 0.000 Altitude 0.61 Substrate 0.60 0.63 R 0.74 of Navarino Island showed that beaver engineering in these ecosystems increased instream sedimentation and created taxonomically simpliﬁed, but more productive benthic macroinvertebrate assemblages, in which diversity, richness, and functional feeding groups were reduced Hexatoma Meridialaris Udamocercia Luchoelmis Limonia Rheochorema Metamonius Hemerodromia Pelugorperla Edwardsina Gigantodax by half, while abundance and secondary production

0.05 and taxa that exhibited an increased three- to ﬁvefold in beaver ponds. Our results \ show an increased density of benthic macroinvertebrates in site IV (240 m.a.s.l), where an abandoned beaver dam values

p dominated the system. Sedimentation disrupts benthic stream communities, and releases of suspended solids can affect benthic populations, by reducing total density or augmenting resistant species such as oligochaetes and chironomids (Ward and Stanford 1982; Miserendino and Pizzolon 2003). Consistent with this, site IV had a sig- balo River regression summary of benthic macroinvertebrates in response to ﬁve selected variables (altitude, temperature, year, substrate, and conductivit

´ niﬁcantly higher abundance of oligochaetes, chirono- 2 R mids, and also amphipods (Hyallela sp.). Furthermore, macroinvertebrate richness, diversity, and number of Max functional feeding groups were signiﬁcantly lower at this site, further complementing previous studies associated Models were selected based on overall Diptera Tipulidae Ephemeroptera Leptophlebiidae Plecoptera Notonemouridae Coleoptera Elmidae Diptera Tipulidae Diptera Tipulidae 0.51 0.049 Substrate 0.49 Altitude 0.30 Year Trichoptera Hydrobiosidae Ephemeroptera Nesameletidae Diptera Tipulidae Plecoptera Gripopterygidae Diptera Blephlariceridae Diptera Chironomidae/Orthocladiinae 0.68 0.000 Altitude 0.69 Substrate Order Family/subfamily Genus Table 7 Diptera Simuliidae gradient of the Ro with monitoring the effects of the exotic invasive North

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American beaver on benthic macroinvertebrate community Anderson, and Simoń Castillo for providing valuable comments on assemblages (Anderson and Rosemond 2007). Density of this manuscript. Special thanks are provided to the anonymous reviewers, who provided comments that have significantly improved filterers significantly decreased toward the mouth of the the final version of this work. Tamara Contador is supported by Ro´balo River, and in contrast with other Patagonian streams, FONDECYT Grant 11130451. This paper is a contribution to the collector-gatherers showed a fluctuating density pattern Universidad de Magallanes and the Research Program of the Chilean through the altitudinal gradient, rather than an uniform LTSER network at Sub-Antarctic Biocultural Conservation Program and Omora Ethnobotanical Park, Chile. increasing pattern toward the mouth of the river (Mis- erendino and Pizzolon 2000; Table 5). References The Ro´balo River as a natural laboratory and reference site for Sub-Antarctic Magellanic Anderson CB, Rosemond A (2007) Ecosystem engineering by freshwater ecosystems invasive exotic beavers reduces in-stream diversity and enhances ecosystem function in Cape Horn, Chile. Oecologia The purpose of this study was to provide the basis for 154:141–153. doi:10.1007/s00442-007-0757-4 Armesto J, Rozzi R, Smith-Ramirez C, Arroyo MT (1998) Conser- future research regarding southern South American Mag- vation targets in South American temperate forests. Science ellanic Sub-Antarctic freshwater ecosystems in the context 282:1271–1272. doi:10.2307/2897286 of global change as given by climate change, the intro- Contador TA (2011) Benthic macroinvertebrates of temperate, sub- duction of exotic species, increased urbanization, among Antarctic streams: effects of altitudinal zoning and temperature on the phenology of aquatic insects associated Ro´balo river, Navarino others. With the reference information gathered from this Island (55°S), Chile. Dissertation, University of North Texas study, we can now undertake experiments on mechanisms Contador TA, Kennedy JH, Rozzi R (2012) The conservation status of of thermal tolerance (in species currently displaying alti- South American aquatic insects in the literature. Biodivers tudinal distribution limits within the Ro´balo River and Conserv 21:2095–2107. doi:10.1007/s10531-012-0299-x Convey P, Stevens MI (2007) Antarctic biodiversity. Science other watersheds), obtain field data on phenological pat- 317:1877. doi:10.1126/science.1147261 terns of species found at multiple spatial scales (within the Crawley MJ (2007) The R book. Wiley, England altitudinal gradient of the Ro´balo watershed and, for Domıńguez E, Fernańdez HR (2009) Macroinvertebrados bentońicos example across a latitudinal gradient in southern Chile), or Sudamericanos: Sistema´tica y Biologıá, 2nd edn. Fundacioń Miguel Lillo, Tucumań model projected changes in both thermally determined Harrelson C, Rawlins CL, Potyondy JP (1994) Stream channel distributions and voltinism patterns according to climate references sites: an illustrated guide to field technique. USDA change scenarios to test these predictions by long-term Forestry Service, Fort Collins monitoring. Studies of this sort are critical. Ecosystems at Hassan R, Scholes R, Ash N (2005) Millenium ecosystem assessment. Ecosystems and human well-being: current state and trends. higher latitudes and altitudes are experiencing some of the Island Press. http://www.unep.org/maweb/documents/document. fastest rates of warming on the planet (Hassan et al. 2005), 766.aspx.pdf. Accessed 13 March 2013 and southern South America watersheds can be considered Hauer RF, Baron JS, Campbell DH, Fausch KD, Hostetler W, as ‘‘sentinel systems,’’ providing early warning of wider Leavesley GH, Leavitt PR, McKnight DM, Stanford JA (1997) Assessment of climate change and freshwater ecosystems of the scale change. By studying these systems, we are likely to Rocky Mountains, USA and Canada. Hydrol Process 11: gain considerable insight into climate change impacts not 903–924. doi:10.1002/(SICI)1099-1085(19970630) only on these quite simple ecosystems but also on the more Hauer RF, Stanford JA, Giersch JJ, Lowe WH (2000) Distribution and complex, species-rich systems found in warmer regions of abundance patterns of macroinvertebrates in a mountain stream: an analysis along multiple environmental gradients. Verh Int the globe (Woodward et al. 2010). Verein Limnol 27:1485–1488. doi:0368-0770/00/0027-01485 Hulton NRJ, Purves RS, McCulloch RD, Sugden DE, Bently MJ Acknowledgments Support to conduct this work was provided by (2002) The last glacial maximum in southern South America. the University of North Texas Beth Baird Scholarship, the Institute of Quat Sci Rev 21:233–241. doi:10.1016/S0277-3791(01)00103-2 Ecology and Biodiversity (Chile) (Grants ICM P05-002 and PFB-23), Jacobsen D (2004) Contrasting patterns in local and zonal family the Omora Ethnobotanical Park-University of Magallanes, and the richness of stream invertebrates along an Andean altitudinal Sub-Antarctic Biocultural Conservation Program (www.chile.unt. gradient. Freshw Biol 49:1293–1305. doi:10.1111/j.1365-2427. edu). We thank field support by the many students of the Tracing 2004.01274.x Darwin’s Path course series carried out in Navarino Island, especially Kampstra P (2008) Beanplot: a boxplot alternative for visual Sebastian Rosenfeld, Heather Perry, Jeffrey Mabe, Ernesto Davis, comparison of distributions. J Stat Softw 28: Code Snippet 1. Cristobal Pizarro, Rodrigo Molina, Kelli Moses, Alexandria Poole, http://www.jstatsoft.org/. Accessed 5 April 2012 Charles Braman, and Michael Simononok. Activities by Charles Krosch MN, Baker M, Mather PB, Cranston PS (2011) Systematics Braman and Michael Simononok, in support of this study, were and biogeography of the Gondwanan Orthocladiinae (Diptera: supported by an NSF International Research Experience for Students Chironomidae). Mol Phylogenet Evol 59:458–468. doi:10.1016/ Grant (OISE 0854350) awarded to the University of North Texas Sub- j.ympev.2011.03.003 Antarctic Biocultural Conservation Program, in association with the McCulloch RD, Clapperton CM, Rabassa J, Currant AP (1997) The Universidad de Magallanes, and the Ecological Society of America glacial and post-glacial environmental history of Fuego-Patag- SEEDS Program. The authors thank Lisa Naughton, Christopher onia. In: McEwan I, Borrero LA, Prieto A (eds) Patagonia:

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natural history, prehistory and ethnography. Princeton Univer- Rozzi R, Armesto JJ, Gutie´rrez J, Anderson CB, Massardo F, Likens sity Press, Princeton, pp 12–31 G, Poole A, Moses K, Hargrove G, Mansilla A, Kennedy JH, Merritt RW, Cummins K (2007) Trophic relations of macroinverte- Willson M, Jax J, Jones C, Callicott JB, Kalin MT (2012) brates. In: Hauer FR, Lamberti GA (eds) Methods in stream Integrating ecology and environmental ethics: earth stewardship ecology. Academic Press, San Diego, pp 585–610 in the southern end of the Americas. Bioscience 628:1226–1236. Merritt RW, Cummins K, Berg MB (2008) An introduction to the doi:10.1525/bio.2012.62.3.4 aquatic insects of North America. Kendall/Hunt Publishing Snyder RL, Spano D, Duce P, Cesaraccio C (2001) Temperature data Company, Dubuque for phenological models. Int J Biometeorol 45:178–183. doi:10. Miserendino ML, Pizzolon LA (2000) Macroinvertebrates of a fluvial 1007/s004840100103 system in Patagonia: altitudinal zonation and functional structure. Sweeney BW, Jackson JK, Newbold JD, Funk DH (1990) Climate Archiv Fur Hydrobiol 150:55–83. doi:0003-9136/00/0150-0055 Change and the Life Histories and Biogeography of Aquatic Miserendino ML, Pizzolon LA (2003) Distribution of macroinverte- Insects in Eastern North America. In: Firth P (ed) Global climate brate assemblages in the Azul-Quemquemtreu river basin, change and freshwater ecosystems. Springer, Berlin, pp 143–176 Patagonia, Argentina. New Zeal J Mar Fresh 37:525–539. Vannote RL, Minshall GW, Cummins KW, Sedell JR, Cushing CE doi:0028-8330/03/3703-0525 (1980) The river continuum concept. Can J Fish Aquat Sci Mittermeier RA, Mittermeier CG, Brooks T, Pilgrim JD, Konstant 37:130–137. doi:10.1139/f80-017 WR, Fonseca GA, Kormos C (2003) Wilderness and biodiversity Ward J, Stanford J (1982) Thermal responses in the evolutionary conservation. Proc Natl Acad Sci USA 100:10309–10313. ecology of aquatic insects. Annu Rev Entomol 27:97–117. doi:10.1073/pnas.1732458100 doi:10.1146/annurev.en.27.010182.000525 Pisano E (1980) Distribucioń y caracterı´sticas de la vegetacioń del Winterbourn MJ (1978) The macroinvertebrate fauna of a New archipie´lago del Cabo de Hornos. An Inst Patagonia Ser Cien Zealand forest stream. N Z J Zool 5:157–169. doi:10.1080/ Nat 11:192–224 03014223.1978.10423746 Porter C, Santana A (2003) Rapid 20th century retreat of Ventisquero Winterbourn MJ, Cadbury S, Ilg C, Milner AM (2008) Mayfly Marinelli in the Cordillera Darwin icefield. An Inst Patagonia production in a New Zealand glacial stream and the potential Ser Cien Nat 31:17–26 effect of climate change. Hydrobiologia 603:211–219. doi:10. R.app GUI 1.65 (6833 Snow Leopard build), S. Urbanek & H.-J. 1007/s10750-9273-0 Bibiko, Ó R Foundation for Statistical Computing, 2014 Woodward G, Perkins DM, Brown LE (2010) Climate change and Rozzi R, Anderson CB, Pizarro JC, Massardo F, Medina Y, Mansilla freshwater ecosystems: impacts across multiple levels of organiza- A, Kennedy JH, Ojeda J, Contador TA, Morales V, Moses K, tion. Phil T R Soc B 365:2093–2106. doi:10.1098/rstb.2010.0055 Poole A, Armesto JJ, Kalin MT (2010) Field environmental Zar JH (2010) Biostatistical Analysis. Pearson Prentice-Hall, Upper philosophy and biocultural conservation at the Omora Ethnob- Saddle River otanical Park: methodological approaches to broaden the ways of integrating the social component (‘‘S’’) in Long-Term Socio- Ecological Research (LTSER) Sites. Rev Chil Hist Nat 83:27–68. doi:10.4067/S0716-078X2010000100004

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