Impact of Chaitén Volcano Ashfall on Native and Exotic Fish Recovery

Science of the Total Environment 752 (2021) 141864

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Science of the Total Environment

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Impact of Chaitén Volcano ashfall on native and exotic ﬁsh recovery, recolonization, and abundance

Cecilia Yanina Di Prinzio a,b,⁎, Brooke Penaluna c, Marta Gladys Grech a,b, Luz María Manzo a, María Laura Miserendino a,b, Ricardo Casaux a a Centro de Investigación Esquel de Montaña y Estepa Patagónica (CONICET-UNPSJB), Roca 780, Esquel, Chubut, Argentina b Facultad de Ciencias Naturales y Ciencias de la Salud, Universidad Nacional de la Patagonia San Juan Bosco, Esquel, Chubut, Argentina c U.S. Department of Agriculture, Forest Service, Paciﬁc Northwest Research Station, 3200 SW Jefferson Way, Corvallis, OR 97331, United States of America

HIGHLIGHTS GRAPHICAL ABSTRACT

• Fish recolonization is ongoing taking 4 days to 9 months after the eruption. • Fish abundances changed over the 21- month study period post-volcanic eruption. • Introduced Rainbow Trout was the pioneer recolonizer. • Catﬁsh were the slowest to recolonize albeit suffered lower impact from the eruption.

article info abstract

Article history: The effects of volcanic disturbance on aquatic communities and their recovery are poorly studied. To fill this gap, Received 15 May 2020 we explored the effects on fish communities in rivers in Argentina of the 2008 eruption of Chaitén Volcano in Received in revised form 27 July 2020 southern Chile (42.8° lat. S). The eruption produced volcanic plumes of ash that persisted in the atmosphere Accepted 19 August 2020 for several months. Borne on westerly winds, deposits of tephra crossed the Andes Mountains, reaching the At- Available online 21 August 2020 lantic coast (Argentina). We compared the pre- and post-eruption abundances of a native catfish Hatcheria Editor: Sergi Sabater macraei, and two introduced trout from rivers covered by the volcanic plumes (Argentina) using Before-After- Control-Impact analysis to explore fish recovery. Total suspended solids from volcanic ashfall, macroinvertebrate Keywords: abundance and richness, and species ecological attributes influenced the spatial arrangement of fish in rivers. Volcanic disturbance Twenty-one months after the eruption, Rainbow Trout, Oncorhynchus mykiss, had not returned to pre-eruption Fish repopulation abundances in the sampled rivers, and only four rivers had regained pre-eruption species composition, suggest- Disturbance ing that disturbance is still ongoing. The abundance of introduced fishes was strongly, negatively correlated with Ash deposition TSS, suggesting that ashfall affected these fish probably by clogging and abrasion of the gills. Fish recolonized pre- Tephra fall viously occupied habitats 4 days to 9 months after the disturbance. Hatcheria macraei was the slowest to recolonize, whereas O. mykiss were the pioneer fish in 4 rivers following the eruption and recolonized all 5 rivers where they were present prior to the eruption. In one river, the catfish and the Brown Trout, Salmo trutta, were still ab- sent 21 months post-eruption, potentially owing to the lack of riparian cover that would have deflected the entry of ash. Rainbow Trout suffered significant declines in abundance, whereas Brown Trout and catfish generally did not, owing to their ecological attributes. Total fish abundance was negatively correlated with ash thickness, but positively related to prey availability. © 2020 Elsevier B.V. All rights reserved.

⁎ Corresponding author at: Centro de Investigación Esquel de Montaña y Estepa Patagónica (CONICET-UNPSJB), Roca 780, Esquel, Chubut, Argentina. E-mail address: [email protected] (C.Y. Di Prinzio).

1. Introduction assessed (Inbar et al., 1995). The 2011 eruption of Puyehue-Cordón Caulle in Chile was another opportunity to investigate the role of volca- On 2 May 2008, the Chaitén Volcano in southern Chile released an nic eruptions in shaping fish responses. Although declines in introduced explosive plume of ash and steam into the atmosphere, coating a salmonid abundances post-eruption were linked to changes in habitat broad area across southern South America with ash without warning. and macroinvertebrate assemblages, with decreasing effect with in- Strong eruptive activity continued over the next week, and the ash col- creasing distance from the eruption site, the eruption impact on native umn reached 30 km high at its peak, but gradually diminished over the fishes was not studied (Lallement et al., 2016). A better understanding next several months (Watt et al., 2009). The average ash thickness de- of the effects of volcanic ashfall on fishes of South America is needed, es- posited across affected regions of Argentina was 5–10 cm (Watt et al., pecially for native fishes. 2009). More generally, explosive volcanic eruptions are recognized as The native ichthyofauna of the Patagonia is characterized by a low unpredictable natural disturbances that may result in profound biolog- species richness (Ringuelet, 1975; Baigún and Ferriz, 2003; Soto et al., ical and environmental responses depending on the magnitude, compo- 2006). Since the early 1900s, the Patagonia region of Argentina has un- sition of the ejected material, particle size, distance from the explosion, dergone continuous stocking of introduced salmonids, mostly for recre- and duration of the event (Annen and Wagner, 2003; Martin et al., ational purposes (Pascual et al., 2007) resulting in the dominance and 2009; Mather, 2015). Volcanic processes involved in eruptions are widespread distribution of trout, including Rainbow Trout Oncorhyn- highly variable in their potential to disturb ecosystems, and often lesser chus mykiss, Brown Trout Salmo trutta and Brook Trout Salvelinus impacts can be found when fine volcanic ash and lighter particles are fontinalis (Pascual et al., 2002; Arismendi et al., 2019). Consequently, dispersed across broader areas (Arendt et al., 1999; Annen and native fishes currently face continued pressure by invasive salmonids, Wagner, 2003; Martin et al., 2009; Ruggieri et al., 2012). as reflected by the declining numbers in native biota (Macchi et al., Volcanic eruptions lead to a wide range of new environmental condi- 1999; Pascual et al., 2002; Lattuca et al., 2008; among others). Bello tions, as well as a broad spectrum of biotic responses at different scales and Úbeda (1998) estimated that 60% of the native Patagonian fish spe- (Turner et al., 1997). Many responses can benefit the spread of recover- cies have been designated as “threatened”, with some endemic fishes ing biota, but an existing population or community may be extirpated by also regarded as “rare” (López et al., 2003). severe disturbance (del Moral, 1981). For example, the May 1980 erup- Here, we provide baseline information on the responses of native tion of Mount St. Helens in southwestern Washington state, USA, caused and introduced fishes to ashfall from the Chaitén Volcano eruption by a dramatic decrease in terrestrial insect populations (Edwards and comparing pre-eruption and post-eruption data across rivers with a Schwartz, 1981)andmodified the dominant taxa in water bodies closest gradient of ashfall influence. We hypothesized that greater thickness to the blast zone (Anderson and Wisseman, 1987; Edwards and Sugg, of volcanic ash in rivers would have stronger impacts on fish communi- 2005). Chironomid assemblages changed in response to tephra deposi- ties. For example, the increase in total suspended solids might clog fish tion in Lake Galletué, Chile likely from Llaima Volcano in 1957, with gills and suffocate them, or cause abrasion. Both native and exotic fish the replacement of Ablabesmyia by Parakiefferiella (Urrutia et al., 2007). predate on aquatic macroinvertebrates (Di Prinzio and Casaux, 2012; Changes in the percentage of collector-gatherer invertebrates in Arismendi et al., 2012), and, consequently, we anticipated that changes Tongariro River, New Zealand, following a series of eruptions of Mount in available prey would reduce fish feeding and lower fish condition, as Ruapehu in 1995–1996 led to a deterioration in water quality and reported in Miserendino et al. (2012). We also anticipated differences in changes to food webs (Collier et al., 2002). The 2011 eruption of the fish responses following the eruption, owing to species´ ecological attri- Puyehue-Cordón Caulle complex, Chile led to the decline of Ephemerop- butes. For example, the native catfish Hatcheria macraei occupies ben- tera, Plecoptera and Trichoptera (EPT) densities, mainly in rivers closer thic habitats, S. trutta use the full water column, but tend to use pools, to the eruption site (Lallement et al., 2014). In response to the 2008 whereas O. mykiss uses the entire water column and many habitat Chaitén explosion, there was a steep decrease in macroinvertebrate den- types (McIntosh, 2000; López et al., 2003; Casalinuovo et al., 2017). Re- sity and richness in rivers of Argentina, with small systems being more sults of this work will help inform management decisions on whether severely affected than larger ones (Miserendino et al., 2012). restocking actions are necessary to accelerate the recovery of fishes fol- Fish responses to volcanic eruptions vary depending on the severity lowing disturbance. of volcanic processes they experience and proximity of the volcano, with the most devastating direct effects closer to the volcano, but indi- rectly and, sometimes, at great distances via ashfall. Studies conducted 2. Material and methods after the 1980 Mount St. Helens eruption revealed that fish mortality was caused by heat and the increase in suspended sediments and thus 2.1. Chaitén volcano eruption water turbidity from ash and mechanical gill damage (abrasion) caused by ash particles (Whitman et al., 1982; Leither, 1989; Bisson et al., The largest explosive eruption globally since the 1991 Hudson Vol- 2005). Similarly, in New Zealand historic ash-laden floods moving cano eruption (Chile), the Chaitén Volcano (42°50′21.94″S-72°39′5.38″ down rivers affected current diadromous and freshwater fish distribu- W; 962 m.a.s.l.) eruption began on 2 May of 2008 (Naranjo and Stern, tions (McDowall, 1996), and populations that recolonized rivers in 2004). Rhyolitic eruptions such as Chaitén are relatively rare (Ruggieri areas covered with volcanic ash consisted almost entirely of diadro- et al., 2012), and it was the first of its type since Novarupta, Alaska, mous fishes. Rivers in New Zealand with lighter ashfall provided refugia USA, in 1912 (Watt et al., 2009). Ash columns from the volcano jetted for fishes to recolonize nearby habitats that were more affected by ash rapidly into the stratosphere to an altitude of >21 km, followed by lava post-eruption (McDowall, 1996). After the 2008 Kasatochi eruption in dome effusion and continuous low-altitude ash plumes (Lara, 2009). the Aleutian Islands, Alaska, USA, salmon populations increased as a re- After several hours of eruption, ash was falling across awidespread area sult of the changes in the food web dynamics owing to phytoplankton of Chile and Argentina. Predominant westerly winds (Sernageomin, blooms (Olgun et al., 2013). The 1912 eruption of Mount Katmai, Alaska 2008) dispersed ash emissions to the east over Argentina, reaching all killed four thousand salmon through suffocation from excessive sedi- the way to the Atlantic Ocean, 1400 km from the eruption site (Durant mentation in streams from tephra fall, but also by eliminating their mac- et al., 2012). In the northwest of Patagonia, up to 30 cm of ash deposition roinvertebrate food base (Eicher and Rounsefell, 1957). was recorded (CDP pers. obs.). Thedimensions and depth of the falling Though some studies have examined the effects of volcanic erup- ash ranged from 50 km2 (gravel tephra, > 5 cm thick) to 480 km2 (fine tions on fish and fish habitats, there is still a lack of understanding tephra, > 10 cm thick) (Watt et al., 2009; Crisafulli et al., 2015). During about fish responses, especially in South America. In 1991, the Hudson the first week of the volcanic activity, nearly 1.6 × 1011 kg of ash (160 Volcano erupted in southern Patagonia, but fish responses were not Mtons) were deposited over 200,000 km2 (Watt et al., 2009)in C.Y. Di Prinzio et al. / Science of the Total Environment 752 (2021) 141864 3

Argentina, and after ten days of ashfall, Stewart et al. (2009) estimated in May, June and October of 2008; February, June and October of 2009; that the total volume of erupted matter was >2 km3. and March of 2010. The Chaitén tephra was made up of pumice and obsidian fragments We followed the same sampling methods throughout the study, in- (Lara et al., 2013), similar in the number and abundance of particle sizes cluding surveys of physicochemical parameters, fish, and macroinverte- from Mount St. Helens (Durant et al., 2012). There were five particle brates, using the sampling protocol from our pre-eruption research sizes from the fallout between 80 and 250 km from the epicenter, de- (Miserendino et al., 2011; Di Prinzio et al., 2009, 2013, 2015; Di Prinzio creasing to three fine sizes between 250 and 500 km away. and Casaux, 2012). For each sampling event, we measured water conductivity (μS/cm), water temperature (°C), and dissolved oxygen 2.2. Site selection – environmental characterization (mg/L) with a sensION 156 multiparameter probe. In order to obtain the total suspended solids (TSS) values, we collected water below the To evaluate the effects of volcanic ashonaquaticecosystems,wese- surface, kept it at 4 °C, and transported it to the laboratory. We filtered lected our study rivers based on the availability of data from previous water samples were filtered and calculated the differences between the field surveys (2005–2006) prior to the eruption. We selected five rivers: final and initial weights of dried filters. Physicochemical data were Glyn (Glyn), Manguera (Mang) Nant y Fall (NyF), Chiquito (Chiq) and later compared to the available pre-eruption information. Esquel (Eqs) that lie between 42 and 43°S, in the western Patagonia, To assess the in-river habitat available to the biota, we calculated the Argentina, within the area affected by ashfall deposition (Fig. 1). We proc- habitat condition index (HCI) using the assessment procedure for high essedtheashplumedispersalfromtheeruptionoftheChaiténvolcano gradient rivers (Barbour et al., 1999). This method ranks 10 river channel mapped from MODIS (Moderate Resolution Imaging Spectroradiometrer; features (e.g., epifaunal substrate availability, frequency of riffles, etc.) http://modis.gsfc.nasa.gov) satellite images (from 3 May to 8 May). We from 0 to 200. A score of 200 points indicates the river is natural and pris- obtained the deposited ash thickness (mm) from an isopach map of the tine and in its best possible condition. This index provides a numerical Chaitén distal ash deposit in Watt et al. (2009). We georeferenced the value related to the river's physical habitat to support biota and is a mea- data to the Universal Transverse Mercator coordinate system to use as a sure of the spatial heterogeneity of the river (Castela et al., 2008). cartographic base and generated a shape layer that was rasterized by the open source software QGIS 3.4. No changes in land use occurred 2.3. Biological sampling before and after eruption along our study rivers between 2005 and 2010, so that the only impact observed was the ashfall from the 2008 eruption. Our previous, pre- We followed the same sampling protocol for fish, macroinvertebrates, eruption studies involved seasonal sampling during winter, spring, and and environmental characteristics over the duration of the study summer 2005 and autumn 2006, and we revisited them post-eruption (Table 1). We collected fish along 100 m reaches using a backpack

Fig. 1. Map of five rivers in the Chubut province, Argentina and deposited ash thickness (mm), modified from Watt et al. (2009; right). Streams were sampled in 2005–2006 and in 2008 immediately after the eruption of the Chaitén Volcano. 4 C.Y. Di Prinzio et al. / Science of the Total Environment 752 (2021) 141864 electrofisher and dipnets (output 300 W set at 300 V) and with passes of (x + 1) transformed and standardized. Statistical analyses were carried equal effort by the same operator in a zigzag pattern. We identified all out using CANOCO package version 4.0 (ter Braak and Smilauer, 1998). captured fish to species following López et al. (2003). Fishes were We also performed single non-parametric correlation tests (Spearman counted, measured (total length, cm), weighed (W, accuracy 0.01 g), rank) to explore the relationships among fish abundance with physico- and returned to the river. We calculated fish condition factor using chemical parameters, macroinvertebrate density, and macroinvertebrate length–weight relationships (105 xWL−3;W=weighting,L=total richness using the statistical software STATISTICA version 6.0 (Ludwing length in cm). and Reynolds, 1988). With a Surber sampler (0.09 m2;205μm pore size), we collected 6 To investigate the variation in the species data set, and the relation- benthic macroinvertebrate samples (replicates) were collected from ship between species composition, rivers, and physicochemical param- run/riffles. Samples were fixedinsituwith4%formaldehydeandsorted eters, we used multivariate ordination. Biological data were log (x +1) in the laboratory under at least 5 X magnification. We identified macro- transformed prior to the analysis, where x is the abundance of fish spe- invertebrate species to the lowest possible taxonomic level using cies. We first conducted an exploratory Detrended Correspondence regional identification keys (Domínguez and Fernández, 2009)and Analysis (DCA) to elucidate the best type of response-model (unimodal counted them. To make databases comparable, we carefully revised versus linear). DCA revealed that the gradient length was <3 standard and modified species lists and matrices when necessary in order to ad- deviations, evidence that the dataset had short gradients and the linear just the level of identification of different groups. model is appropriate. Thus, we used a Redundancy Analysis (RDA) to investigate the associations of physicochemical parameters in rivers with 2.4. Data analysis fish species abundance. The RDA analysis was performed on the correlation matrix to avoid variables from becoming dominant owing to their We used Before-After-Control-Impact (BACI) analysis to compare large measurement units. We used forward selection of physicochemi- physicochemical parameters, fish abundance, fish condition factor, cal parameters to identify a subset of variables that significantly and in- macroinvertebrate density, and macroinvertebrate richness for rivers dependently explain the variation in the dataset. pre- and post-eruption. BACI is a powerful tool to evaluate changes to habitats and biota, using a t-test approach (Stewart-Oaten et al., 3. Results 1986). However, because the study area was covered by the volcanic ash (over 200,000 km2, Watt et al., 2009), unfortunately, we were un- 3.1. Environmental variables able to have control sites that were unaffected by ashfall, thus we refer to our analyses as BAI hereafter. We assume that the observed 3.1.1. BAI changes between the pre- and post-eruption sampling periods resulted Ashfall deposition in river and riparian zones was documented by from the volcanic ash, but without control sites we cannot eliminate the photos of sampling sites showing the foremost visible effect (Fig. 1). possibility that changes are from temporal effects. Statistical analyses The distance from the eruption site was 109 km to the Nant y Fall were conducted using STATISTICA package version 6.0 (Ludwing and River, 109.9 km to the Chiquito River, 111.4 km to the Esquel River, Reynolds, 1988). 111.9 km to the Manguera River and 112.5 km to the Glyn River. Of all We conducted a Principal Component Analysis (PCA) in order to iden- the habitat variables recorded, only TSS varied significantly after the tify which physicochemical parameters explain the patterns observed in eruption (p <0.05)(Table 1, Fig. 2). The largest increase in TSS values macroinvertebrate density, macroinvertebrate richness, and river charac- in the water column was observed in autumn of 2008; over the subse- teristics by their scores on PCA axes. The environmental data were log quent months values remained high, with some slight variation (Fig. 2).

Table 1 Summary of the Before (2005–2006) and After (2008–2010) Impact (BAI) analysis with t-test analysis of the physicochemical parameters and biological variables, following the eruption of the Chaitén Volcano from rivers of the Chubut province, Argentina. Sample size (n) is in brackets. * indicates p-value signiﬁcance.

Physicochemical parameters Mean Before Mean After T df p

Total suspended solids (mg.L−1) 3.62 (20) 15.78 (45) −9.86 4 0.005* Water temperature (°C) 7.77 (20) 8.85 (45) −1.94 4 0.12 Water Conductivity (μS/cm) 77.20 (20) 62.63 (45) 2.33 4 0.07 Dissolved oxygen (mg/L) 11.57 (20) 10.56 (45) 0.94 4 0.39 HIC 143.8 141.6 0.97 4 0.38 Biological variables Fish Abundance Species Total (O. mykiss-S. trutta-H. macraei) 23.19 (813) 5.45 (417) 3.44 4 0.02* Exotic (O. mykiss-S. trutta) 32.92 (789) 8.41 (411) 5.36 4 0.005* O. mykiss 37.85 (673) 10.99 (385) 7.24 4 0.001* S. trutta 14.25 (116) 1.85 (26) 1.04 1 0.48 Native H. macraei 1.62 (24) 0.18 (6) 3.06 3 0.054 Fish Condition Factor Species Total (O. mykiss-S. trutta-H. macraei) 0.99 (813) 1 (417) 0.34 4 0.74 O. mykiss 1.00 (673) 1.12 (385) 2.49 4 0.06 Exotic S. trutta 0.51 (116) 1.17 (26) 1.17 1 0.44 Native H. macraei 0.51 (24) 0.67 (6) 0.87 3 0.44 Fish Total Length (cm) Species Exotic O. mykiss 10.1 (673) 10.4 (385) −0.37 4 0.72 S. trutta 6.8 (116) 6.3 (26) 0.19 1 0.87 Native H. macraei 7.5 (24) 6.1 (6) 0.77 3 0.49 Macroinvertebrates Density (ind.m2) 5796.4 2881.5 2.84 3 0.06 Species Richness 22.2 14.3 6.87 3 0.006* C.Y. Di Prinzio et al. / Science of the Total Environment 752 (2021) 141864 5

Fig. 2. Total suspended solid (TSS) from before (2005–2006) and after (2008–2010) the eruption of the Chaitén Volcano from ﬁve rivers in the Chubut province, Argentina. Rivers include Glyn (Glyn), Manguera (Mang), Nant y Fall (NyF), Chiquito (Chiq), and Esquel (Eqs).

3.1.2. Ashfall effect on environmental variables (Nant y Fall, Chiquito, Esquel, Manguera). O. mykiss (atNantyFall The PCA-biplot of sites and exploratory variables based on the and Esquel) and S. trutta (at Glyn) were found 4 days after the erup- first two axes explained 74.2% of the total variance (Fig. 3; Table 2). tion. In Manguera and Chiquito, O. mykiss appeared after 49 days, The first ordination axis was mainly determined by macroinverte- whereas in Glyn it took 5 months. S. trutta never reappeared in brate density and water conductivity, followed by macroinverte- Esquel. The native H. macraei first appeared 49 days after the erup- brate richness and distance from the volcano (Table 2). TSS and ash tion in Manguera, and after 9 months in Glyn and Nant y Fall; it did thickness defined the second axis. Axis 2 clearly distinguishes not reappear in Esquel (Fig. 4). After the eruption, the abundance among rivers by time period, with rivers sampled pre-eruption hav- of all fish species greatly decreased in all rivers, and fish were unable ing negative values of TSS and ash thickness and rivers sampled post- to recover to pre-eruption abundances (Fig. 5). Although we caught eruption having positive values. one native Galaxias maculatus in Nant y Fall following the volcanic ashfall, we did not include it in the analysis because the species 3.2. Fish assemblage was not present in our pre-eruption catches.

Mean length values of fishes were larger between pre- and post- 3.2.1. BAI and multivariate analysis eruption (Table 1). Oncorhynchus mykiss were eventually captured in The BAI design of our study revealed significant differences in total all rivers where they had been present pre-eruption, and they were fish abundance pre- and post-eruption (p < 0.05), with lower abun- the first fish detected in four out of the five rivers post-eruption dance post-eruption in all 5 rivers (Fig. 5; Table 1). The decreasing 6 C.Y. Di Prinzio et al. / Science of the Total Environment 752 (2021) 141864

Fig. 3. Principal Component Analysis biplot shows the variability of various physicochemical parameters from before (2005–2006) and after (2008–2010) the eruption of the Chaitén Volcano from ﬁve sites in rivers of the Chubut province, Argentina.

pattern did not differ between native and introduced fish, but it was sta- density and species richness (which were positively correlated with tistically significant for the introduced trout, and particularly for RDA1) were other significant variables explaining fish distribution. O. mykiss (Fig. 5; Table 1). Fish condition factor did not change signifi- Pre-eruption rivers where the three fish species were abundant were po- cantly following the eruption (Table 1). The total abundance of all fish sitioned on the right side of the plot, whereas post-eruption rivers char- species was positively correlated with ash thickness (Table 3). acterized by low density of fishes were grouped all together towards the O. mykiss abundance was positively correlated to water conductivity, left at the negative end of RDA1. First axis showed strong negative corre- whereas S. trutta abundance was negatively correlated to conductivity lation of the 2 introduced trout with TSS, and a positive relationship with and positively correlated to distance from the volcano and to macroin- macroinvertebrate density and richness. However, we observed a weak vertebrate species richness (Table 3). No correlations among the native correlation of the native fish abundance with TSS and macroinvertebrate fish species and environmental and biological variables were detected. density and richness. The BAI analysis showed a significant decrease in macroinvertebrate species richness (p < 0.05), but not in the macroinvertebrate density 4. Discussion (p = 0.06) (Table 1). The RDA-triplot showed that 99.2% of the overall variability was ex- The May 2008 Chaitén Volcano eruption in southern Chile blanketed plained by the first two axes (Fig. 6; Table 4). The first axis explained rivers in Argentina with heavy ash deposition, resulting in varying levels 50.6% of the variance and was defined by a gradient in TSS, which in- of resilience of fish depending on each species´ ecological attributes and creased towards the negative end of RDA1. Moreover, macroinvertebrate on macroinvertebrate abundance and richness. We found changes in abundances of fish following the explosion, and different recolonization patterns that depended on species and river condition. Similar to obser- vations by Miserendino et al. (2012), massive ash fallout led to in- Table 2 creased levels of TSS in the water, which, in turn, affected fish Summary of Principal Component Analysis performed with environmental variables re- recolonization and abundances across rivers. This conforms to previous corded before (2005–2006) and after (2008–2010) the ashfall of Chaitén volcano, at five studies that have shown that increased ash deposition can lead to insta- rivers of Chubut Province (Argentina). bility in aquatic systems owing to increased sediment loads, elevated PCA axes summary Axis 1 Axis 2 Total variance turbidity levels, and habitat modification that affect fishes (Jowett and Eigenvalues 3.44 2.49 1.00 Duncan, 1990; Fausch and Bramblett, 1991; Dale et al., 2005). The % variation 43.03 31.17 Mount St. Helens eruption in 1980 affected Clearwater Creek, which Cum. % variation 43.03 74.21 was in the blowdown and tephrafall zone (Bisson et al., 2005). Trout Eigenvectors and sculpins (Cottus spp.) in Clearwater Creek probably took refuge in Water temperature 0.28 0.43 nearby lakes, tributaries, or springs recovering within three years of − Total suspended solids 0.23 0.53 the eruption (Crisafulli and Hawkins, 1998; Bisson et al., 2005). Conductance 0.45 0.09 fi Dissolved oxygen −0.15 −0.43 Full recolonization of shes into previously occupied habitats is on- Ash thickness −0.27 0.49 going, beginning anywhere from a few days after eruption to years Distance from volcano −0.36 −0.24 later, although only partial recolonization had occurred in the Esquel Macroinvertebrates density 0.51 −0.004 River by the end of the study. O. mykiss was the pioneer fish recolonizing Macroinvertebrates species richness 0.39 −0.15 all rivers following the eruption, probably from a source population that C.Y. Di Prinzio et al. / Science of the Total Environment 752 (2021) 141864 7

Fig. 4. Schematic diagram illustrating ﬁsh recolonization following the eruption of the Chaitén Volcano from ﬁve rivers in the Chubut province, Argentina. Fish presence from 2005 to 2006 (left) sets a baseline to understand recolonization following the eruption (right). Orange squares represent Oncorhynchus mykiss,bluesquares:Hatcheria macraei, and red squares: Salmo trutta. Rivers include Glyn (Glyn), Manguera (Mang), Nant y Fall (NyF), Chiquito (Chiq), and Esquel (Eqs).

survived in the protection of local refugia, such as a nearby tributary them an advantage for survival owing to hiding in cover. H. macraei is where ashfall deposition was potentially thinner. Recolonization was also small in body size, and because size is inversely related to survivor- faster for introduced trout than for the native catfish, probably owing ship, small animals may be able to find protection in refuges more easily to the native fish species being a poorer disperser (benthic catfish do compared to larger animals, as documented following the Mount St. not commonly migrate). Similar patterns were observed in the rivers Helens eruption (Crisafulli et al., 2015). Following the eruption at following ashfall from the Puyehue-Cordón Caulle eruption, where Puyehue-Cordón Caulle, fish numbers returned to pre-eruption values O. mykiss recolonized rivers faster than other fishes (Lallement et al., after 30 months (exceeding our study period by 9 months), arriving at 2016). In one river (Esquel), the native H. macraei and the introduced equilibrium as conditions improved (Lallement et al., 2016). Another S. trutta disappeared following the eruption, potentially owing to the potential reason for the lack of full recovery in fish abundances in the lack of riparian cover to buffer the entry of ash, suggesting that full re- current study is that spawning may not have been successful for all covery of fishes in this river may take more time. Around the Pacific fishes because ash deposition continued for, at least, 10 months after Rim, where the frequency of volcanic activity is high, the recolonization the Chaitén eruption, through February 2009. If a fish did manage to of rivers by fish depends on volcanic disturbance intensity. For example, spawn, the ash deposition could have reduced the development and in New Zealand rivers where ash deposition is common, the fish fauna survival of eggs and larvae by blocking the interstitial spaces in the consists of diadromous fishes, where as in rivers with less ashfall have gravel-redd structure, which can hamper the exchange of dissolved ox- a mix of diadromous and non-diadromous fishes (McDowall, 1996). ygen and carbon dioxide between the water and respiring eggs or larvae Similar findings were noted by Lallement et al. (2016) in response to (Harrod and Theurer, 2002). the eruption of the Puyehue-Cordón Caulle in Chile. Following the eruption, we document a decrease in fish abundances Twenty-one months after the eruption of the Chaitén volcano, intro- across species, especially severe for introduced trout including duced trout still had not returned to pre-eruption abundances, but only O. mykiss. Young-of-year fish declined in high-impact streams following Eqs did not show the same fish composition as before. Although the Puyehue-Cordón Caulle eruption, but not in low-impact streams O. mykiss displayed a marked decrease in abundance following the ex- (Lallement et al., 2016). Here, the decreases in fish abundances were plosion, S. trutta and H. macraei did not decrease as sharply. The native negatively correlated with TSS, probably owing to the direct effect of H. macraei occupy benthic habitats (López et al., 2003)andS. trutta ash deposition in the water that probably led to clogging and abrasion can use the full water column, but prefer pools (Casalinuovo et al., of the gills (Crisafulli et al., 2015) and may have depleted oxygen levels 2017), potentially allowing both species to be more tolerant of lower in the water, although this factor was not significant. We suggest that it oxygen conditions that may have resulted from ashfall, although mea- is possible that oxygen levels were depleted patchily across the river sured dissolved oxygen levels did not decrease significantly after the reaches, and that our sampling may not have captured that variability, eruption. Moreover, the native H. macraei is a rheophilic and negative because we did not find statistically significant decreases in dissolved phototactic catfish, so its behavior during daylight is mostly resting or oxygen. Other studies show direct effects on fish occur when elevated hiding in interstitial spaces (Barriga et al., 2012), which may give TSS from ashfall leads to clogging of gills, less channel substrate 8 C.Y. Di Prinzio et al. / Science of the Total Environment 752 (2021) 141864

Fig. 5. Percent change in fish abundance from before (2005–2006) to after (2008–2010) the eruption of the Chaitén Volcano from five rivers of the Chubut province, Argentina. Dotted lines show the percent abundance from before the eruption. Rivers include Glyn (Glyn), Manguera (Mang), Nant y Fall (NyF), Chiquito (Chiq), and Esquel (Eqs). interstitial spaces for refuge, lower available oxygen, and abrasion of Although fish can be affected by both direct and indirect pathways gills and scales (Bo et al., 2007; Harrison et al., 2007; Klowden, 2007; following disturbance events, we propose that changes in trout abun- McKenzie et al., 2019). dances may have also been related to prey availability, even though

Table 3 Values of the Spearman's correlation coefficient of the three fish species and the biological and environmental explanatories variables recorded into the post-erupted period (2008–2010) of the ashfall of Chaitén volcano, at five stream of Chubut Province (Argentina). * indicated p values significance.

Total abundance

All fish species Native fish specie Exotic fish specie O. mykiss S. trutta (n = 417) (n =6) (n = 411) (n = 385) (n = 26)

r p r p r p r p r p

Water temperature (°C) 0.09 0.58 0.22 0.25 0.10 0.56 0.10 0.55 0.19 0.49 Total suspended solids (mg.L−1) −0.23 0.17 −0.18 0.35 −0.22 0.19 −0.24 0.15 −0.18 0.51 Water conductivity (μS/cm) 0.28 0.10 0.01 0.93 0.29 0.08 0.33 0.04* −0.74 0.002* Dissolved oxygen (mg.L) 0.20 0.24 −0.32 0.09 0.20 0.24 0.25 0.14 −0.47 0.08 Ash thickness −0.39 0.01* −0.11 0.54 −0.39 0.01* −0.25 0.14 −0.82 0.0002* Distance from volcano (Km) −0.13 0.42 0.18 0.35 −0.15 0.36 −0.28 0.10 0.82 0.0002* Benthos density (ind.m2) −0.22 0.28 −0.1 0.69 −0.21 0.31 −0.16 0.42 0.46 0.13 Benthos species richness −0.13 0.51 0.10 0.69 −0.13 0.53 −0.1 0.62 0.67 0.01* C.Y. Di Prinzio et al. / Science of the Total Environment 752 (2021) 141864 9

Fig. 6. Redundancy Analysis (RDA) triplot for native and introduced ﬁshes across sites for physiochemical parameters from before (2005–2006) and after (2008–2010) the eruption of the Chaitén Volcano from rivers of the Chubut province, Argentina. Sites are located on ﬁve rivers, including Glyn, Manguera, Nant y Fall, Chiquito, and Esquel rivers.

no major declines in condition factor of fish. We showed that fish abun- (Miserendino et al., 2012) leading to cascading effects on fish. Addition- dances were positively correlated to both macroinvertebrate abundance ally, depending on the geomorphology and hydrology of rivers that and richness, which builds on findings by Miserendino et al. (2012) that have their headwaters high in the Andes Mountains, periods of rain observed a decrease of invertebrate density and richness after ashfall and snow melt could remobilize ashfall deposits, which would extend from the Chaitén Volcano, especially in small rivers. Macroinvertebrates or lead to lag effects of the disturbance event through time. have an important role in rivers as an intermediate trophic link between primary and tertiary consumers (McIntosh and Townsend, 1996; 5. Conclusion McIntosh, 2000). Indirect effects from elevated levels of TSS on fish occur when functional processes in food webs are altered, including In rivers of South America, volcanic disturbances are an impor- modifying consumers (fishes) and their trophic links (Wood and tant factor influencing the structure and renewal of aquatic ecosys- Armitage, 1997; McIntosh and Townsend, 1996; McIntosh, 2000). For tems, which is important for their long-term productivity. Studies example, an increase in phytoplankton biomass results in nutrient load- investigating the role of volcanic eruptions in shaping fish assem- ing and the attenuation of light (Modenutti et al., 2013), similar to what blages in southern South America are scarce, with the exception of occurs with elevated TSS levels from ashfall, can potentially reduce/ Lallement et al. (2016). In the current study, we evaluated the effects eliminate zooplankton (Wolinski et al., 2013) or macroinvertebrates of ash deposition on fish species composition and abundances in rivers over the 21 months after the Chaitén eruption and related these effects to habitat and macroinvertebrate changes. One of our key fi fi Table 4 ndings was the pace of sh species recolonization after the volcanic Results of Redundancy Analysis for the first two axes with native (H. macraei) and exotic eruption. Fish that could occupy benthic habitats suffered lower im- (O. mykiss and S. trutta), before (2005–2006) and after (2008–2010) ash fall of Chaitén pacts on their numbers, but fishes with limited dispersal ability also volcano, in five stream of Chubut (Argentina). recolonized more slowly. Our study extended for 21 months follow- RDA ing the eruption, but it is clear that changes are continuing to occur, Axes summary especially in Esquel River. It is important to consider that natural dis- Total variance = 1.000 RDA 1 RDA 2 RDA 3 turbance events rejuvenate aquatic habitats over the long-term by providing critical sediment inputs for stream substrates, which be- Sum of canonical eigenvalues = 0.55 Eigenvalues 0.50 0.04 0.004 come the building blocks of complex aquatic habitat (Penaluna Species-environment (S-E) correlations 0.97 0.63 0.000 et al., 2018). Fish recovery is occurring, but whether recovery will re- Cumulative % variance of species data 50.6 54.5 54.9 turn rivers to preexisting conditions or whether fish assemblages Cumulative % variance of S-E relation 92.2 99.2 100.0 and river habitats emerge into a novel state is unclear. For this rea- Correlation with axes son, we suggest that fish restocking, an ad-hoc management strategy Total Suspended Solids - 0.90 −0.16 0.02 employed in the study area to enhance recreational fishing, is not Benthos density 0.55 −0.49 0.02 needed, as fish populations appear likely to recover successfully on Benthos species richness 0.55 −0.50 0.01 their own as suitable habitats become available. 10 C.Y. Di Prinzio et al. / Science of the Total Environment 752 (2021) 141864

CRediT authorship contribution statement Casalinuovo, M., Alonso, M., Macchi, P., Kuroda, J., 2017. Brown Trout in Argentina: His- tory, Interactions and Perspectives. Brown Trout: biology, ecology and management. Wiley, Hoboken, New Jersey, pp. 599–621. Cecilia Yanina Di Prinzio: Conceptualization, Data curation, Formal Castela, J., Ferreira, V., Gracia, M., 2008. Evaluation of stream ecological integrity using lit- analysis, Investigation, Methodology, Visualization, Software, Writing - ter decomposition and benthic invertebrates. Environ. Pollut. 153, 440–449. https:// original draft. Brooke Penaluna: Conceptualization, Formal analysis, doi.org/10.1016/j.envpol.2007.08.005. Collier, K., Parkyn, S., Quinn, J., Scarsbrook, M., 2002. Bouncing back: How fast can stream Methodology, Visualization, Supervision, Validation, Writing - original invertebrates recolonise? Water and Atmosphere. NIWA , pp. 9–11. www.niwa.co.nz/ draft. 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Annales de Limnology-International Journal of Lim- interests or personal relationships that could have appeared to influ- nology 48, 21–30. https://doi.org/10.1051/limn/2011055. ence the work reported in this paper. Di Prinzio, C.Y., Casaux, R.J., Miserendino, M.L., 2009. Effects of land use on fish assemblages in Patagonian low order streams. Annales de Limnology-International Journal of Limnology 45, 267–277. https://doi.org/10.1051/limn/2009030. Acknowledgements Di Prinzio, C.Y., Miserendino, M.L., Casaux, R., 2013. Feeding strategy of the non-native rainbow trout, Oncorhynchus mykiss, in low-order Patagonian streams. Fisheries – This paper was supported by the CONICET (PIP 11220080101907) Manag Ecol 20, 414 425. https://doi.org/10.1111/fme.12028. Di Prinzio, C.Y., Omad, G., Miserendino, M.L., Casaux, R., 2015. Selective foraging by non- and the Fulbright exchange scholarship to CDP to Oregon State Univer- native rainbow trout on invertebrates in Patagonian streams in Argentina. 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