Diet and Feeding Ecology of Non-Native Fishes in Lentic and Lotic Freshwater Habitats

Home , Bottom feeder

Aquatic Invasions (2018) Volume 13, Issue 4: 565–573 DOI: https://doi.org/10.3391/ai.2018.13.4.13 © 2018 The Author(s). Journal compilation © 2018 REABIC This paper is published under terms of the Creative Commons Attribution License (Attribution 4.0 International - CC BY 4.0) Special Issue: Biological Invasions in Inland Waters

Research Article

Diet and feeding ecology of non-native fishes in lentic and lotic freshwater habitats

Diego Azevedo Zoccal Garcia1,2,*, Ana Paula Vidotto-Magnoni2 and Mário Luís Orsi2 1Programa de Pós-Graduação em Ciências Biológicas, Universidade Estadual de Londrina, Rodovia Celso Garcia Cid, Laboratório de Ecologia de Peixes e Invasões Biológicas, Londrina, PR, CEP 86.057-970, Brazil 2Laboratório de Ecologia de Peixes e Invasões Biológicas, Universidade Estadual de Londrina, Rodovia Celso Garcia Cid, Londrina, PR, CEP 86.057-970, Brazil *Corresponding author E-mail: [email protected] (DAZG), [email protected] (APVM), [email protected] (MLO)

Received: 24 May 2018 / Accepted: 31 October 2018 / Published online: 12 November 2018 Handling editor: Jean Vitule

Abstract

The Paranapanema River is most frequently invaded by non-native fish from the Upper Paraná River Freshwater Ecoregion. To understand how the diet of non-native fishes varies based on habitat type, we studied 12 populations of 6 non-native fish species with the aim of verifying whether diet, niche breadth, or trophic guild vary between lentic and lotic habitats. Fish were sampled in both habitats in the Paranapanema River basin between August 2014 and March 2016. A permutational multivariate analysis of variance – PERMANOVA was applied so that the composition of fish diet could be compared between habitats. Levin’s standardized index was used to evaluate the trophic niche breadth of the species, revealing differences in the diets of Ossancora eigenmanni, Auchenipterus osteomystax and Trachelyopterus galeatus based on habitats. Seven trophic guilds were identified, and those for Serrasalmus marginatus, Loricariichthys platymetopon, and T. galeatus were the same (piscivores, detritivores, and omnivores, respectively) in both habitats. In contrast, the trophic guilds of O. eigenmanni, A. osteomystax, and Plagioscion squamosissimus varied between the habitats. Habitat-specific variability in the diet composition of the species and, for the most, the niche breadth in the lotic habitats increased; therefore, we conclude that this type of environment can provide access to a greater variety of food resources for non-native fishes. Key words: allochthonous species, biological invasions, establishment, food resources, niche breadth, reservoir, upper Paraná river

Introduction identifying the environmental, biological, and human factors responsible for the successful establishment Invasive aquatic species have extended their distri- of invasive species, it is important to discover bution ranges in worldwide ecosystems as a result of features that are common among species and invaded barrier removal, canal construction, commercial and areas (Shea and Chesson 2002). ornamental aquaculture, and human mobility (Leprieur Invasive fish species are particularly pervasive, et al. 2008; Gozlan et al. 2010; Seebens et al. 2017; causing food web disruption (Britton et al. 2010; Martin Lima Junior et al. 2018). Aquatic invaders can disrupt et al. 2010; Gallardo et al. 2016; Copp et al. 2017) and ecosystem processes by reducing the abundance and threatening biodiversity (Pelicice and Agostinho 2009; diversity of native communities (Gallardo et al. Matsuzaki et al. 2016). However, food resources impact 2016). Food web alterations can then occur because population fitness and define the permanence of non- of influences on established trophic interactions in native species (Zambrano et al. 2010). Furthermore, aquatic communities (Vitousek 1990; Shea and the spatial and temporal variability promoted by Chesson 2002; Gallardo et al. 2016). In addition to human activities (e.g., construction of dams) favors

565 D.A.Z. Garcia et al. non-native species with higher tolerances to changes samples from lentic and lotic habitats in the Paraná in physicochemical characteristics and plasticity in life River watershed. The species chosen are typically history traits (Marchetti et al. 2004; Gozlan et al. 2010). the most abundant in the Upper Paraná River flood- Among the goals of biological invasion studies plain. In the invaded area, these species occur in are predicting those environments most susceptible multiple habitats that have differing hydro-geomor- to invasion, defining species that will become invasive, phological characteristics due to natural features and and identifying factors that facilitate establishment impacts promoted by dams. Environmental differences (Marchetti et al. 2004; Fleming and Dibble 2015). reflect food availability, and it is expected that the Several factors are associated with the invasion non-native fish populations will present different success of a species. Among them are its life history feeding behaviors. We tested the hypothesis that for characteristics, such as tolerance to environmental shifts specialist species, the diet will not vary as the (Moyle and Light 1996a), rapid growth (Graebner et resources consumed do not vary. The trophic niche al. 2012), reproductive investment (Lodge 1993; breadth will be the same; however, for generalists, Simberloff and Rejmanek 2011), and feeding plasti- diet will be more variable in lotic habitats due to the city (Agostinho et al. 2015; Pander et al. 2016). In incorporation of the allochthonous material that will this context, improved knowledge of the feeding increase the availability of feeding resources. There- ecology of non-native fishes is needed to understand fore, it is probable that lotic habitats with riparian the invasion process (Moyle and Ellsworth 2004; vegetation on both margins may provide feeding Kornis et al. 2013) and to develop management resources that are more diverse. strategies (García-Berthou 2007; Leuven et al. 2017). Therefore, it is important to describe the use of food Methods resources under the influence of various environmental conditions so that habitats that are susceptible to Study area species invasion can be identified, and information The springs of the Paranapanema River are located for controlling the spread of those species can be in the Serra de Paranapiacaba (southeastern Brazil) provided (Ricciardi and Rasmussen 1998; Kolar and at 900 m altitude, flowing 930 km to the west before Lodge 2001; Sepulveda 2018). its confluence with the Paraná River (Figure 1). Plasticity in life history traits is a feature of Originally, the Paranapanema River basin contained successful invaders; they can rapidly respond to new the Atlantic Rainforest and Brazilian Savannah conditions (Gozlan et al. 2010). Some studies address biomes (hotspots) that have since been converted to fish escapes from aquaculture facilities, impacts on agriculture and livestock uses. other species, or invasion status (Pelicice and Agostinho This study was performed in two types of habitats 2009; Vitule et al. 2009; Ortega et al. 2015; Xiong et in the Lower Paranapanema River basin: lentic al. 2015; Casimiro et al. 2018; Garcia et al. 2018). (Lagoon 1 and Lagoon 2) and lotic (the Pirapozinho Other studies aim to understand the conditions that and Anhumas rivers, Figure 1, Supplementary material determine invasion success (Agostinho et al. 2015; Table S1). The lagoons studied were formed after Pazianoto et al. 2016; Cassemiro et al. 2018; Franco the Rosana Reservoir was filled in 1986. Lagoon 1 is et al. 2018; Tonella et al. 2018). The biology of located in the state of São Paulo and borders the Neotropical freshwater fishes comparing native and Morro do Diabo State Park, whereas Lagoon 2 is non-native ranges have been the focus of multiple located in the state of Paraná. The Pirapozinho and other studies, including trophic ecology (Agostinho et Anhumas rivers are located in the state of São Paulo al. 2015; Lima Junior et al. 2015; Tonella et al. 2018). and flow directly into the reservoirs of Rosana and When a natural geographic barrier (Sete Quedas Taquaruçu, respectively. Falls) to movement of some fish species was flooded with the construction of the Itaipu Dam, a massive Sampling invasion of the Upper Paraná from the Lower Paraná basin resulted. After this event, more than 30 fish Fishes were sampled quarterly from August 2014 to species colonized the Upper Paraná River floodplain March 2016 by capturing with a seine (6.0 m2, 0.5 cm and some of its tributaries (Júlio Júnior et al. 2009; mesh) and sieve (0.4 m2, 0.5 cm mesh) over a time Vitule et al. 2012). Some species became dominant span of one hour by five people. Furthermore, 14 (in terms of abundance) and have successfully invaded gillnets were used (2 to 14 cm meshes between the new basin (Agostinho et al. 2004; Luiz et al. opposing knots), 1,000 m2 of net per site. Nets were 2004; Bailly et al. 2011; Tonella et al. 2018). placed near aquatic macrophytes, at sunset and Here, we describe diet composition, niche breadth, removed the following morning, being exposed for and trophic guild for six of these species based on approximately 12 hours. Fishes were anesthetized by

566 Diet and feeding ecology of non-native fishes

Figure 1. Map of the sampling sites of the Paranapanema River basin, southeast/southern Brazil. A = Rosana Dam; B = Taquaruçu Dam; C = Capivara Dam.

immersion in a water solution of clove oil (Animal Data analysis Ethics Committee of Universidade Estadual de Londrina n. 30992.2014.33). They were then fixed with 10% Fish diets were determined by analyzing stomach formalin buffered with calcium carbonate. In the contents through the use of stereoscopic and optical laboratory, fishes were identified using specialized microscopes. Food items were identified to the literature (Britski et al. 2007; Graça and Pavanelli lowest possible taxonomic level using specific iden- 2007; Ota et al. 2018) and by specialists from the tification keys. Dietary analysis was based on the Museu de Zoologia of the Universidade Estadual de volume of each food item (Hyslop 1980), obtained Londrina, then transferred to 70% ethanol. by displacing large items in water in a graduated A total of 290 individuals belonging to six successful cylinder (0.1 ml graduations) or small items on a non-native species were studied: Serrasalmus margi- glass millimeter plate (mm3). The volume obtained natus Valenciennes, 1837 (Serrasalmidae; 27 indivi- (mm3) was converted to milliliters when the volume duals); Loricariichthys platymetopon Isbrücker and was less than 0.1 ml (Hellawell and Abel 1971). Nijssen, 1979 (Loricariidae; 51 individuals); Ossancora For each species, differences in dietary compo- eigenmanni (Boulenger, 1895) (Doradidae; 26 indivi- sitions between lentic and lotic habitats were tested duals); Auchenipterus osteomystax (Miranda-Ribeiro, using permutational multivariate analysis of variance 1918) (Auchenipteridae; 27 individuals); Trachelyo- (PERMANOVA; Anderson et al. 2008), which was pterus galetaus Linnaeus, 1766 (Auchenipteridae; 98 applied to a matrix of food items per analyzed individuals); and Plagioscion squamosissimus (Heckel, stomach. The Bray-Curtis distance was used as a 1840) (Sciaenidae; 61 individuals). Stomachs were measure of dissimilarity, and 9999 permutations removed and deposited in 70% ethanol for additional were used to test the significance of the pseudo-F analysis. The first quarter of the intestine of L. platy- statistic derived from PERMANOVA. Statistical metopon was also used in the analysis. analyses were conducted using the R Programming

567 D.A.Z. Garcia et al.

Environment and the Vegan package (The R Project Table S2). Loricariichthys platymetopon primarily for Statistical Computing, http://www.r-project.org/; fed on organic detritus (volume ~ 80%) in both habi- Oksanen et al. 2007). tats. The diet of P. squamosissimus was composed Trophic niche breadth was estimated for each species primarily of the Decapoda and fish in both habitats. using Levin’s standardized index: BA = (B−1)/(n−1), where BA is Levin’s standardized index, n is the Trophic niche breadth number of items, and B = 1/(∑ ), where B is the trophic niche breadth, and pi is the proportion of Wider niche breadths were verified for A. osteomystax, item i in the diet (Krebs 1998). This calculates the S. marginatus, L. platymetopon, and P. squamosissimus evenness of distribution for any one item among the in lotic habitats, where the greatest richness and various food resources. evenness of food items was found (Figure 2, Table S2). Trophic guilds were determined for each habitat On the other hand, O. eigenmanni and T. galeatus because fishes can vary their feeding responses accor- demonstrated wider niche breadths in lentic habitats. ding to the environment. Trophic guilds were based on those described by Delariva et al. (2013) and Trophic guild adapted from Mérona et al. (2001): detritivores: more Fish exhibited seven trophic guilds (Figure 2, Table S2). than 50% detritus/sediment in the stomachs; plankti- Serrasalmus marginatus (piscivore), L. platymetopon vores: more than 50% plankton in the stomachs; (detritivore), and T. galeatus (omnivore) maintained terrestrial insectivores: more than 50% terrestrial their feeding habits in both types of habitats. In insects in the stomachs; carcinophagous: more than contrast, there was a clear shift in O. eigenmanni, 50% decapods (crab and shrimp) in the stomachs; which was invertivorous and planktivorous in lentic invertivores: more than 50% others invertebrates in the and lotic habitats, respectively, in A. osteomystax, stomachs; piscivores: more than 50% fish (including which was planktivorous in lentic habitats and ter- scales and the rays of fish fins) in the stomachs; restrial insectivorous in lotic habitats, and in P. squa- omnivores: none of the above but including items of mosissimus, which presented the carcinophagous animal and plant origins (leaf, flower, fruit, or seed habit in lentic habitats and the piscivorous habit in of higher plants). lotic habitats (Figure 2, Table S2).

Results Discussion Diet composition Non-native species invade new areas once they The diets of O. eigenmanni, A. osteomystax, and overcome environmental barriers and become T. galeatus differed between habitats (PERMANOVA, established (Colautti and MacIsaac 2004; Blackburn Pseudo-F1,21 = 1.75, P = 0.042; Pseudo-F1,12 = 2.31, et al. 2011). The specialists S. marginatus (piscivorous) P = 0.004; Pseudo-F1,70 = 1.94, P = 0.005, respectively), and L. platymetopon (detritivorous), and omnivorous whereas those of S. marginatus, L. platymetopon, T. galeatus are among the most abundant species in and P. squamosissimus did not (Pseudo-F1,24 = 1.37, various biotopes of the Upper Paraná River floodplain P = 0.205; Pseudo-F1,48 = 1.99, P = 0.100; Pseudo- (Agostinho et al. 2004; Luiz et al. 2004; Bailly et al. F1,40 = 0.75, P = 0.602, respectively). The diet of 2011), because they have feeding plasticity, and the O. eigenmanni was composed predominantly of the environment provides greater availability of food Gastropoda, Ostracoda, Acari, and Trichoptera (larvae) resources (Tonella et al. 2018). In this study, these in lentic habitats, but of Copepoda and Ostracoda with species maintained the same trophic guilds in lentic associated detritus (organic and inorganic) in lotic and lotic habitats. The ability to maintain large habitats (Figure 2, Table S2). Cladocera was the populations through the same food resource ingestion primary food item found in the stomachs of provides invasion success (Gido and Franssen 2007). A. osteomystax in lentic habitats, but Coleoptera and In contrast, O. eigenmanni, A. osteomystax, and others terrestrial insects dominated in lotic areas. P. squamosissimus (generalist species) differed their Coleptera and plant materials were predominant in trophic guilds in both habitats. These populations diet of T. galeatus in lentic habitats, whereas plant showed opportunistic diets, and most of them materials (> 45% by volume), and the Decapoda, showed wider trophic niche breadth in lotic habitats. Aranae, terrestrial insects, and Orthoptera were Auchenipterus osteomystax, for example, the wider dominant in lotic habitats. trophic niche breadth in lotic habitats can be attributed The diet of S. marginatus was composed primarily to the greater availability of allochthonous resources of fish in both lentic and lotic habitats (Figure 2, in this environment. It is noteworthy that organisms

568 Diet and feeding ecology of non-native fishes

Figure 2. Diet composition (% volume) of non-native fishes sampled in lentic and lotic habitats of the Paranapanema River basin, southern Brazil: Serrasalmus marginatus (A), Loricariichthys platymetopon (B), Ossancora eigenmanni (C), Auchenipterus osteomystax (D), Trachelyopterus galeatus (E), and Plagioscion squamosissimus (F). Cla = Cladocera; Cra = Crab; Shr = Shrimp; Cop = Copepoda; Ost = Ostracoda; Aca = Acari; Ara = Aranae; EpN = Ephemeroptera (nymph); EpA = Ephemeroptera (adult); OdN = Odonata (nymph); OdA = Odonata (adult); Ort = Orthoptera; Hom = Homoptera; Col = Coleoptera; Dip = Diptera; TrL = Trichoptera (larvae); Hym = Hymenoptera; Aqi = Aquatic insetc; Tei = Terrestrial insect; Gas = Gastropoda; Fis = Fish; Pla = Plant material; Alg = Algae; Ode = Organic detritus; Ide = Inorganic detritus/sediment.

with hard parts may be over-represented compared also have facilitated the establishment (Pereira et al. to soft-bodied organisms that may digest faster. 2016; Tonella et al. 2018). In this floodplain, a The successful establishment of S. marginatus coexistence between the native S. maculatus and the into the Upper Paraná River basin can be attributed non-native S. marginatus was created by trophic to its behavioral and reproductive aspects (Agostinho niche segregation (Alves et al. 2017). In this study, 2003; Agostinho et al. 2004). The aggressive territorial the species in lentic habitats showed high propensity behavior might be the reason for declines in (volume ~ 90%) to feed on fish, probably juveniles populations of the native congener Serrasalmus and small fish inhabiting the lagoons of the Lower maculatus Kner, 1858 in the Upper Paraná River Paranapanema River (Casatti et al. 2003). The highest basin (Agostinho and Júlio Júnior 2000; Agostinho trophic breadth in lotic habitats may be due to the greater 2003). The piscivorous habit of S. marginatus may consumption of plant material. This consumption

569 D.A.Z. Garcia et al. may occur due to accidental ingestion when catching 2012; Tonella et al. 2018) because these food items fish that live close to aquatic macrophytes and are highly available in reservoirs (Bonecker et al. riparian vegetation present in the both margins. 2001; Rocha et al. 2009). Detritivory is one of the most specialized fish The diet of T. galeatus was highly diverse, trophic habits (Gerking 1994), possibly explaining showing that this species is better able to explore why the diets were similar between the habitats used feeding resources in lentic habitats, where it had a by L. platymetopon. The dominance of detritus and wider niche breadth. Omnivorous fish have high sediment in the diet of L. platymetopon contributed food plasticity (i.e., they can shift food resources), to its low trophic niche breadth. However, species and the broad diet of T. galeatus is an advantageous that feed at low levels in the food web tend to become strategy in the invasion process (Moyle and Light integrated into the community (Gido and Franssen 1996b; Ruesink 2005). In the early stages of life, its 2007) because detritus is rarely limited in aquatic diet is composed primarily of aquatic insects and environments (Moyle and Light 1996a; Winemiller microcrustaceans (Santin et al. 2015). Throughout its and Kelso-Winemiller 2003). Therefore, detritivory development, individuals continue to prefer insects is considered a useful food strategy for invasive species (Andrian and Barbieri 1996; Hahn et al. 1998; Ximenes (Gido and Franssen 2007; Agostinho et al. 2015; Liew et al. 2011). Reportedly, T. galeatus is opportunistic et al. 2016; Pazianoto et al. 2016). Furthermore, the when feeding on fruit, which composed a large part environments studied are located in stretches of the of its diet, primarily in the lotic habitats. Oppor- Paraná River, whose dynamics includes periods of tunistic feeding is an attribute of invasive aquatic flooding and entry of this resource into the system. species that facilitates establishment (Ricciardi and Ossancora eigenmanni showed an opportunistic Rasmussen 1998). In addition to the invasive detriti- habit in invertebrates in lentic habitats and in plankton vores, the omnivores promote increased turbidity (Copepoda and Ostracoda) with associated detritus and nutrient concentration (Mormul et al. 2012; in lotic habitats. The invertivorous habit adopted in Gallardo et al. 2016), possibly leading to a reduction lentic habitats resulted from the abundance of this in the abundance of submerged macrophytes, a result resource in lagoon bottoms and morphological adap- of changes in nutrient dynamics through excretion and tations for feeding on benthic organisms. Its mouth bioturbation (Matsuzaki et al. 2007). Omnivorous fish is terminal with dentigerous plaques in both jaws can still decrease the abundance of benthic inverte- (Graça and Pavanelli 2007). In lotic habitats, greater brates by direct consumption, habitat disturbance, or consumption of organisms associated with detritus uprooting of macrophytes (Matsuzaki et al. 2009; resulted in narrower trophic niche breadth. Despite Gallardo et al. 2016). this, the planktivorous habit adopted by O. eigen- Plagioscion squamosissimus proved to be a manni in lotic habitats might indicate that the species shrimp specialist (carcinophagous) in lentic habitats. can adopt this strategy to facilitate invasion (Gido and In contrast, the species shows a piscivorous habit Franssen 2007; Agostinho et al. 2015). Therefore, (> 50% fish) and wider niche breadth in lotic habitats. bottom-feeder species such as L. platymetopon and In both native (Williams et al. 1998) and invaded areas O. eigenmanni are likely to establish wherever they (Hahn et al. 1997; Stefani and Rocha 2009; Capra and are introduced because their resources are unlimited. Bennemann 2009; Vidotto-Magnoni and Carvalho The impacts of bottom-feeders include feeding on 2009), the diet of P. squamosissimus varies among the eggs of invertebrates and other fishes and fish, crustaceans, plant materials, and insects (e.g., competing with bottom-dwelling fish for food Ephemeroptera, Odonata, and Chironomidae). The (Chaichana and Jongphadungkiet 2012). variety of food items consumed by P. squamosis- Auchenipterus osteomystax fed primarily on the simus indicates food plasticity; it can be considered a Cladocera in lentic habitats (planktivores) and on the generalist (Stefani and Rocha 2009). Nevertheless, Coleoptera and terrestrial insects in lotic habitats in most cases, when P. squamosissimus eats shrimp, (terrestrial insectivores). This species is generally this is the only type of food item available (Bennemann characterized as aquatic insectivorous (Hahn et al. et al. 2006). In the Upper Paraná basin, the carnivo- 1998; Barili et al. 2012; Tonella et al. 2018). The rous habit has important roles in the feeding patterns presence of riparian vegetation interfered positively of the species, from early stages (feeding on the in the diet of A. osteomystax because of contribu- Cladocera and Copepoda) until adulthood (eating tions of allochthonous materials as food items mainly shrimp and fish; Neves et al. 2015). (Coleoptera and terrestrial insects). Its ability to eat Although O. eigenmanni and T. galeatus showed aquatic and terrestrial insects and microcrustaceans greater abilities to exploit feeding resources in lentic (e.g., Cladocera) guaranteed success in colonizing of habitats (wider trophic niche breadth), the riparian reservoirs of the Upper Paraná basin (Barili et al. vegetation present in both margins in the lotic habitats

570 Diet and feeding ecology of non-native fishes provided a broader food spectrum to aquatic commu- Andrian IF, Barbieri G (1996) Espectro alimentar e variações sazonal nities and enlarged the niche breadth of the other e espacial da composição da dieta de Parauchenipterus galeatus Linaeus, 1766, (Siluriformes, Auchenipteridae) na região do species. The greater availability of food resources for fish reservatório de Itaipu, PR. Revista Brasileira de Biologia 56: occurs mainly during high-water periods (Junk et al. 409–422 1989; Walker et al. 2013). Here, the results partially Barili E, Fugi R, Novakowski GC, Agostinho AA (2012) support the hypothesis that wider niche breadth are Impoudment effects in the population of Auchenipterus osteomystax (Siluriformes: Auchenipteridae): a Neotropical reservoir expected in lotic environments without damming case. Revista de Biología Tropical 60: 699–708, https://doi.org/ impacts. 10.15517/rbt.v60i2.3985 In summary, the successful colonization of these Bailly D, Batista-Silva VF, Abelha MCF, Kashiwaki EAL, Fernandes CA, Carvalho ED (2011) Relative abundance and reproductive non-native fish species in new areas is expected because tatics of a Loricariidae species at Saraiva Lagoon, Ilha Grande they have diet plasticity as an adaptive advantage. While National Park, MS-PR, Brazil. Biota Neotropica 11: 171–178, S. marginatus, L. platymetopon, and P. squamosis- https://doi.org/10.1590/S1676-06032011000300014 simus (specialist species) did not vary their diet Bennemann ST, Capra LG, Galves W, Shibatta OA (2006) Dinâmica trófica de Plagioscion squamosissimus (Perciformes, Sciaenidae) compositions according to habitats, O. eigenmanni, em trechos de influência da represa Capivara (rios Paranapanema A. osteomystax, and T. galeatus did so. Furthermore, e Tibagi). 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Supplementary material The following supplementary material is available for this article: Table S1. Characterization of the sampling sites of the Paranapanema River basin, southern Brazil. Table S2. Standard length range, diets composition, trophic niche breadth and trophic guilds of non-native fishes sampled in lentic and lotic habitats of the Paranapanema River basin, southern Brazil. This material is available as part of online article from: http://www.aquaticinvasions.net/2018/Supplements/AI_2018_Garcia_etal_SupplementaryTables.xlsx

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