Received: 25 March 2020 | Revised: 12 October 2020 | Accepted: 31 October 2020 DOI: 10.1111/gcb.15442 PRIMARY RESEARCH ARTICLE Two centuries for an almost complete community turnover from native to non-native species in a riverine ecosystem Phillip J. Haubrock1,2 | Francesca Pilotto3 | Gianna Innocenti4 | Simone Cianfanelli4 | Peter Haase1,5 1Department of River Ecology and Conservation, Senckenberg Research Abstract Institute and Natural History Museum Non-native species introductions affect freshwater communities by changing com- Frankfurt, Gelnhausen, Germany munity compositions, functional roles, trait occurrences and ecological niche spaces. 2Faculty of Fisheries and Protection of Waters, South Bohemian Research Reconstructing such changes over long periods is difficult due to limited data availa- Center of Aquaculture and Biodiversity of bility. We collected information spanning 215 years on fish and selected macroinver- Hydrocenoses, University of South Bohemia in České Budějovice, Vodňany, Czech tebrate groups (Mollusca and Crustacea) in the inner-Florentine stretch of the Arno Republic River (Italy) and associated water grid, to investigate temporal changes. We identified 3Environmental Archaeology Lab, Department of Historical, Philosophical and an almost complete turnover from native to non-native fish (1800: 92% native; 2015: Religious Studies, Umeå University, Umeå, 94% non-native species) and macroinvertebrate species (1800: 100% native; 2015: Sweden 70% non-native species). Non-native fish species were observed ~50 years earlier 4Museo di Storia Naturale ‘La Specola’, Sistema Museale di Ateneo dell'Università di compared to macroinvertebrate species, indicating phased invasion processes. In Firenze, Firenze, Italy contrast, α-diversity of both communities increased significantly following a linear 5Faculty of Biology, University of Duisburg– pattern. Separate analyses of changes in -diversities for native and non-native spe- Essen, Essen, Germany α cies of both fish and macroinvertebrates were nonlinear. Functional richness and di- Correspondence vergence of fish and macroinvertebrate communities decreased non-significantly, as Phillip J. Haubrock, Department of River Ecology and Conservation, Senckenberg the loss of native species was compensated by non-native species. Introductions of Research Institute and Natural History non-native fish and macroinvertebrate species occurred outside the niche space of Museum Frankfurt, Clamecystrasse 12, 63571 Gelnhausen, Germany. native species. Native and non-native fish species exhibited greater overlap in niche Email: [email protected] space over time (62%–68%) and non-native species eventually replaced native spe- cies. Native and non-native macroinvertebrate niches overlapped to a lesser extent (15%–30%), with non-natives occupying mostly unoccupied niche space. These tem- poral changes in niche spaces of both biotic groups are a direct response to the ob- served changes in α-diversity and species turnover. These changes are potentially driven by deteriorations in hydromorphology as indicated by alterations in trait mo- dalities. Additionally, we identified that angling played a considerable role for fish introductions. Our results support previous findings that the community turnover from native to non-native species can be facilitated by, for example, deteriorating en- vironmental conditions and that variations in communities are multifaceted requiring more indicators than single metrics. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2020 The Authors. Global Change Biology published by John Wiley & Sons Ltd 606 | wileyonlinelibrary.com/journal/gcb Glob Change Biol. 2021;27:606–623. HAUBROCK ET AL. | 607 KEYWORDS Arno River, fish, functional redundancy, hydromorphology, invasion, macroinvertebrates, time series analysis, traits 1 | INTRODUCTION role in outlining species-specific behaviours and local adaptations, such as adaptive feeding behaviour due to, for example, emergent Global changes are increasing the spread of non-native species multiple predator effects (e.g. Barrios-O'Neill et al., 2014; Lindqvist & (Capinha, Brotons, et al., 2013; Capinha, Larson, et al., 2013; Mazza Huner, 2017). Of particular interest is the introduction of new traits et al., 2014), often causing irreversible ecological damages (Essl et al., through new species, such as a higher fertility (e.g. Bishai et al., 1974; 2020; Gozlan, 2008; Gozlan & Newton, 2009). Freshwater systems Marchetti et al., 2004; Usher, 1986) elevated abiotic tolerances (Copp have been identified to be particularly vulnerable to invasions (Gherardi, et al., 2009; Gherardi, 2006), novel defences or predation techniques 2007; Ricciardi & Rasmussen, 1999; Sala et al., 2000; Strayer, 2010). (Bosher et al., 2006; Fine et al., 1997; Kimbro et al., 2009). Moreover, Several freshwater species, particularly fish, molluscs and crustaceans, non-native species can alter the trait compositions of native species have been intentionally or unintentionally introduced into lakes and with specific traits potentially disappearing due to increasing compe- rivers by humans (e.g. Haubrock, Kubec, et al., 2019; Mrugała et al., tition (Brown et al., 2002; Mangla et al., 2011) or resource partition- 2015). For example, the introduction of edible non-native crustaceans ing (Haubrock, Azzini, et al., 2019; Jackson et al., 2014). Such studies (e.g. Procambarus clarkii) and molluscs (e.g. Corbicula spp.) has fre- indicated that the analysis of species traits can elucidate important quently been related to cultural introductions (e.g. religious releases or biotic interactions between native and non-native species. However, the introduction of species native in the original area of a certain culture the dynamics of trait composition through time have not gained suffi- to mantain traditions, see e.g. Bodon et al., in press; Britton & Morton, cient scientific attention and remain mostly anecdotal (Fox et al., 2007; 1979; Cianfanelli et al., 2017; Counts, 1983; Liu et al., 2013), while the Lindqvist & Huner, 2017). This is particularly true in the context of introduction of a broad spectrum of fish and other macroinvertebrate multiple introduction events (Chapple et al., 2012) and in comparative species is often related to stockings, ballast water of ships, aquaculture analyses across different biotic groups. and recreational angling (Cambray, 2003; Savini et al., 2010). One ecosystem where information on the temporal course of fish According to the invasion meltdown theory (Crane et al., 2020; and macroinvertebrate species introductions does exist is the Arno Simberloff, 2006; Simberloff & Von Holle, 1999), the successive intro- River in Tuscany (Italy), which is known for its anthropogenic usage duction of non-native species can, above a certain threshold, facilitate and economic importance for the development of the city of Florence the introduction of further non-native species, potentially increasing (Masters, 1998; Rinaldi & Simon, 1998; Sznura, 2010). We compiled effects on native communities (Ellender & Weyl, 2014). Investigating presence/absence data for fish and macroinvertebrate species (mol- effects of such frequent non-native species introductions in freshwa- luscs and crustaceans) from the Arno River between ~1800 and 2015, ter ecosystems, however, generally suffers from a lack of appropriate as well as their species-specific trait information and analysed temporal long-term data that are needed to reconstruct introduction events changes in species and trait composition for the two biotic groups. In (Strayer et al., 2006) as well as the resulting changes in the (native) com- particular, we calculated changes in (a) α-diversity and temporal turn- munity (Haubrock, Azzini, et al., 2019; Haubrock, Balzani, et al., 2019). over, (b) trait modalities as a prerequisite to (c) functional composition, Historical notes on the occurrence of non-native species play an im- functional metrics and resulting niche space to understand whether portant role as they can allow to reconstruct a timeline of species intro- non-native species occupy an empty or occupied niche, which would duction and to reliably approximate species population trends (Bried & inform on competition dynamics. Finally, we (d) inferred and discussed Siepielski, 2018; Bucharova & van Kleunen, 2009; Carlton, 2009). Such potential drivers of these changes. For the latter, we faced the com- temporal information retrieved from early natural history collections, mon issue of lacking continuous information on environmental vari- scientific records, surveys or citizen science (Horns et al., 2018) often ables over such a long period of time. We thus compensated for this are based on presence/absence data, which can potentially be used to using changes in traits that reflect changes in certain environmental compare species occurrences over time (Pollock, 2006). Nevertheless, conditions as proxies, and by compiling information on environmental such information must be carefully evaluated due to the often unclear change using historical notes. origin and the sampling method applied. We hypothesized (i) a significant temporal turnover in species Temporal changes in community composition triggered by fre- over the past 215 years driven by the successive introduction of non- quent introductions of non-native species not