Influence of riparian forests on fish assemblages in temperate lowland streams
Franco Teixeira-de Mello, Mariana Meerhoff, Ivan González-Bergonzoni, Esben Astrup Kristensen, Annette Baattrup-Pedersen, et al. Environmental Biology of Fishes ISSN 0378-1909 Volume 99 Number 1 Environ Biol Fish (2016) 99:133-144 DOI 10.1007/s10641-015-0462-9
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Author's personal copy Environ Biol Fish (2015) 99:133–144 DOI 10.1007/s10641-015-0462-9
Influence of riparian forests on fish assemblages in temperate lowland streams Franco Teixeira-de Mello & Mariana Meerhoff & Ivan González-Bergonzoni & Esben Astrup Kristensen & Annette Baattrup-Pedersen & Erik Jeppesen
Received: 24 March 2015 / Accepted: 6 November 2015 / Published online: 17 November 2015 # Springer Science+Business Media Dordrecht 2015
Abstract The characteristics of riparian vegetation along streams vary with natural and anthropogenic factors. Deforestation for agricultural purposes has consequences for the physical in-stream structure and function, such as the predominance of autotrophic or heterotrophic stream metabolism. Open canopy lowland streams are often dominated by macrophytes, with potential direct and indirect effects on the fish community. We tested for possible differences in the structure (relative abundance of species, mean body size, and density) and composition (species richness, species identity, and different trophic groups) of fish assemblages between open canopy streams (OCS) and riparian forest streams (RFS), including pool and riffle habitats, in temperate lowland Denmark. OCS reaches exhibited higher alpha and beta diversity and frequently hosted rare species. Almost 50 % of the recorded species appeared only in OCS.
OCS also had smaller mean body size of fish and tended to have higher fish densities. The relative abundance of the different trophic groups did not differ between the two streams types, but the RFS had a higher abundance and occurrence frequency of intolerant salmonids. Our results suggest that modification of riparian habitats can affect richness patterns and that strong functional changes may occur as a consequence of forest clearance through changes in the relative importance of a keystone species, trout (Salmo trutta).
F. Teixeira-de Mello (*) : M. Meerhoff : I. González-Bergonzoni Departamento de Ecología Teórica y Aplicada, CURE-Facultad de Ciencias, Universidad de la República, Tacuarembó s/n, Maldonado, Uruguay e-mail:
[email protected]
The characteristics of lowland streams vary with natural and/or anthropogenic factors (e.g. Moldenke and ver Linden 2007; Julian et al. 2011), among which the most commonly mentioned is a longitudinal decrease in the influence of forests from headwaters to mouth, with well-known consequences for the physical in-stream structure and function, at least in the temperate zones (Vannote et al. 1980; Gregory et al. 1991). For example, whether autotrophic and heterotrophic stream metabolism predominates is strongly dependent on the relative importance of the organic matter input from riparian vegetation, such as leaf litter, and light availability, the latter affecting the development of autochthonous primary producers such as periphyton and macrophytes
M. Meerhoff : A. Baattrup-Pedersen : E. Jeppesen Department of Bioscience and Arctic Research Centre, Aarhus University, Vejlsøvej 25, 8600 Silkeborg, Denmark E. A. Kristensen Alectia A/S, Skanderborgvej 190, 8260 Viby J., Denmark E. Jeppesen Sino-Danish Centre for Education and Research (SDC), Beijing, China
Keywords Fish ecology . Deforestation . Stream macrophytes . Temperate streams . Lowland stream . Salmo trutta
Introduction
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(Anderson and Sedell 1979; Vannote et al. 1980; Cummins et al. 1989; Sweeney 1993; Davies et al. 2008; Julian et al. 2011). In cold-temperate parts of Europe, the predominant terrestrial biome is temperate forests, which should therefore be present under natural conditions along most streams. However, most lowland plains have undergone significant changes due to conversion to agricultural land, including intense deforestation transforming forested riparian land into open canopy. These changes have caused tremendous impacts in stream characteristics. In forested streams, large woody debris create different types of habitats with varying depth and substrate characteristics (Keller and Swanson 1979; Bilby 1984), whereas macrophytes create habitat variability in open canopy streams (Sand-Jensen et al. 1989; Bell et al. 2013). Furthermore, streams with riparian forests (RFS) are partially shaded and the temperature fluctuations are moderated, resulting in lower in-stream primary production (Karr and Schlosser 1978; Peterjohn and Correll 1984; Osborne and Kovacic 1993; Sweeney 1993; Rasmussen et al. 2011; Kristensen et al. 2015). Open canopy streams (OCS), in contrast, receive more light and potentially a higher nutrient input through runoff from agricultural land (Peterjohn and Correll 1984; Kronvang et al. 2005), which may lead to higher densities of primary producers, primarily macrophytes and associated periphyton (Kelly et al. 1983; SandJensen et al. 1989), with fluctuating temperature and oxygen levels as a result (Sand-Jensen et al. 1989; Julian et al. 2011; Kristensen et al. 2015). High primary production may further stimulate secondary production. It has been observed that the abundance of macroinvertebrates is considerably higher where macrophytes are present than in non-vegetated areas (e.g. Orth et al. 1984; Gregg and Rose 1985; Iversen et al. 1985; Shupryt and Stelzer 2009). Macrophytes can also minimize the predation risk on several invertebrate groups and small fishes (Stoner 1979; Rozas and Odum 1988; Jordan 2002; Meerhoff et al. 2007; Teixeira-de Mello et al. 2009). Lowland streams in Denmark are typically either forested or open canopy streams. Here, we investigated how the different characteristics of these two stream types affect fish assemblages. The specific aim was to test for differences in the structure (relative abundance of species, density, and mean body size) and composition (species richness, species identity, and trophic groups) of fish assemblages. We hypothesized that: i) fish diversity
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would be higher under more natural conditions in riparian forest streams (since the small fluctuations in oxygen and low temperature levels could allow co-occurrence of both tolerant and intolerant species) and that, ii) the higher abundance of macrophytes in open canopy streams would promote higher fish abundance and smaller-bodied species (likely through enhanced food availability and refuge against predation). Also, we compared the relative importance of fish trophic groups in the two stream types since different trophic groups could be favored by several direct and indirect mechanisms associated with the contrasting habitat conditions (e.g. refuge, food availability, sizedependent biotic interactions).
Methods We analyzed 24 stream segments, each 50-m long, including pool and riffle habitats, in 18 streams located in agricultural areas in Jutland, Denmark (Fig. 1). They were all lowland streams with middle-sized catchments ( 0.05) (Fig. 5a). None of the streams in Table 3 Percentage of riparian forest (RFS) and open canopy streams (OCS) hosting each fish species (n = 12 for each stream type), ordered from top to bottom according to the higher frequency of occurrence in RFS
Species
either of the two groups was classified as having high ecological status. However, the category Bbad status^ appeared only in OCS, and the proportion of streams with Bgood status^ was higher in RFS (Fig. 5b). DFFV was not calculated in three RFS streams having only two fish species present as the index requires presence of at least three species (Kristensen et al. 2014).
Discussion In contrast to our first hypothesis, the OCS reaches exhibited higher α and β diversity and frequently hosted rare species (i.e. fish species with low density and low
Common name
OCS streams
RFS streams
Salmo trutta
Brown trout
75
83
Anguilla anguilla
European eel
67
75
Gasterosteus aculeatus
Three-spined stickleback
100
58
Lampetra fluviatilis
European river lamprey
75
58
Rutilus rutilus
Roach
25
42
Gobio gobio
Gudgeon
8
33
Perca fluviatilis
European perch
33
25
Lota lota
Burbot
0
25 8
Pungitius pungitius
Nine-spined stickleback
25
Leuciscus leuciscus
Common dace
42
0
Esox lucius
Northern pike
33
0
Gymnocephalus cernuus
Ruffe
25
0
Oncorhynchus mykiss
Rainbow trout
25
0
Cottus gobio
Bullhead
17
0
Phoxinus phoxinus
Eurasian minnow
17
0
Thymallus thymallus
Grayling
17
0
Carassius carassius
Crucian carp
17
0
Barbatula barbatula
Stone loach
8
0
Platichthys flesus
Flounder
8
0
Salmo salar
Atlantic salmon
8
0
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Fig. 3 Accumulation (Clench) curve of fish species in open canopy (OCS) and riparian forest (RFS) streams and standard deviations. Non-linear estimation with the Simplex & Quasi-Newton algorithm
frequency of occurrence), with almost 50 % of the recorded species appearing only in OCS. However, the RFS did indeed show higher abundance and frequency of the sensitive salmonids (e.g. intolerant to low O2 concentrations). In accordance with our second hypothesis, the OCS had smaller-sized fishes and showed a tendency to host higher fish densities. The relative abundance of the different trophic groups did not, however, differ between the two streams types. The distinct fish assemblages (richness, mean body size, density, relative abundances, and trophic groups) in OCS and RFS streams are likely the result of a series of direct and Fig. 4 Relative abundance of fish species common in RFS (riparian forest) and OCS (open canopy) streams. * marginally significant (p < 0.1) differences between RFS and OCS
indirect mechanisms, many of which are potentially related to macrophyte abundance and composition (summarized in the conceptual model of Fig. 6). High spatial heterogeneity created by macrophytes may enhance refuge and food availability for smaller fishes as seen also in lakes (e.g. Teixeira-de Mello et al. 2009) and reservoirs (e.g. Pelicice et al. 2005). A high density of macrophytes generally lowers water velocity at the reach level (Fig. 6), but at the same time small areas with high velocities may develop in-between beds of macrophytes, increasing habitat diversity. Furthermore, depending on their physical structure the different
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Table 4 Relative abundance and species composition of each trophic group of fishes in streams with contrasting riparian vegetation in Denmark Trophic group
OCS streams
RFS streams
Species
Piscivores
0.3 ± 0.2
0
E. lucius
Invertivores-piscivores
9.6 ± 3.1
7.1 ± 2.9
A. Anguilla, S. salar, P. fluviatilis, O. mykiss
Invertivores
72.8 ± 6.6
79.2 ± 5.9
S. trutta, L. lota, G. aculeatus, P. flexus, C. caracius, C. gobio, T. thymallus, L. leuciscus, P. pungitius, B. barbatula, G. cernus, G. gobio
Omni-invertivores-herbivores
7.0 ± 3.6
9.7 ± 4.1
T. tinca, R. rutilus
Detritivores
10.2 ± 3.5
4.0 ± 1.4
L. fluviatilis
macrophyte species offer different habitat conditions for fish, which may explain the overall higher fish diversity observed in OCS stream type. For example, Callitriche spp., which are abundant in Danish streams, create complex flow patterns with high variability in flow velocity (CV 56.6 %), whereas flow patterns within species with simple growth forms, such as Sparganium sp., are less variable (CV 25.8 %) (Bell et al. 2013). Higher instream production in OCS (Sand-Jensen et al. 1989) may also have contributed to the observed higher fish species diversity as predicted also by the River Continuum Concept (RCC) (Vannote et al. 1980). When naturally heterotrophic forested headwater streams shift to open water reaches, the autotrophic production increases, as shown in several studies performed along longitudinal gradients in streams (Ibañez et al. 2009; Winemiller et al. 2011; Pease et al. 2012). Besides higher instream production, OCS also had a smaller proportion of gravel and a higher proportion of fine sediments than RFS, and they were also deeper. The habitable area was therefore proportionally larger in OCS than in RFS, which may also have contributed to the higher fish diversity. The physical differences found
between the two stream types have also been seen in other studies of Danish streams (Kristensen et al. 2015) and in studies of forested and open canopy small agricultural streams in temperate USA (Julian et al. 2011). The increased stream depth in OCS than in macrophytefree streams with similar discharge might be a consequence of macrophyte-generated higher flow resistance and lower velocity (e.g. Westlake 1975; Dawson and Kern-Hansen 1979; Dawson 1989; Gurnell 1994; SandJensen 1998; Julian et al. 2011). Additionally, management activities such as weed cutting and dredging performed to ensure water runoff from agricultural land may add to increased stream depths in OCS (BaattrupPedersen et al. 2009; Kristensen et al. 2015). The lack of riparian shade promotes higher water temperature (Johnson 2004; Kristensen et al. 2015), which along with the previously mentioned processes (i.e. lower velocity, more organic matter, more macrophytes) can lead to lower oxygen concentrations in OCS, particularly at night (Westlake 1975; SandJensen et al. 1989; Sand-Jensen 1998). This may favor tolerant species such as sticklebacks (Kraak et al. 2000) and disfavor salmonid reproduction (Jones et al. 1999).
Fig. 5 Danish Fish Index for Streams (DFFV). a Left panel = mean and SE of DFFV values; b right panel = the proportion of RFS (riparian forest) and OCS (open canopy) streams relative to ecological quality
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Fig. 6 Conceptual model of the possible relationships between the different abiotic and biotic components driven by the loss of riparian forests in streams (open canopy, OCS, and riparian forest, RFS, streams)
Particularly, S. trutta is a cold-water, low-oxygen intolerant species that is currently strongly affected by increases in temperature in various regions of the globe (Eaton and Scheller 1996; Jonsson and Jonsson 2009; Lassalle and Rochard 2009; Almodóvar et al. 2011) and by reductions in water flow (Jonsson and Jonsson 2009). Traditionally, high taxonomic richness is perceived as a sign of good environmental state, and richness is therefore used in several biological indexes (e.g. the Index of Biological Integrity, IBI, (Karr 1981) and DFFV). Although our results showed very similar DFFV values, three riparian streams could not be classified as less than three species occurred. Our results suggest that modification of riparian habitats may lead to more complex effects besides those affecting richness patterns. Despite the higher α and β diversity of fish assemblages in open canopy streams, a reduction in the abundance of S. trutta (Willson and Halupka 1995; Payton et al. 2002), and a general reduction in mean body size, can lead
to changes in the functioning of ecosystems (e.g. Brett and Glass 1973; Schlosser 1987; Arim et al. 2007). Such changes may affect the structure and composition of other aquatic communities due to the different trophic roles and often top position of S. trutta in temperate stream food webs (Flecker and Townsend 1994; Huryn 1998; Biggs et al. 2000; Townsend 2003; Greig and McIntosh 2006). Moreover, S. trutta is a species with high recreational angling and commercial value and efforts of conservation and management in Europe are often directed at ensuring its presence (Piccolo 2011). Establishment of forested riparian buffer zones has been suggested as a mitigation measure to filter nutrients and pesticides (Kronvang et al. 2005; Weissteiner et al. 2014) and to trap sediment from agricultural runoff (Liu et al. 2008), as well as to counteract climate changedriven increases in water temperature and the consequent detrimental effects on stream biota (Kristensen et al. 2011; Kristensen et al. 2015). Our results suggest that buffer zones may also contribute to the
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maintainance of species, such as S. trutta, which are otherwise expected to lose suitable habitats due to warming and land cover changes (Filipe et al. 2013). Our work also suggests that different restoration targets (i.e. increasing fish richness versus increasing keystone species (i.e. salmonids) or nutrient input reduction) may require different kinds of management of riparian vegetation. Acknowledgments FTM, MM, and IGB received support from the Sistema Nacional de Investigación (Agencia Nacional de Investigación e Innovación, ANII, Uruguay). FTM was supported by Sistema Nacional de Becas-ANII and CSIC (Uruguay) and SOAS (Denmark) and MM by ANII FCE-2009-2749 and L’ Oréal-UNESCO for Women in Science. EJ was supported by the Research Council for Nature and Universe (272-08-0406), the STF project CRES, CIRCE and FNU (16–7745), and ABP, EK and EJ by EU REFRESH (contract no. 244121) and EU MARS (contract no. 603378). We are grateful to T. Andersen and M. Masdeu for the data on fish diet, Ane Kjeldgaard for the map of the study area, and Anne Mette Poulsen for manuscript editing.
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