FEMS Microbiology Ecology, 91, 2015, fiv041 doi: 10.1093/femsec/fiv041 Advance Access Publication Date: 6 April 2015 Research Article
RESEARCH ARTICLE
Iron supply constrains producer communities in stream ecosystems Chad A. Larson1 , Hongsheng Liu and Sophia I. Passy∗ ∗ Corresponding author: Department of Biology, University of Texas at Arlington, Arlington, TX 76019, USA. Tel:+817-272-2415;
E-mail: [email protected] Present address: Department of Ecology State of Washington, Olympia, Washington. One sentence summary: This is the first continental and experimental investigation to demonstrate that iron limitation is potentially widespread in US streams and can have negative impacts on producer biodiversity and biomass accumulation. Editor: Riks Laanbroek
1
ABSTRACT The current paradigm that stream producers are under exclusive macronutrient control was recently challenged by continental studies, demonstrating that iron supply constrained diatom biodiversity and energy flows. Using algal abundance and water chemistry data from the National Water-Quality Assessment Program, we determined for the first time community thresholds along iron gradients in non-acidic running waters, i.e. 30–79.5 μg L−1 and 70–120 μg L−1 in oligotrophic and eutrophic streams, respectively. Given that Fe concentrations fell below both thresholds in 50% of US streams, and below the eutrophic threshold in 75% of US streams, we suggest that Fe limitation is potentially widespread and attribute it to the restricted distribution of wetlands. We also report results from the first laboratory experiments on algal-iron interactions in streams, revealing that iron supplementation leads to significant biovolume and biodiversity increase in both nitrogen fixing and non-nitrogen fixing algae. Therefore, the progressive brownification of freshwaters due to rising dissolved organic carbon and iron levels can have a stimulating influence on microbial producers with cascading effects along the trophic hierarchy. Future research in running waters should focus on the role of iron in algal physiology and biofilm functions, including accumulation of biomass, fixing atmospheric nitrogen and improving water quality. Keywords: algae; biodiversity; biomass accumulation; brownification; eutrophication; iron; nitrogen fixers; nutrient colimitation; streams
INTRODUCTION The ‘iron age in oceanography’ began in the late 1980s with the discovery that iron limited the growth of oceanic phytoplankton, which has since been confirmed in 40% of the world’s ocean (de Baar et al. 2005). Numerous investigations over the following decades concluded that Fe limitation had a strong impact on oceanic algal carbon uptake, composition and productivity (Martin and Fitzwater 1988; Coale et al. 1996; Boyd et al. 2000). The paradigm in freshwater research, on the other hand, is that photosynthetic communities are products of exclusive macronutrient control (Borchardt 1996; Elser et al. 2007; Sterner 2008).
Recent continental studies have challenged this paradigm by showing that iron supply constrains the energy flows in diatom communities (Passy 2012), as well as their biodiversity at scales ranging from individual stream reaches to entire watersheds (Passy 2008; Passy 2009; Passy 2010). However, unlike the ocean, experimental research on the algal-iron relationships in streams is lacking, despite evidence of a significant increase in periphyton biomass in response to micronutrient addition (Pringle et al. 1986). Although iron is one of the most abundant elements on Earth, it is often limiting to producers across aquatic ecosystems, including the open ocean (Martin and Fitzwater 1988;
Received: 3 February 2015; Accepted: 1 April 2015 C FEMS 2015. All rights reserved. For permissions, please e-mail: [email protected]
1
Downloaded from http://femsec.oxfordjournals.org/ by guest on November 14, 2015
Department of Biology, University of Texas at Arlington, Arlington, TX 76019, USA
2
FEMS Microbiology Ecology, 2015, Vol. 91, No. 5
Fe only. However, maximum producer richness and biomass would be observed when all resources were replete, including N, P and Fe, consistent with the benthic model of coexistence, which predicts that adding nutrients at high supply increases the niche dimensionality of the algal habitat and produces thick and speciose biofilms (Passy 2008). Given the substantial energy and Fe requirements of N2 fixation, we also expected that high levels of both P and Fe were necessary for establishing a diverse and abundant diazotroph community under N-limiting conditions.
MATERIALS AND METHODS The NAWQA Program data Proportional area of all major land cover types in 2946 US watersheds and total dissolved iron in 2437 distinct stream localities were measured by the USGS as part of the NAWQA Program (http://water.usgs.gov/nawqa). Both land cover and iron data were available for 1670 streams. Algal communities were examined in a subset of 392 stream localities, spanning 37.42 latitudinal and 78.55 longitudinal degrees. Of these localities, 162 were classified as oligotrophic (nitrate ≤ 245 μg L−1 and phosphate ≤ 22 μg L−1 ) and 230, as eutrophic (NO3 − > 245 μg L−1 and PO4 3− > 22 μg L−1 ), following Hill and Fanta (2008) and Passy (2008). The 392 streams were sampled one to six times between 1993 and 2006 and 600 quantitative algal samples were collected from the richest-targeted habitats. These habitats harbor the most diverse periphytic assemblages within the reach, including epilithon, epiphyton and epidendron. Algal collection, processing and enumeration followed established protocols (http://pubs.usgs.gov/of/2002/ofr-02-150/). Streams sampled for algae also had data for the month of algal collection on total Fe, NO3 − -N and PO4 3− -P (all water filtered), generated by the NAWQA Program according to Fishman and Friedman (1989). If multiple measurements of the studied nutrients were taken during this month, they were averaged.
Experimental data Microcosm study In February–March 2011 and September–October 2011, we performed two nutrient manipulation experiments in a facility with 24 stream microcosms (see Fig. S1, Supporting Information). These experiments were conducted in different seasons to test the generality of the observed patterns. The microcosms are round glass dishes, measuring 30.5 cm in diameter × 10.2 cm in height and holding 4.5 L of water. In each microcosm, an 8.9 cm propeller mounted on an IKA RW-20 Digital Overhead StirR rer (IKA Works, Inc., Wilmington, North Carolina, USA) was placed just above the substrate in the center of the dish and set at 600 rpm, creating a constant current velocity of 8 cm R sec−1 . The stainless steel propellers were coated with Plasti Dip R Primer, then multiple times with Plasti Dip , after which they were placed in water for 2 weeks. Chemical analysis of this water as well as in control treatments (without Fe) found no traces of Fe. The microcosms were illuminated by 250 W metal halide lamps for 14 h daily at levels sufficient for photosynthesis, i.e. ∼200 μmol m−2 sec−1 (Hill and Fanta 2008). We sampled streams with broad nutrient ranges, i.e. 8.4– 260 μg L−1 NO3 − ,
RESEARCH ARTICLE
Iron supply constrains producer communities in stream ecosystems Chad A. Larson1 , Hongsheng Liu and Sophia I. Passy∗ ∗ Corresponding author: Department of Biology, University of Texas at Arlington, Arlington, TX 76019, USA. Tel:+817-272-2415;
E-mail: [email protected] Present address: Department of Ecology State of Washington, Olympia, Washington. One sentence summary: This is the first continental and experimental investigation to demonstrate that iron limitation is potentially widespread in US streams and can have negative impacts on producer biodiversity and biomass accumulation. Editor: Riks Laanbroek
1
ABSTRACT The current paradigm that stream producers are under exclusive macronutrient control was recently challenged by continental studies, demonstrating that iron supply constrained diatom biodiversity and energy flows. Using algal abundance and water chemistry data from the National Water-Quality Assessment Program, we determined for the first time community thresholds along iron gradients in non-acidic running waters, i.e. 30–79.5 μg L−1 and 70–120 μg L−1 in oligotrophic and eutrophic streams, respectively. Given that Fe concentrations fell below both thresholds in 50% of US streams, and below the eutrophic threshold in 75% of US streams, we suggest that Fe limitation is potentially widespread and attribute it to the restricted distribution of wetlands. We also report results from the first laboratory experiments on algal-iron interactions in streams, revealing that iron supplementation leads to significant biovolume and biodiversity increase in both nitrogen fixing and non-nitrogen fixing algae. Therefore, the progressive brownification of freshwaters due to rising dissolved organic carbon and iron levels can have a stimulating influence on microbial producers with cascading effects along the trophic hierarchy. Future research in running waters should focus on the role of iron in algal physiology and biofilm functions, including accumulation of biomass, fixing atmospheric nitrogen and improving water quality. Keywords: algae; biodiversity; biomass accumulation; brownification; eutrophication; iron; nitrogen fixers; nutrient colimitation; streams
INTRODUCTION The ‘iron age in oceanography’ began in the late 1980s with the discovery that iron limited the growth of oceanic phytoplankton, which has since been confirmed in 40% of the world’s ocean (de Baar et al. 2005). Numerous investigations over the following decades concluded that Fe limitation had a strong impact on oceanic algal carbon uptake, composition and productivity (Martin and Fitzwater 1988; Coale et al. 1996; Boyd et al. 2000). The paradigm in freshwater research, on the other hand, is that photosynthetic communities are products of exclusive macronutrient control (Borchardt 1996; Elser et al. 2007; Sterner 2008).
Recent continental studies have challenged this paradigm by showing that iron supply constrains the energy flows in diatom communities (Passy 2012), as well as their biodiversity at scales ranging from individual stream reaches to entire watersheds (Passy 2008; Passy 2009; Passy 2010). However, unlike the ocean, experimental research on the algal-iron relationships in streams is lacking, despite evidence of a significant increase in periphyton biomass in response to micronutrient addition (Pringle et al. 1986). Although iron is one of the most abundant elements on Earth, it is often limiting to producers across aquatic ecosystems, including the open ocean (Martin and Fitzwater 1988;
Received: 3 February 2015; Accepted: 1 April 2015 C FEMS 2015. All rights reserved. For permissions, please e-mail: [email protected]
1
Downloaded from http://femsec.oxfordjournals.org/ by guest on November 14, 2015
Department of Biology, University of Texas at Arlington, Arlington, TX 76019, USA
2
FEMS Microbiology Ecology, 2015, Vol. 91, No. 5
Fe only. However, maximum producer richness and biomass would be observed when all resources were replete, including N, P and Fe, consistent with the benthic model of coexistence, which predicts that adding nutrients at high supply increases the niche dimensionality of the algal habitat and produces thick and speciose biofilms (Passy 2008). Given the substantial energy and Fe requirements of N2 fixation, we also expected that high levels of both P and Fe were necessary for establishing a diverse and abundant diazotroph community under N-limiting conditions.
MATERIALS AND METHODS The NAWQA Program data Proportional area of all major land cover types in 2946 US watersheds and total dissolved iron in 2437 distinct stream localities were measured by the USGS as part of the NAWQA Program (http://water.usgs.gov/nawqa). Both land cover and iron data were available for 1670 streams. Algal communities were examined in a subset of 392 stream localities, spanning 37.42 latitudinal and 78.55 longitudinal degrees. Of these localities, 162 were classified as oligotrophic (nitrate ≤ 245 μg L−1 and phosphate ≤ 22 μg L−1 ) and 230, as eutrophic (NO3 − > 245 μg L−1 and PO4 3− > 22 μg L−1 ), following Hill and Fanta (2008) and Passy (2008). The 392 streams were sampled one to six times between 1993 and 2006 and 600 quantitative algal samples were collected from the richest-targeted habitats. These habitats harbor the most diverse periphytic assemblages within the reach, including epilithon, epiphyton and epidendron. Algal collection, processing and enumeration followed established protocols (http://pubs.usgs.gov/of/2002/ofr-02-150/). Streams sampled for algae also had data for the month of algal collection on total Fe, NO3 − -N and PO4 3− -P (all water filtered), generated by the NAWQA Program according to Fishman and Friedman (1989). If multiple measurements of the studied nutrients were taken during this month, they were averaged.
Experimental data Microcosm study In February–March 2011 and September–October 2011, we performed two nutrient manipulation experiments in a facility with 24 stream microcosms (see Fig. S1, Supporting Information). These experiments were conducted in different seasons to test the generality of the observed patterns. The microcosms are round glass dishes, measuring 30.5 cm in diameter × 10.2 cm in height and holding 4.5 L of water. In each microcosm, an 8.9 cm propeller mounted on an IKA RW-20 Digital Overhead StirR rer (IKA Works, Inc., Wilmington, North Carolina, USA) was placed just above the substrate in the center of the dish and set at 600 rpm, creating a constant current velocity of 8 cm R sec−1 . The stainless steel propellers were coated with Plasti Dip R Primer, then multiple times with Plasti Dip , after which they were placed in water for 2 weeks. Chemical analysis of this water as well as in control treatments (without Fe) found no traces of Fe. The microcosms were illuminated by 250 W metal halide lamps for 14 h daily at levels sufficient for photosynthesis, i.e. ∼200 μmol m−2 sec−1 (Hill and Fanta 2008). We sampled streams with broad nutrient ranges, i.e. 8.4– 260 μg L−1 NO3 − ,
