Stable Isotopes As Tracers in Aquatic Ecosystems

Stable Isotopes As Tracers in Aquatic Ecosystems

Environmental Reviews Stable isotopes as tracers in aquatic ecosystems Journal: Environmental Reviews Manuscript ID er-2017-0040.R3 Manuscript Type: Review Date Submitted by the Author: 03-Oct-2017 Complete List of Authors: Sánchez-Carrillo, Salvador; Museo Nacional de Ciencias Naturales Álvarez-Cobelas, Miguel; Museo Nacional de Ciencias Naturales Stable isotopes, Tracer addition experiments, ecosystem-scale, Food-web, Keyword: BiogeochemistryDraft https://mc06.manuscriptcentral.com/er-pubs Page 1 of 51 Environmental Reviews 1 Running head: Stable isotopes as tracers in aquatic ecosystems 2 3 Stable isotopes as tracers in aquatic ecosystems 4 5 Salvador Sánchez-Carrillo* and Miguel Álvarez-Cobelas 6 7 1Dep. Biogeochemistry and Microbial Ecol., National Museum of Natural Sciences, 8 Spanish National Research Council (MNCN-CSIC), Serrano 115 dpdo, E-28006- 9 Madrid, Spain 10 11 12 13 14 Draft 15 16 17 18 19 -------------------------------------- 20 *Author for correspondence: 21 [email protected] 22 FAX: +34-915640800 23 1 https://mc06.manuscriptcentral.com/er-pubs Environmental Reviews Page 2 of 51 24 Abstract . The addition of stable isotopes (SI) of 13 C and 15 N has been used to 25 study several aquatic processes, thus avoiding environmental disturbance by the 26 observer. This approach, employed for the last three decades, has contributed to 27 expanding our knowledge of food-web ecology and nutrient dynamics in aquatic 28 systems. Currently, SI addition is considered a powerful complementary tool for 29 studying several ecological and biogeochemical processes at the whole aquatic 30 ecosystem scale, which could not be addressed otherwise. However, their contributions 31 have not been considered jointly nor been evaluated with a view to assessing the 32 reliability and scope of their results from an ecosystem perspective. We intend to bridge 33 this gap by providing a comprehensive review (78 scientific publications reporting in 34 situ 13 C/ 15 N additions at the whole-aquatic-ecosystem scale) addressing the main results 35 arising from their use as tracers. Specifically,Draft we focus on: i) reasons for SI additions at 36 the whole-ecosystem scale to study ecological processes; ii) the paradigms resulting 37 from its use and the insights achieved; iii) uncertainties and drawbacks arising from 38 these SI addition experiments, and iv) the potential of this approach for tackling new 39 paradigms. 40 SI tracer addition at the ecosystem scale has provided new functional insights into 41 numerous ecological processes in aquatic sciences (importance of subsidies in lakes, 42 heterotrophy dominance in benthic food-webs in lakes, wetlands and estuaries; the 43 decrease in N removal efficiency in most aquatic ecosystems due to anthropogenic 44 alteration; the recognition of hyporheic zones and floodplains as hot spots for stream 45 denitrification, and high rates of internal N recycling in tidal freshwater marshes). 46 However, certain constraints such as the high cost of isotopes, the maintenance of the 47 new isotopic steady state and avoidance of biomass changes in any compartment or pool 48 during tracer addition, bear witness to the difficulties of applying this approach to all 2 https://mc06.manuscriptcentral.com/er-pubs Page 3 of 51 Environmental Reviews 49 fields of aquatic ecology and ecosystems. The future development of this approach, 50 rather than expanding to larger and complex aquatic ecosystems, should include other 18 51 stable isotopes, such as phosphorus (P O4). 52 53 Keywords: 13 C, 15 N, tracer addition experiments, food webs, biogeochemistry. 54 55 Draft 3 https://mc06.manuscriptcentral.com/er-pubs Environmental Reviews Page 4 of 51 56 Introduction 57 In aquatic science, the ecosystem scale approach is the ideal framework for the study of 58 all ecological interactions among biotic and abiotic components and their processes 59 within defined boundaries (Likens 1992). The main benefit of the whole-ecosystem 60 scale approach is that it encompasses cross-habitat interactions ( e.g. littoral–pelagic), 61 which are critical for trophic interactions (Jeppesen et al. 1998). Another benefit of this 62 approach is that nominal physical conditions are maintained (e.g. light, thermal 63 structure, mixing) which affect growth, nutrient cycling and succession (Carpenter et al. 64 2001). Although experimental manipulations of entire ecosystems entail certain 65 constraints (for example, pseudoreplication), carefully designed experiments may be 66 considered one of the most powerfulDraft approaches for studying process-level topics 67 relative to ecosystems (Likens 1992). Several nutrient enrichment experiments (N and P 68 fertilizations) at the ecosystem-level have contributed to increase our knowledge of 69 aquatic ecosystem metabolism and trophic cascade effects, hence enabling 70 recommendation of policies for eutrophication remediation (Falkowski et al. 2000; Elser 71 et al. 2007; Schindler 2012; Rosemond et al. 2015; Gough et al. 2016). However, 72 fertilization increases ecosystem disturbances –modifying process rates and fates and 73 altering food-web structure through several feedbacks–, and this can be good or bad 74 depending on study goals (e.g. in oligotrophic systems when phytoplankton response is 75 the goal and biomass needs to be increased or when studying some biogeochemical 76 processes and rates are altered if the available substance is oversaturated). 77 The addition of stable isotopes (SI) of 13 C and 15 N has been used during the last 78 three decades to study several aquatic processes, thereby avoiding disturbance. The 79 temporal stability of SI and the processes governing isotopic fractionation make them 80 useful as tracers, thus allowing measurement of simultaneous ecological and 4 https://mc06.manuscriptcentral.com/er-pubs Page 5 of 51 Environmental Reviews 81 biogeochemical processes at the whole-ecosystem scale (Peterson and Fry; 1987; 82 Schimel 1993; Fry 2006). Since Hershey et al. (1993) and Kling (1994) published their 83 seminal papers using 13 C and 15 N additions at the whole-ecosystem scale, many other 84 studies have been reported. 85 The whole-ecosystem isotope enrichment approach is a robust way to examine 86 nutrient flows through multiple pools simultaneously while maintaining natural 87 hydrologic and biogeochemical gradients (Tobias et al. 2003). In situ 13 C and 15 N 88 additions at the whole-ecosystem scale have provided valuable results to advance i) the 89 study of carbon uptake, taking the relationships between terrestrial and lake biomes into 90 account (e.g. Cole et al. 2002; Kritzberg et al. 2004; Pace et al. 2004; Carpenter et al. 91 2005; Tailape et al. 2008), ii) the uptake, turnover, and retention processes of nitrogen 92 (e.g. Tank et al. 2000a; Merriam etDraft al. 2002; Hall et al. 2009b; Hadwen and Bunn 2005; 93 Hughes et al. 2000; Gribsholt and Boschker 2005), and iii) the trophic dynamics and 94 food web structure ( e.g. Raikow and Hamilton 2001; Hamilton et al. 2004; Galván et al. 95 2012). Much of our current knowledge of freshwater ecology is grounded on the results 96 provided by whole-ecosystem SI experimental additions. Now the time has come to 97 evaluate the validity and scope of the results of these complex experiments to assess 98 their impact on studies of aquatic ecology. However, the emerging success of SI 99 addition experiments has not yet been viewed as a whole or evaluated in order to assess 100 the reliability and scope of their results. This assessment is fundamental to decide the 101 suitability of SI additions at ecosystem-scale for building in current and future 102 paradigms in aquatic science. Here, we intend to bridge this gap by addressing the main 103 subjects arising from the use of 13 C and 15 N as tracers at the whole aquatic ecosystem 104 scale. Since the field of aquatic science is very broad we have focused on contributions 105 to the knowledge of freshwater ecosystems, considering all those located in the 5 https://mc06.manuscriptcentral.com/er-pubs Environmental Reviews Page 6 of 51 106 continental context, including water bodies located in coastal areas with varying degrees 107 of tidal influence ( i.e. saltmarsh, tidal flats and estuaries). Our approach is ecologically- 108 based to address the structure and functioning of ecosystems and, therefore, we have not 109 addressed the study of groundwater, where studies also use SI as tracers together with 110 their natural contents (e.g. Aravena and Robertson 1998; Smith et al. 2004). 111 Specifically, we will focus on the following questions: 1st ) why have SI additions been 112 used at the whole-ecosystem scale in freshwaters to study ecological processes? 2 nd ) to 113 date, what paradigms have emerged at the experimental ecosystem-scale using 13 C and 114 15 N additions and what insights have been achieved? 3rd ) what uncertainties and 115 deficiencies have arisen from those SI addition experiments that should be considered 116 when interpreting the scope of their results? 4th ) can (or should) this approach continue 117 to be used to tackle new paradigmsDraft in the future? To answer these questions, we have 118 reviewed 78 scientific publications reporting in situ 13 C/ 15 N additions to aquatic 119 continental systems and their contributions have carefully been discussed. 120 121 Si addition experiments in freshwaters: trends, compounds used, 122 ecosystems studied and geographic location 123 Fig. 1 shows the trends in publications reporting whole-ecosystem experiments in 124 aquatic systems using 13 C and 15 N additions from 1990. Most experimental additions 125 were carried out in the 2000-2009 period with an increasing application to lentic 126 systems. Although the use of both 13 C and 15 N additions displays similar trends, 15 N 127 experimental additions are more frequent. This is because 15 N was used as a tracer of 128 nitrogen dynamics in streams in two large-scale experiments (see below). The joint use 129 of both SI is uncommon.

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