Taxon-specific variation in δ13C and δ15N of subfossil invertebrate remains: Insights into historical trophodynamics in lake food-webs

Abstract

Keywords: stable isotopes, invertebrate subfossils, sedimentary organic matter, energy and nutrient pathways, boreal lakes Declarations of interest: none 3 4 5 6 7 2 Abstract 8 Carbon and nitrogen stable isotope ratios of sub-fossil invertebrate remains are 9 potentially powerful indicators of nutrient flux, habitat-specific resource utilization, and trophic 10 interactions in lentic food webs, but are rarely estimated for multiple species within lakes. Here 11 we examined historical time series of δ 13 C and δ 15 N in remains of individual invertebrate taxa 12 representing pelagic, littoral and benthic habitats during the 20 th century in five boreal lakes of 13 central Canada. We applied a novel statistical approach based on Generalized Additive Models 14 (GAMs) to quantify the differences in centennial means and trends (i) between invertebrate 15 remains and sedimentary organic matter (SOM), and (ii) among different taxa within each lake to 16 evaluate the coherence of isotope signals during the 20 th century. Differences in mean δ 13 C and 17 δ 15 N were usually significant (p < 0.05) between SOM and invertebrate taxa, and among 18 individual taxa, reflecting selective feeding by invertebrates and differences in trophic position 19 within food webs. In contrast, patterns of historical variance in isotope values varied among 20 lakes with few consistent differences between long-term isotopic trends of SOM and invertebrate 21 remains. In particular, SOM and invertebrate isotopic trends were similar in relatively 22 dystrophic lakes, likely due to the importance of terrestrial carbon in both SOM and invertebrate 23 diets. However, significant SOM-invertebrate trend differences were observed for both δ 13 C and 24 δ 15 N in relatively clear-water lakes, possibly reflecting temporal variation in diets or tissue 25 fractionation. Comparison of historical trends in isotope values among taxa revealed few 26 consistent patterns, likely indicating uncoupled carbon and nitrogen fluxes through invertebrate 27consumers with different habitat specializations or feeding modes. Together, our findings 28 suggest that evaluation of taxon-specific δ 13 C and δ 15 N can provide valuable insights into 29 historical tropho-dynamics in lake food webs. 30

Deforestation caused abrupt shift in Great Lakes nitrogen cycle

“…However, because any impact on the δ 15 N of aquatic nitrogen pools at the base of a food web (i.e., in various pools of dissolved inorganic nitrogen [DIN]) is passed up the trophic ladder to producers (phytoplankton) and their consumers (invertebrates and fish), isotopic analyses of tissues from aquatic producers and consumers can also serve as a highly integrative indicator for anthropogenic impacts on nutrient dynamics, in addition to food web structure, in aquatic environments (Hoffman et al 2012;Morrissey et al 2013). While a majority of isotopic research has approached the question of changing freshwater nutrient dynamics through analyses of sedimentary organic matter (e.g., Talbot 2001;Dubois et al 2018), a growing number of studies are demonstrating that δ 15 N compositions of invertebrates and fish can provide a highly sensitive record for environmental change (e.g., Perga et al 2010;Lumb and Johnson 2012;Fera et al 2017;Anas et al 2019).…”

“…For conservation and restoration efforts in freshwater ecosystems where cultural eutrophication caused by increased nutrient loading poses one of the most significant threats globally (Smith and Schindler 2009), long-term retrospectives that document when and how human activities first began to alter natural ecosystem processes, and the nitrogen cycle in particular, could provide a valuable framework for evaluating which modern human activities pose the greatest risks (Humphries and Winemiller 2009;Canfield et al 2010). Paleolimnological proxy indicators based on the physical, biological, chemical, and isotopic compositions of sediments have long been used to establish trends in past aquatic productivity and water quality (Beeton 1965;Schelske et al 1983;Jeffers et al 2015), but, because of potential taphonomic issues (Anderson 2014;Lu et al 2014) and because these approaches usually do not incorporate consumers, they are unable to measure the direct impacts of anthropogenic nitrogen loading on nutrient dynamics in the wider biotic community (e.g., invertebrates, fish, birds; although for a growing literature on invertebrate analyses, see Perga 2010;Perga et al 2010;van Hardenbroek et al 2010;Frossard et al 2014;Schilder et al 2017;Anas et al 2019). Moreover, while many studies using isotopic analyses of museum-archived vertebrate tissues have been able to make important contributions to understanding how biotic communities have responded to human-caused environmental change during the 20 th century (Fera et al 2017), a lack of suitable specimens from early historical and preindustrial time periods has, in most cases, prevented analyses of longer-term environmental variation in vertebrate taxa (Szpak et al 2018).…”

“…This is important because, in contrast to analyses of bulk sedimentary organic matter, which is composed of a spatially, temporally, and biologically heterogeneous mixture of sources of detritus (Lu et al ), with fish bone or scales, the ability to compare “taxonomically anchored” isotopic patterns across different parts of a food web will enable much higher‐resolution interpretations of environmental change at both the level of nutrient dynamics and the level of broader food web structures. Moreover, with respect to measuring the isotopic compositions of ancient organic materials, the ability to purify collagen extracted from bone (through pretreatment steps outlined below) and assess the extent to which its constituent carbon and nitrogen are biogenic (e.g., using well‐established and precise C : N Atomic criteria; DeNiro ; Szpak ) provides an additional advantage relative to other important paleontological materials (e.g., chitinous remains from subfossil invertebrates; Anas et al ) and makes bone and scale collagen particularly well suited for intersite comparisons of isotopic variation in biota across time and space. Furthermore, because collagen from bones and scales is constructed and remodeled slowly throughout the life of an organism, the isotopic composition of collagen can provide a lifetime average record of dietary intake and environmental conditions that is less susceptible to seasonal or short‐term idiosyncratic shifts in behavior (Hobson and Clark ).…”

Water chemistry, landscape, and spatial controls of δ13C and δ15N of zooplankton taxa in boreal lakes: One size does not fit all

“…Given the likely differences in energy and nutrient fluxes through zooplankton taxa with varying dietary niches (Anas et al, 2019;Barnett, Finlay, & Beisner, 2007;Matthews & Mazumder, 2003), we hypothesised that lake/catchment-specific (CHEM + HYDR_LAND) controls of SI composition vary among zooplankton taxa with different dietary niches. Because our previous work (Anas et al, 2014;Scott, Wissel, Gibson, & Birks, 2010) indicated a limited importance of spatial factors in influencing several water chemistry variables (i.e.…”

“…Analyses of their dietary contributions to predators such as fish are often based on SI analyses of carbon and nitrogen (Cabana & Rasmussen, 1994;Persaud & Dillon, 2010;Vander Zanden & Rasmussen, 1999). As mentioned above, among-lake variability in δ 13 C and δ 15 N of these secondary producers can be related to a range of factors associated with energy and nutrient fluxes in lakes, whereas these relations may vary among taxa with different feeding modes and/or habitat specialisations given the likely variations in energy and nutrient pathways through different food-web compartments (Anas et al, 2019;Matthews & Mazumder, 2003;Persaud et al, 2009). For instance, factors controlling primary production can be strongly correlated to δ 13 C variation of selective feeders of phytoplankton relative to non-selective feeders, whereas zooplankton.…”