Terrestrial organic matter support of lake food webs: Evidence from lake metabolism and stable hydrogen isotopes of consumers

Abstract

We quantified the utilization of terrestrial organic matter (OM) in the food web of a humic lake by analyzing the metabolism and the consumers' stable isotopic (C, H, N) composition in benthic and pelagic habitats. Terrestrial OM inputs (3 g C m 22 d 21 ) to the lake greatly exceeded autochthonous OM production (3 mg C m 22 d 21 ) in the lake. Heterotrophic bacterial growth (19 mg C m 22 d 21 ) and community respiration (115 mg C m 22 d 21 ) were high relative to algal photosynthesis and were predominantly (. 85%) supported by terrestrial OM in both habitats. Consequently, terrestrial OM fueled most (85%) of the total production at the base of the lake's food web (i.e., the sum of primary and bacterial production). Despite the uncertainties of quantitatively estimating resource use based on stable isotopes, terrestrial OM clearly also supported around half the zooplankton (47%), macrozoobenthos (63%), and fish (57%) biomass. These results indicate that, although rates of terrestrial OM inputs were around three orders of magnitude greater than that of autochthonous OM production, the use of the two resources by higher trophic levels was roughly equal. The disproportionally low reliance on terrestrial OM at higher trophic levels, compared with its high rates of input and high support of basic biomass production in the lake, suggests that autochthonous resources could not be completely replaced by terrestrial resources and indicates an upper limit to terrestrial support of lake food webs.

Selective consumption and metabolic allocation of terrestrial and algal carbon determine allochthony in lake bacteria

“…Interestingly, our results suggest a lower limit in bacterial biomass allochthony in the order of~70% even in more productive systems where terrestrial DOC becomes more diluted by algal C (Figure 1). These patterns are coherent with previous studies which noted similar high levels of allochthony of bacterial biomass (79% ± 16) across a wide range in lake productivity or color in Québec on the basis of the isotopic composition of bacterial fatty acids (Berggren et al, 2014), as well as in a lake in northern Sweden (480%) (Karlsson et al, 2012) and Selective carbon consumption and allocation F Guillemette et al in two Wisconsin lakes (Kritzberg et al, 2004), although lower estimates have also been reported in the latter (range of 35-70%). Our results are also consistent with a recent hypothesis, suggesting that the rapid transfer and efficient incorporation of compounds exported from soils and leaf litter, or produced via photochemical degradation, may account for a large share of total bacterial production in boreal streams and lakes (up to 80%) (Berggren et al, 2010a, b).…”

“…Here we used previously published values for these parameters, and also a well-established isotopic model (IsoError; Phillips and Gregg, 2001) to account for their variability, but we cannot discard that some methodological biases, isotopic artifacts or secondary C incorporation pathways such as anaplerotic C fixation may have influenced our estimates of allochthony (See Supplementary Note 1 for a discussion of these issues). It should be emphasized that our estimates of bacterial biomass allochthony fall well within the range recently reported in other regions (Kritzberg et al, 2004;Karlsson et al, 2012;Berggren et al, 2014), and that the patterns in BR of terrestrial C also agree with previous reports, that is, that BR in unproductive lakes is dominated by terrestrial C (Karlsson et al, 2007;Karlsson et al, 2008). In addition, it is unlikely that the link that we found between the patterns of allocation of terrestrial versus algal C in the experimental incubations with ambient lake Chl a and phosphorous concentration (both of which being completely unconnected to the actual isotopic or metabolic mass balance), would emerge from chance or methodological bias, providing further evidence that these patterns in bacterial DOC utilization and allocation across lakes that we describe here are real.…”

“…This approach was shown to yield algal δ 13 C estimates that compare well with other approaches (Karlsson et al, 2007;Marty and Planas, 2008). There is clear evidence that zooplankton biomass may also contain terrestrial C (Cole et al, 2011;Karlsson et al, 2012), and to account for this we further assumed a 16% contribution of terrestrial C to zooplankton biomass, based on the average terrestrial C content reported by Mohamed and Taylor, 2009 for other Canadian temperate lakes (N = 25), and in accordance with the level of allochthony previously observed in several of the lakes sampled in this study (del Giorgio and France, 1996). We further used the range of zooplankton allochthony 9-23% (±1 s.d.)…”

“…The increase in terrestrial C incorporation efficiency into biomass with increasing system productivity implies that even in eutrophic systems, where bacteria overwhelmingly consume algal-derived C, the isotopic signature of bacterial biomass may still be largely terrestrial. There is now irrefutable evidence of widespread allochthony in freshwater zooplankton and fish (Cole et al, 2011;Karlsson et al, 2012;Berggren et al, 2014), but these metazoans have a low capacity to consume and grow on detrital terrestrial C (Brett et al, 2009), so this transfer must necessarily involve an efficient repackaging of terrestrial C in the form of aquatic bacterial biomass (Berggren et al, 2010b) that can then circulate within aquatic food webs. Given the large losses that occur during the transfer of C in food webs, the systematically high terrestrial signature of bacterial biomass may be one of the keys to sustaining the widespread presence of terrestrial C measured in zooplankton even in more productive or nutrient enriched systems (Cole et al, 2002).…”

Periphyton support for littoral secondary production in a highly humic boreal lake

“…The allochthonous contribution generally increases in importance with decreasing light penetration into water (Ask et al 2009, Karlsson et al 2009, Solomon et al 2011), a condition typical of humic lakes. Allochthonous C can support higher trophic levels via a microbial link in pelagic (Jones 1992, Pace et al 2004) and benthic (Premke et al 2010, Karlsson et al 2012) food webs. However, colored allochthonous dissolved organic C (DOC) reduces light availability for phytoplankton and benthic algae, so it also constrains whole-lake primary production and ultimately secondary production (Karlsson et al 2009, Jones et al 2012.…”