Variable littoral-pelagic coupling as a food-web response to seasonal changes in pelagic primary production

Abstract

1. Lakes are among the most seasonally forced ecosystems on Earth. Seasonal variation in temperature and light produce cyclic patterns in water column mixing, nutrient supply and phytoplankton biomass. Diet responses of consumers to these patterns have rarely been quantified. Moreover, pelagic‐littoral coupling of dietary resources by mobile consumers is commonly considered to be static over annual cycles. 2. This study quantifies littoral‐pelagic diet responses of multiple consumers to a strong shift in pelagic phytoplankton abundance over an annual cycle (September 2014 to August 2015) in a large (area 614 km2), oligotrophic, monomictic lake (Lake Taupō, New Zealand). Intra‐annual patterns in pelagic phytoplankton (chlorophyll a) and zooplankton were determined over multiple years. Major resource and consumer δ13C and δ15N were then collected over an annual cycle. Temporal patterns in food‐web structure were examined using convex hulls as a proxy of community trophic niche size. Diet was quantified using mixing models for zooplankton, meso‐predatory zooplanktivorous common smelt (Retropinna retropinna) and benthivorous common bullies (Gobiomorphus cotidianus), as well as the top‐predator rainbow trout (Oncorhynchus mykiss). Trophic structure patterns for smelt, bullies and trout were then independently examined using compound‐specific amino acid δ15N analyses (CSIA‐AA). 3. Lake Taupō demonstrated similar food‐web patterns to other lakes globally. Phytoplankton and zooplankton demonstrated strong seasonal oscillations of abundance driven by both bottom‐up (nutrient supply) and top‐down (stable limit cycle) drivers. The food web demonstrated the typical nested structure. It responded to seasonally low and high pelagic resource availability periods by expansion and contraction, respectively, of trophic niche space. In response to lower pelagic phytoplankton abundance during summer stratification, and phytoplankton accumulation at a deep chlorophyll maximum (DCM), zooplankton abundance reduced and their diet became dominated by phytoplankton from below the thermocline (i.e. the hypolimnion and DCM). This change may have been prompted by the combined drivers of avoidance of predation and depauperate food supply in surface waters. 4. The diet of smelt and bullies switched from predominantly zooplankton to benthic macroinvertebrates, synchronous with the decline in pelagic zooplankton. Trout diet, inferred from comparison of isotopic signatures of tissues with different turnover rates, also increased littoral resource reliance over the stratified period. Smelt, bully and trout CSIA‐AA data confirmed estimates of trophic position and indicated a greater degree of trophic complexity in the littoral than the pelagic food chain. 5. Food webs in large, deep lakes such as Taupō are expected to be primarily pelagic. This study demonstrates the need to re‐examine this expectation due to seasonal variations in productivity. The relatively small littoral areas in large lakes, combined with meso‐predators’ highly seasonally variable littoral resource use, may drive strong seasonal top‐down effects on littoral macroinvertebrate prey. Our study supports the notion that food‐web interactions are highly dynamic and responsive to seasonal forcing. By linking food‐web dynamics to dynamic environmental conditions, this study provides a framework for future studies research on understanding lake food‐web responses to a range of annual/seasonal and global environmental change drivers.