High capacity for a dietary specialist consumer population to cope with increasing cyanobacterial blooms

Abstract

We present a common-garden experiment to examine the amphipod Monoporeia affinis, a key deposit-feeder in the Baltic Sea, a low diversity system offering a good model for studying local adaptations. In the northern part of this system, the seasonal development of phytoplankton is characterized by a single diatom bloom (high nutritional quality), whereas in the south, the diatom bloom is followed by a cyanobacteria bloom (low nutritional quality) during summer. Therefore, the nutrient input to the benthic system differs between the sea basins. Accordingly, the amphipod populations were expected to be dietary specialists in the north and generalists in the south. We tested this hypothesis using a combination of stable isotope tracers, trophic niche analyses, and various endpoints of growth and health status. We found that when mixed with diatomes, the toxin-producing cyanobacteria, were efficiently incorporated and used for growth by both populations. However, contrary to expectations, the feeding plasticity was more pronounced in the northern population, indicating genetically-based divergence and suggesting that these animals can develop ecological adaptations to the climate-induced northward cyanobacteria expansion in this system. These findings improve our understanding regarding possible adaptations of the deposit-feeders to increasing cyanobacteria under global warming world in both limnic and marine ecosystems. It is possible that the observed effects apply to other consumers facing altered food quality due to environmental changes.

Figure 1

Satellite view of the Baltic Sea on July 25, 2019 (NOAA: Satellite SuomiNPP; data processed by SMHI), showing cyanobacterial blooms covering a great part of the Baltic Proper. White dots represent collection sites for Monoporeia affinis used in the common-garden experiment in the Baltic Proper (BP: stn. Grund utsjö) and northern Bothnian Sea (BoS: stn. N21). The experimental sediment, diatoms, and cyanobacteria were collected close to the BP station (see text for differences in characteristics among sediments).

Figure 2

Summary of the experimental design and statistical approaches to test the effect of different diet regimes (LD low diatom, HD high diatom, LDHC low diatom high cyanobacteria, HDLC high diatom low cyanobacteria, S sediment only) on amphipods from the BP and BoS basins. The phytoplankton material added per microcosm in the experimental treatments and expressed as dry mass (mg dwt) of the diatoms and cyanobacteria for high and low levels of each food type. See details on statistical tests in the text.

Figure 3

Stable isotope bi-plot of δ¹⁵N and δ¹³C values in the different components of the experimental system. Left panel: the food sources in the experimental microcosms (squares), including sediment (brown), diatoms (dark green), and cyanobacteria (turquoise), and the test animals (shaded field). Right panel: a zoom-in of the shaded field from the left panel showing the signatures of the amphipods originated from the BP (triangles) and BoS (circles) populations. The colour coding: Initials (black) and the treatments: Control (grey), HD (green), HDLC (blue), LD (olive green), LDHC (turquoise). The data are shown as group means with SE as error bars.

Figure 4

Body condition parameters (Growth and C:N ratio) and Acetylcholinesterase (AChE) activity for amphipods from each population and diet treatment. The diets include supplementation of the control sediment (S) with Low and High Diatom (LD, HD), and a combination of diatoms with low and high cyanobacteria (LDHC, HDLC). Colour represents each treatment: Control (grey), HD (green), HDLC (blue), LD (olive green), LDHC (turquoise). Values are mean ± SE for body conditions parameters and geometric mean [95% CI] for AChE activity. See Table 2 for statistical comparisons and Table S3, Supplementary Information: with absolute differences for the treatments under comparison.

Figure 5

Density box-plot of Bayesian estimates of Standard Ellipse Area (SEAb) for each treatment and population with initial and control amphipods to the left of the dotted vertical line. Black dots indicate the SEAb with 50, 75 and 95% credible intervals produced from 10⁵ Bayesian iterations of SEA (SEAb).