Respirometry reveals major lineage-based differences in the energetics of osmoregulation in aquatic invertebrates

Abstract

All freshwater organisms are challenged to control their internal balance of water and ions in strongly hypotonic environments. We compared the influence of external salinity on the oxygen consumption rates (ṀO2) of three species of freshwater insects, one snail and two crustaceans. Consistent with available literature, we found a clear decrease in ṀO2 with increasing salinity in the snail Elimia sp. and crustaceans Hyalella azteca and Gammarus pulex (r5=-0.90, P=0.03). However, we show here for the first time that metabolic rate was unchanged by salinity in the aquatic insects, whereas ion transport rates were positively correlated with higher salinities. In contrast, when we examined the ionic influx rates in the freshwater snail and crustaceans, we found that Ca uptake rates were highest under the most dilute conditions, while Na uptake rates increased with salinity. In G. pulex exposed to a serially diluted ion matrix, Ca uptake rates were positively associated with ṀO2 (r5=-0.93, P=0.02). This positive association between Ca uptake rate and ṀO2 was also observed when conductivity was held constant but Ca concentration was manipulated (1.7-17.3 mg Ca l-1) (r5=0.94, P=0.05). This finding potentially implicates the cost of calcium uptake as a driver of increased metabolic rate under dilute conditions in organisms with calcified exoskeletons and suggests major phyletic differences in osmoregulatory physiology. Freshwater insects may be energetically challenged by higher salinities, while lower salinities may be more challenging for other freshwater taxa.

Keywords: Aquatic insects; Aquatic invertebrates; Calcium; Ion transport; Metabolic rate; Salinity.

Fig. 1.

Dendrogram showing the taxonomic structure of the species used in these experiments. The dendrogram was generated using phyloT software; class, order, family and wet mass are shown for each species.

Fig. 2.

The influence of salinity on oxygen consumption rate (Ṁ_O2) of aquatic invertebrates. Lineage-specific patterns emerge, with crustaceans (A,B) and a snail (C) showing increased oxygen consumption with decreasing salinity, and mayflies (D,E) and a caddisfly (F) showing no change [n=16 for artificial soft water (ASW); n=8 for other treatments].

Fig. 3.

Effect of salinity on sodium uptake rates. Sodium uptake rates were positively associated with salinity and sodium concentration in Gammarus pulex, Hyalella azteca and Elimia sp. when exposed to a serial dilution. Data are means±s.e.m. (n=8).

Fig. 4.

Effect of salinity and Ṁ_O2 on calcium uptake rates. (A) Calcium uptake rates were negatively associated with salinity and calcium concentration in G. pulex when exposed to a serial dilution. (B) Calcium uptake rates were positively associated with oxygen consumption rates in G. pulex. The same pattern was observed in H. azteca. Data are means±s.e.m. (n=8).

Fig. 5.

Effect of calcium concentration and Ṁ_O2 on calcium uptake rates. Calcium uptake rates were positively associated with (A) calcium concentration and (B) Ṁ_O2 in G. pulex when conductivity was held constant but calcium was varied from 1.7 to 17.3 mg l⁻¹. Data are means±s.e.m. (n=8).

Fig. 6.

Three models of energetics and fluxes in aquatic organisms. (A) Metabolic rate is higher in dilute conditions and is associated with the increased need to offset diffusive losses (e.g. snails). (B) Metabolic rate increases with salinity to meet the increasing energetic demands of ion transport (e.g. observed primarily in some marine/euryhaline species). (C) Metabolic rate does not change with salinity (e.g. aquatic insects).