Hemoglobin concentration in Daphnia (D. galeata–hyalina) from the epilimnion is related to the state of nutrition and the degree of protein homeostasis

Abstract

The function of hemoglobin (Hb), which is a key protein of many species, was analyzed in Daphnia from the field. Temperature and oxygen content; abundance and composition of phytoplankton; and abundance, body, and clutch sizes of the Daphnia assemblage were measured in the epilimnion and around the thermocline of a reservoir for 2 yr. In addition, carbohydrate, lactate, and hemoglobin concentrations were determined in whole Daphnia. In Daphnia from the thermocline, hypoxia-induced Hb expression was responsible for an increase in Hb concentration in parallel with a decrease in oxygen content. In Daphnia from oxygen-rich water (epilimnion), however, Hb concentration unexpectedly showed a negative relationship to temperature and to the animals' temperature-dependent metabolic rate. Furthermore, the seasonal minima of Hb concentration coincided with low food (phytoplankton) availability and maxima of Daphnia's reproductive activity. These data suggest that Hb serves a dual function as respiratory protein and protein store. Laboratory experiments supported this hypothesis: starvation caused the concentration of Hb and other hemolymph proteins to decrease during normoxia, whereas the hemolymph protein store remained stable during hypoxia. Hemolymph proteins obviously function as a buffer between food (protein) availability and protein demand, with the latter increasing with temperature mainly because of elevated growth and reproduction rates. Accordingly, the size of the hemolymph protein store can indicate the state of nutrition of Daphnia (and possibly other species) from oxygen-rich water, which can easily be assessed by spectroscopic measurement of Hb in whole animals.

Oxygen- and capacity-limited thermal tolerance: bridging ecology and physiology

“…These limits lie at the edge of or outside the range of aerobic power budget (Zakhartsev et al, 2003;Pörtner and Knust, 2007;Chen et al, 2015), beyond critical limits (T c , where there is a transition to anaerobic metabolism; Box 1) and close to the co-evolving denaturation temperature (T d ) (see Farrell, 2009, and below). Such testing raises concerns, as it bypasses the sublethal thresholds at the core of OCLTT, such as pejus temperature (T p , the onset of capacity limitation and hypoxaemia) and T c , and their ecological relevance ( primarily of T p ), which has been demonstrated in field studies Perry et al, 2005;Breau et al, 2011;Eliason et al, 2011Eliason et al, , 2013Deutsch et al, 2015;Dahlke et al, 2016;Jakob et al, 2016;Pörtner and Knust, 2007;Pörtner et al, 2008;Storch et al, 2011;Schwerin et al, 2010;Takasuka et al, 2007).…”

Seasonal and interannual changes in water temperature affect the genetic structure of a Daphnia assemblage (D. longispina complex) through genotype‐specific thermal tolerances

“…The dominance of G6.1 around the oxygen-depleted thermocline was in accordance with a high capacity for hemoglobin expression in the corresponding CL (Pinkhaus et al 2007). An absence of diurnal vertical migration has been previously ascertained for the D. longispina species complex of Saidenbach Reservoir (Schwerin et al 2010). …”

“…A 1-yr study on the D. longispina complex from Saidenbach Reservoir (Pinkhaus et al 2007) provided evidence for connections between the genetic spatiotemporal heterogeneity of the Daphnia assemblage and seasonal changes in water temperature. A 2-yr study on the same species complex (Schwerin et al 2010) focused on hemoglobin function in Daphnia from the field. A 3-yr study on this same complex analyzed relationships between seasonal and interannual changes in abundance of Daphnia species and hybrids and temperature conditions in winter, focusing on the yearspecific seasonal success of different winter strategies (overwintering, resting eggs).…”

Benthic–pelagic coupling in lake ecosystems: the key role of chironomid pupae as prey of pelagic fish

“…The mean annual concentration of total phosphorus is approximately 13.4 lg/L (Horn and Horn 2008). The reservoir is well oxygenated from the winter through the end of August (Schwerin et al 2010). The sediment thickness decreases from the bottom of the channel-shaped reservoir (37 cm) to the littoral zone (,10 cm) (Ulrich 1997).…”

“…The littoral zones are represented by near shore habitats of two bays with water depths above the compensation depth of 8-10 m. The compensation depth is defined as the depth at which the light level falls below a threshold of 1% of surface values. The profundal zone corresponds to the habitat below the compensation depth and thermocline (water depths between 10 and 45 m) in the deeper parts of the bays and the central basin (Schwerin et al 2010). The vertical penetration of photosynthetic active radiation (PAR ¼ 400-700 nm) was measured weekly in situ using a LI-Cor Li-189 spherical quantum sensor.…”