Persistent and delayed effects of toxic cyanobacteria exposure on life history traits of a common zooplankter

Abstract

Anthropogenic eutrophication has resulted in shifts in phytoplankton community composition worldwide which represent dramatic changes in resource quality and availability for grazers such as rotifers. For these grazers, harmful algal blooms may have consequences that persist across several generations. We hypothesized that rotifers exposed to a pulse of the toxigenic cyanobacterium Microcystis aeruginosa, would suffer demographic and physiological effects that decreased their ability to recover after cyanobacteria exposure. Additionally, we hypothesized that rotifer population recovery after harmful algal blooms is modulated by delayed effects of pre-bloom food availability. We used laboratory experiments to test the effects of switching from a high quality diet to toxigenic cyanobacteria on the physiological condition and associated life history changes of the common rotifer Brachionus calyciflorus. We found that M. aeruginosa exposure decreased fecundity of rotifers by 51.5%, and early exposure to high levels of the high-quality food Chlamydomonas sp. did not ameliorate this negative effect. Rotifers exposed to Microcystis produced lower quality offspring (by 16.6%). However, we found that the effect of Microcystis on offspring body size was dependent on the density of food available in early life. Exposure to high-density food for the first 3 d of life tempered the negative effects of Microcystis exposure, whereas initial exposure to low-density food resulted in a 9.0% decrease in offspring length. We found that the negative effects of exposure to toxigenic cyanobacteria may accumulate across generations and limit the ability of rotifer populations to withstand the predicted increasing frequency and duration of harmful algal blooms.

Maternal effects are no match for stressful conditions: a test of the maternal match hypothesis in a common zooplankter

“…Optimal egg size theory makes the prediction that under lower resource availability ( Microcystis ) the produced eggs and offspring will be larger than under high resource availability ( Chlamydomonas ). We found support for this in earlier work (Beyer & Hambright ). As a subset of anticipatory parental effects, the maternal match hypothesis makes the further prediction that offspring produced by Microcystis ‐reared mothers will be more fit than those produced by Chlamydomonas ‐reared mothers when raised with Microcystis .…”

“…In considering the relationship between offspring size and fitness, our results, that larger offspring had lower fitness, are counterintuitive when considered within the traditional framework of the OEST. Although we did not directly measure offspring size in this experiment, we have done so under similar experimental conditions, and found that diet has a strong effect on offspring size (Beyer & Hambright ). That these offspring were less fit, even though they have presumably larger energy reserves for somatic maintenance and reproduction, warrants speculation.…”

“…In an earlier experiment, we found that mothers exposed to poor food quality produced fewer and larger offspring, contingent upon early exposure to high amounts of high‐quality food, thus supporting the OEST. Based on the maternal match hypothesis, we predicted that if larger offspring were produced under poor food quality (as shown in Beyer & Hambright ), they would have higher fitness if they were raised in the same food quality, assuming predictability of offspring environment by maternal experiences. Our evidence leads us to reject the maternal match hypothesis under these conditions and provides further support that toxigenic algal blooms may have more extensive effects on grazer populations through transmissive maternal effects than can be evaluated using traditional experimental methods, which use only single generations of rotifers, because the effects of exposure to toxigenic algae propagate and intensify across generations.…”

“…Under our conditions, high population growth rates of B. calyciflorus are obtained on a diet of Chlamydomonas but not Microcystis . Additionally, this strain of Microcystis produces microcystins under our culture conditions (see Beyer & Hambright for further details).…”

“…As resource availability declines, and thus offspring survival risk increases, the per capita investment by mothers should increase, leading to larger offspring, which comes at a cost of a decline in the number of offspring produced (Krist 2010). This theory has been tested in a broad variety of organisms, and support has been found in diverse taxa including collared flycatchers Ficedula albicollis (Krist & Munclinger 2015); Atlantic salmon Salmo salar (Rollinson & Hutchings 2013) and invertebrates like the crustacean zooplankter Daphnia pulex (Li & Jiang 2014) and the rotifer Brachionus calyciflorus (Beyer & Hambright 2016). However, support for the OEST is not universal (e.g.…”