Toxicity and Risk of Plant-Produced Alkaloids to Daphnia magna.

Abstract

Background Many plants contain phytotoxic alkaloids to deter herbivorous pests and grazing animals. Alkaloids include quinolizidine and indole alkaloids found in the lupin (Lupinus spp.), an ornamental flower and emerging protein crop, as well as pyrrolizidine alkaloids in the ragwort (Senecio jacobaea), an invasive, weed-like flower. When lupins and ragworts are present in large densities in fields, there is a concern that alkaloids may leach into freshwater environments in amounts that may affect non-target organisms, such as Daphnia magna. This study aimed to investigate i) the acute toxicity of alkaloids (gramine, heliotrine, lupanine, lupinine, monocrotaline, monocrotaline N-oxide, senecionine and sparteine) in D. magna, ii) the contribution of these individual alkaloids to lupin plant extract toxicity, iii) the longer term reproductive effects of a representative alkaloid, sparteine, and finalise with iv) a tentative risk assessment for the sum of alkaloids measured in soil and surface waters. Results The alkaloids exhibited toxicity, with 48 h EC50 values in the range of 5.6 to >100 mg/L. The 48 h EC50 of the Lupinus angustifolius plant extract was 1.38 mg/L, which was far more toxic than the simulated extract where lethality was <10% at 10 mg/L after 48 h. Hence, non-measured compounds may have contributed to the joint toxicity. Daphnid mothers exposed to >2.5 mg/L sparteine produced significantly fewer and smaller offspring during the 21-day exposure, making chronic effects occur at concentrations approximately 10-fold lower than the 48 h EC50 for sparteine. The risk assessment of cumulated alkaloids measured in drain, running and pond waters showed a potential risk, particularly for stagnant pond water, where concentrations were severalfold higher than in the drain and running waters. Conclusions The results highlight that natural toxins may contribute to poor chemical quality of natural waters, and that natural toxins from upcoming crops or invasive weeds should be considered aquatic in risk assessments.

The Beauty is a beast: Does leachate from the invasive terrestrial plant Impatiens glandulifera affect aquatic food webs?

“…This is supported by the results of our mesocosm study, where we could show that after precipitation the population density of A. obliquus and D. magna were reduced. A recent study showing that during rainfall the concentration of secondary plant metabolites was about ten times higher in surface water of streams further support our findings (Griffiths et al, 2021; Günthardt et al, 2020; Kisielius et al, 2020). Unfortunately, we could not reliably measure the concentration of 2‐MNQ in the mesocosms.…”

“…If donor plants grow in riparian areas, allelochemicals may cross ecosystem boundaries (Jackrel & Wootton, 2015) and leach into the adjacent water bodies, especially during precipitation, which was shown for allelochemicals from bracken (Skrbic et al, 2021). Ecotoxicological studies in the laboratory, performed with the extracted allelochemical juglone and other natural toxins, revealed negative effects of these compounds on water dwelling organisms, such as an increased mortality in zoo‐ and phytoplankton (Griffiths et al, 2021; Westfall et al, 1961; Wright et al, 2007). Based on these findings, invasive terrestrial plants, that form monospecific stands in riparian areas may not only affect terrestrial native plant species they may additionally affect the neighboring aquatic ecosystems.…”

“…Based on these findings, invasive terrestrial plants, that form monospecific stands in riparian areas may not only affect terrestrial native plant species they may additionally affect the neighboring aquatic ecosystems. Griffith et al (2021) could show that plant produced phytotoxic alkaloids, e.g., from the lupin ( Lupinus spp .) or the ragwort ( Senecio jacobaea ), elicit effects on life history and morphological parameters in Daphnia magna .…”

Allelochemical run-off from the invasive terrestrial plant Impatiens glandulifera decreases defensibility in Daphnia

“…When allelochemical producing plants grow in low densities, the amount of allelochemicals leaching into adjacent waters may be negligible. However, it was shown for example that phytotoxins, such as pyrrolizidine alkaloids (PA), produced by Senecio jacobaea or Petasites hybridus, were found in concentrations up to 90 ng/l in small streams and up to 230 ng/l in seepage water from groundwater wells 28,30 . Furthermore, rainfall increased PA concentrations by a factor of ten in stream water, which might be critical for aquatic ecosystems during rainy season 28 .…”

“…1-4-naphthoquionones, to which 2-MNQ belongs, are a class of redox-active molecules that may cause oxidative stress in cells and have been shown to increase the mortality in parasites (Trypanosoma brucei), human cancer cells, or aquatic invertebrates (Eurytemora affinis) [37][38][39] . In sub-lethal concentrations such compounds can affect the fitness of organisms either by reducing growth, reducing fecundity or compromising the immune system 30,40 . It was shown that a similar compound, juglone (5-hydroxy-1,4-naphthoquinone), an allelochemical produced by the black walnut tree, Juglans nigra, can increase the mortality in D. magna, when the animals are treated with finely ground walnut hulls or the purified substance 37,41 .…”