Algal Toxins Alter Copepod Feeding Behavior

Abstract

Using digital holographic cinematography, we quantify and compare the feeding behavior of free-swimming copepods, Acartia tonsa, on nutritional prey (Storeatula major) to that occurring during exposure to toxic and non-toxic strains of Karenia brevis and Karlodinium veneficum. These two harmful algal species produce polyketide toxins with different modes of action and potency. We distinguish between two different beating modes of the copepod’s feeding appendages–a “sampling beating” that has short durations (<100 ms) and involves little fluid entrainment and a longer duration “grazing beating” that persists up to 1200 ms and generates feeding currents. The durations of both beating modes have log-normal distributions. Without prey, A. tonsa only samples the environment at low frequency. Upon introduction of non-toxic food, it increases its sampling time moderately and the grazing period substantially. On mono algal diets for either of the toxic dinoflagellates, sampling time fraction is high but the grazing is very limited. A. tonsa demonstrates aversion to both toxic algal species. In mixtures of S. major and the neurotoxin producing K. brevis, sampling and grazing diminish rapidly, presumably due to neurological effects of consuming brevetoxins while trying to feed on S. major. In contrast, on mixtures of cytotoxin producing K. veneficum, both behavioral modes persist, indicating that intake of karlotoxins does not immediately inhibit the copepod’s grazing behavior. These findings add critical insight into how these algal toxins may influence the copepod’s feeding behavior, and suggest how some harmful algal species may alter top-down control exerted by grazers like copepods.

Osmotic stress does not trigger brevetoxin production in the dinoflagellateKarenia brevis

“…However, there is increasing evidence that brevetoxins promote the survival of K. brevis by deterring grazing by zooplankton (12)(13)(14). Studies investigating the functional role of toxins in organisms have a long history, and one that is deep-seated in terrestrial systems, including numerous terrestrial plants (e.g., 16,32,33).…”

“…Competition experiments reveal that K. brevis produces allelopathic compounds, which inhibit the growth of competing phytoplankton and thereby help enable this slowgrowing species to dominate; however, brevetoxins themselves do not appear to be responsible for this inhibition (10,11). Recent studies support the hypothesis that brevetoxins serve as grazing deterrents, which promote population survival by decreasing grazing mortality rates (12)(13)(14), consistent with a classic defensive role for this neurotoxin. Furthermore, very recently published experiments show that limitation of growth rate by nitrogen and phosphorus increases cellular brevetoxin concentrations by two-to threefold, consistent with the behavior of other grazing defense toxins in terrestrial plants and phytoplankton (15)(16)(17)(18).…”

Distinctly different behavioral responses of a copepod, Temora longicornis , to different strains of toxic dinoflagellates, Alexandrium spp.

“…Most previous studies of the response of copepods to toxic algae are incubation studies, in which the net outcome of the copepod-prey interaction is quantified in terms of feeding rate, prey selection, growth or egg production rate, or other similar bulk measures (reviewed by Turner, 2014). The direct video observation of individual responses and of direct copepod-prey cell interactions provided by this and a few other studies (Bruno et al, 2012;Hong et al, 2012;Tiselius et al, 2013) Selander et al, 2006;Teegarden, 1999). The fact that the copepods can distinguish between cells of very similar size and shape suggests that selection is mediated by chemical information.…”

“…In the presence of toxic Karenia spp. cells it also (within 10 min) reduces appendage beat activity to only sample the environment, and resumes more active feeding if the prey environment becomes favorable (Hong et al, 2012).…”

“…A further complicating factor is that different strains and natural populations of the same algal species may vary in their toxicity and with its growth conditions (Burkholder and Glibert, 2006;Cembella, 1998). With a few exceptions (e.g., Hong et al, 2012), only macroscopic responses (e.g. mortality and feeding rate) rather than behavioral responses are examined, and in most cases it is not possible to establish a mechanistic relationship between the algal toxin profile and its effects on the copepod grazer.…”