Perceiving the algae: How feeding‐current feeding copepods detect their nonmotile prey

Abstract

Feeding‐current feeding copepods detect and capture prey individually, but the mechanism by which nonmotile prey is detected has been unclear. Early reports that copepods detect phytoplankton prey at distances of one body length or more led to the hypothesis that solutes leaking from the prey would be carried to the copepod by the sheared feeding current and arrive prior to the prey, thus allowing the copepod to adjust the feeding current to bring the prey within reach of the feeding appendages. Many subsequent studies have been interpreted assuming this mechanism, which appears currently to be the main accepted view. Here, we review the observations available in the literature and add our own data to show that in most cases the prey, whether phytoplankton cells or inert particles, has to be within a few prey radii from the setae of the feeding appendages to elicit a capture response. We further demonstrate that (1) long‐range chemical detection is incompatible with known algal leakage rates and reasonable assumptions of sensitivity, (2) that near‐field chemical detection is constrained by diffusion across the boundary layer of the sensor and takes longer than observed near‐contact times, and (3) that most reported detection distances are well predicted by models of fluid mechanical signal generation and detection. We conclude that near‐field mechanoreception is the common prey detection mode in pelagic copepods. Prey detection distances are thus governed mainly by the reach of the feeding appendages, in contrast to the strong prey size‐dependency implied by remote chemical prey detection.

Reply to comment: Prey perception in feeding‐current feeding copepods

“…We argue that chemical detection is neither required nor likely for remote detection at such short distances. First, the ∼ 100 μ m detection distance for a 45‐ μ m sized prey cell reported here is in fact similar to that predicted (50–200 μ m) by mechanoreception and the fluid mechanical mechanisms examined by Gonçalves and Kiørboe (). Second, the chemosensory apical pores on the setae of the feeding appendages, as found in copepods (Paffenhofer and Loyd ) and many other crustaceans, are normally considered to have gustatory (taste) rather olfactory (smell) function; i.e., they only mediate chemical signals upon direct contact with the source (Hallberg and Skog ).…”

“…While it is well established that ambush feeders perceive their prey by the fluid mechanical disturbance that the swimming prey generates (Jonsson and Tiselius ; Yen and Strickler ; Svensen and Kiørboe ; Jiang and Paffenhöfer ), the mechanism and distance at which feeding‐current feeding copepods can detect non‐motile prey remains a controversial issue. In a series of recent studies involving six different species as well as several developmental stages we observed that in all cases, prey had to be in the immediate vicinity of the feeding appendage setae in order to elicit a capture response (Bruno et al ; Kjellerup and Kiørboe ; Tiselius et al ; Gonçalves et al ; Gonçalves and Kiørboe ). We also reviewed all available evidence of prey perception and found that, in most cases, cells as well as inert plastic particles were detected within a few prey cell radii from the setae of the feeding appendages (Gonçalves and Kiørboe ).…”

“…Mainly using the copepod Eucalanus pileatus as model species, they provide three main arguments: (1) remote detection is necessary for survival in a dilute environment; (2) remote detection is manifest only at low prey concentrations and can therefore only be observed under such conditions; (3) remote chemical detection is feasible and the main mechanism of remote detection. Below we examine their arguments, however, without repeating the evidence and reasoning in Gonçalves and Kiørboe ().…”

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

“…Schultz and Kiørboe (2009) suggested that copepods possess the ability to remotely discriminate non-toxic and toxic algae before capture. Recently however the ability of copepods to remotely detect phytoplankton based on their chemical characteristics has been questioned (Gonçalves and Kiørboe, 2015), and our observations suggest that prey selection is based on post-capture discrimination and that unwanted cells are rejected following a handling time. Vanderploeg et al (1990) reported a similar observation in a freshwater copepod.…”

Molecular gut content analysis demonstrates that Calanus grazing on Phaeocystis pouchetii and Skeletonema marinoi is sensitive to bloom phase but not prey density

“…Due to their small size, many phytoplankton species with diameters < 5 µm are not typically considered to be important food sources for copepods, which frequently exhibit prey choice based on size (Sommer et al 2000) or swimming behavior (Kiørboe & Visser 1999), and even chemical cues in the case of larger aggregates (Goncalves & Kiørboe 2015). The high-latitude hapto phyte Phaeocystis spp.…”