MARINE ECOLOGY PROGRESS SERIES Vol. 67: 235-249, 1990 Published November 1 Mar. Ecol. Prog. Ser. Predation by copepods upon natural populations of Phaeocystis pouchetii as a function of the physiological state of the prey Kenneth W. step', Jens Ch. ~ejstgaard~,Hein Rune Skjoldall, Francisco ~eyl ' Institute of Marine Research, Postbox 1870, Nordnes, N-5024 Bergen, Norway University of Bergen, Department of Marine Biology, N-5065 Blomsterdalen, Norway ABSTRACT Confl~chngdata have been previously presented on the ablllty of copepods to prey upon the prymneslophyte Phaeocystls pouchetu Whde some have suggested that gelatinous colonies of thls species contan blochemlcal substances that prevent the~rconsumption others have shown that both slngle cells and colon~esof P pouchetu can serve as an excellent food source The present study presents data from feedlng expenments uslng 4 specles of copepods and natural samples of phytoplank- ton prey from a south-north transect dunng May 1989 in the Barents Sea Natural phytoplankton contalned P pouchefn colonies m assoclatlon wth varylng amounts of diatoms Along the transect these colonies vaned from h~ghlyfluorescent and healthy In the north to weakly fluorescent In the south Results of expenments uslng both image analysis and radiotracer techniques indicate that diatoms were actlvely preyed upon In all expenments wth long-chain-formlng species as the preferred food Predahon upon P pouchefn colon~eswas dependent upon the physiological condition of the colonies Healthy colonies were not consumed, while suscephble colon~eswere consumed at rates 2 to 10 tlmes those for chain-forrmng dlatoms The selective predalon descnbed here has important impl~cationsfor specles composition in Archc waters INTRODUCTION Smayda (1989) have reported a lack of P. pouchetii ingestion by Acartia spp., they attributed this Is Phaeocystis pouchetii (Hariot) grazed by herbivor- phenomenon to the size of the colonies, rather than to ous zooplankton? P. pouchetii blooms have been chemical undesirability. reported to have harmful effects on migration of fish Phaeocystis pouchetii is a member of the Prym- populations (Savage 1930) and on fish catches (Brad- nesiophyceae, a group known for the production of stock & MacKenzie 1981, Chang 1984). Sieburth (1958, toxic or harmful compounds (Shilo 1967, Carmichael 1960, 1965) documented the sterility of penguin guts in 1986, Estep & MacIntyre 1989a). P. pouchetii alternates populations feeding upon euphausiids in Antarctic P. between a gelatinous colony with a large number of pouchetii blooms. Sterility imparted to the guts of these nonmotile, embedded cells, and a motile swarmer animals was demonstrated to be a function of acrylic stage with 2 flagella and a haptonema (Chang 1984).A acid produced by P. pouchetu colonies (Sieburth 1961). non-motile benthic stage may also be present (Kayser An inhibitory effect of P. pouchetii colonies upon zoo- 1970). It is an important species in Antarctic and Arctic plankton predation has also been suggested (Martens ecosystems, as well as in some temperate and boreal 1980, 1981, Daro 1985, Schnack et al. 1985, Claustre et waters (Burkholder & Sieburth 1961, Lancelot et al. al. 1990). However, the inhibitory effect of P. pouchetii 1987). In the Barents Sea the colonial form of this has recently been called into question by field and species typically dominates the spring bloom, along laboratory experiments showing active predation by with diatoms. The relative abundance of diatoms and P. copepods upon colonies and single cells of P. pouchetii pouchetii appears to vary depending upon the stock of (Eilertsen et al. 1989, Tande & BAmstedt 1987). Huntley zooplankton, possibly as a result of discrimination et al. (1987) comment that 'It is difficult to say exactly against P. pouchetii by copepods, allowing this alga to how the legend of Phaeocystis unpalatability to zoo- dominate in the presence of large zooplankton stocks plankton began' [our emphasis]. Although Verity & (Skjoldal & Rey 1989). O Inter-ResearcWPrinted m Germany 236 Mar. Ecol. Prog. Ser 67: 235-249, 1990 The production of toxic chemical compounds by stations for predation experiments (Fig. 1). Stns 1 and 2 prymnesiophytes (e.g. Prymnesium and Chryso- were located in Atlantic water in the western Barents chrornulina) is highly dependent on the physiological Sea. Stn 3 was located in the polar front region west of state of the organism (Shilo 1967),and possibly on the Bear Island. Stns 4 and 5 were located in the Hopen presence or absence of particular CO-occurringspecies Depth in Atlantic water east of Bear Island and in in the population (Estep & MacIntyre 1989a).If there is meltwater closer to the ice edge, respectively. Stns 1 to any truth to the unpalatability of Phaeocystis pouchetii, 5 correspond to RV 'G.O.Sars' Stns 578, 586, 595, 604 we would expect the same relationship with physiolog- and 612, respectively. ical condition to be important. We therefore set out to Stations were selected on the basis of the physiologi- examine copepod predation upon P, pouchetii colonies cal condition of Phaeocystis pouchetii colonies. Phy- in different physiological states to determine if feeding siological condition was determined by the fluores- behaviour was variable or constant. The present paper cence of individual cells within the colonies. Phyto- examines 5 stations where P. pouchetii occurred in plankton lose their autofluorescence when in poor con- different physiological conditions and with variable dition; reductions of 30 % immediately upon death and amounts of CO-occurringdiatoms. Using a combination 75 % 24 h after death have been reported (Tsuji & of image analysis and radiotracer experiments, we Yanagita 1981). Healthy P. pouchetii populations nor- demonstrate that, while predation upon diatoms was mally form lobed colonies with individual cells showing constant for all stations, predation upon P. pouchetii medium-bright, red-orange autofluorescence, while was a function of the physiological state of the colonies. cells from unhealthy colonies lose fluorescence and individual colonies become depleted of cells, the latter due either to cell death or to transformation to the MATERIALS AND METHODS motile stage (Verity et al. 1988). Copepods for predation experiments were collected Sampling and experimental setup. Sample collec- with 50, 100 or 150 m-to-surface vertical net hauls, tion, experimental work and data recording were con- using a WP2 net (mesh size 200 pm, l m opening ducted between 13 and 22 May 1989, during a cruise in diameter) fitted with a PVC plastic bag in a 14 1, nonfil- the Barents Sea onboard the RV 'G.O. Sars'. We chose 5 tering, black cod-end. Temperature differences from bottom to top of the net hauls were always less than 2°C. To mlnimize disturbance to the animals as a result of collection and handling, the net was retrieved at 0.2 m S-'. Upon arrival at the surface, the plastic bag containing the sample was immediately removed from the cod-end without rinsing. This treatment avoided inclusion of animals attached to the net that may have been damaged during the haul. Actively swimming and feeding copepods, as defined by ~Mackas& Burns (1986), were gently siphoned from the sample, and replicate, monospecific groups of 3 to 25 adult females 7 5 and Stage CV copepodites were immediately pipetted into beakers with 40 m1 of 0.47 ym Nuclepore-filtered 74 seawater at in situ temperatures. Individuals were pipetted under a Wild M5A dissecting microscope 73 using dim light to minimize disturbance of the animals. Natural populations of phytoplankton prey were col- 72 lected from the same sites at a depth of 20 m, approxi- 7 I mately equal to the weak chlorophyll maximum, using 30 1 Nislun bottles. Contaminating zooplankton were 7 0 removed from the samples, and the natural, unconcen- 69 trated algal assemblages were used as prey for the copepods. In Expts 1, 2, 4 and 5, algae were inoculated 6 8 I Is 1g 23 27 31 39 oF with copepods within 1 h. In Expt 3, the algal sample (collected at Stn 3a; Fig. 1) was incubated on deck for Fig l. Sarnpllng statlons where natural populations of algae 6 d to induce senescence, by depleting residual n~trate and zooalankton were obtained for z red at ion exoeriments. In Expt 3, 'algae were collected from Stn 3a but incubated with the zooplankton taken at Stn 3 Microscopic image analysis experiments. Predation Estep et. al.: Predation on Phaeocystis pouchetj~ 237 Table 1. Number and size of copepods contained in experimental flasks for image-analysis experiments Expt No. of flasks Species No. of ind. Mean cephlothorax length (mm) I 3 Calanus finmarchicus" 23 2.75 I 1 Calanus finmarchlcus Calanus hyperboreus Metridia longa 3 Calanus finmal-ch~cus 13-15 3 Calanus hyperboreus 5 3 Calanus finmarchicus 17-19 3 Calanus finmarchicus 16-2 1 2 Calanus h yperboreus 4-5 1 Calanus glacialis 14 a All individuals were CV1 female, with the exception of M. longa, which was mixture of CV/CVI female experiments were conducted in 800 m1 polyethylene stained filters and stained with 75 pg n~l-' Primulin (in tissue-culture flasks, each with in situ concentrations of 0.1 M Trizma HC1, pH to 4.0) for 30 min. Stained filters phytoplankton and, except in the controls, 3 to 25 were examined with UV (BP 365, FT 395, LP 397) and individuals from a single copepod species (Table 1). blue light (450 to 490, FT 510, LP 520) using a Zeiss The size of the culture flask was chosen as a conl- Axioplan epifluorescence microscope (Car1 Zeiss, F.R. promise to reduce edge effects (Mullin 1963, Tackx & Germany). When examined with the UV filter, the Polk 1986, O'Brien 1988) while retaining a sufficient staining procedure used here imparts a blue colour to copepod concentration to give measurable predation. protistan protoplasm and a dull-fluorescent-brown col- Experiments were begun immediately after sufficient our to the mucus matrix surrounding Phaeocystis copepods had been sorted (less than 1.5 h after sample pouchetii colonies.