The paradox of diatom-copepod interactions*

Traditionally, diatoms have been associated w ~ t h productive pelagic food chains that lead, through suspensionfeeding planktonic copepods, to top consumers and important fisheries Here, 15 laborator~es located ivorldw~de in 12 d~ffer ent countries and representing a variety of marine, estuarine and freshwater environments present strong evidence that diatom diets are in fact inferior for copepod reproduction When fed to females of 16 copepod species, all but 1 of the 17 diatoms e x a m ~ n e d significantly reduced egg production rates or egg viability compared to non-diatom controls These effects are hypothesized to influence copepod recruitment patterns and the flow of energy in marine food webs. KEY WORDSDiatom-copepod mteractions . Copepod recruitm e n t . Food webs The 'classic' pelagic food web refers to the widely held concept of a trophic linkage between outbursts of diatom-rich phytoplankton, copepod production and fish (Runge 1988, Cushing 1989, Legendre 1990). The spring diatom bloom, for example, is considered to initiate and support the cycle of secondary production and growth of fish larvae that depend predominantly on the egg and naupliar stages of planktonic copepods, the dominant constituents of the zooplankton in most oceanic regions, for food (Turner 1984, Mann 1993). The stratified waters of the oligotrophic or post-bloom temperate ocean, on the other hand, support a flagellate-dominated, microbial production, which has traditionally been considered to be ineffectively transferred to the mesozooplankton and fish (Cushing 1989). It has long been known that many copepod species feed on diatoms in the sea (Lebour 1922, Marshal1 & Orr 1955). However, the importance of diatoms as a dominant and high quality food source for copepod product~on has recently been questioned (Kleppel et al. 1991, Kleppel 1993). For example, new studies have reported that some diatom species induce copepod egg mortality by blocking embryogenesis (Poulet et al. 1995, Ianora et al. 1996, Uye 1996). The implications of these results challenge the traditional view of the role of diatoms in the pelagic food web. Here, we report observations designed to determine 'Authors given in a lphabet~c order. "Addressee for correspondence. E-mail: poulet@sb-roscoff.fr whether the inhibitory effects of diatoms on copepod '"Present address. Faculty of Apphed Bioloqical Science, are indeed a phenomenon. Hiroshima University, ~ i ~ a s h i ~ i r o s h i m a , . Japan Using the same protocols described in detail in Poulet O Inter-Research 1997 Resale o f full article n o t permjt ted Mar Ecol Prog Ser 157: 287-293, 1997 et al. (1995) and Uye (1996), 15 laboratories located worldwide have examined the reproductive response of a number of copepod species to different diatom species, representing a variety of temperate and subarctic freshwater, estuarine, and coastal ocean environments (see Table 1). The reproductive response of copepods to various food treatments was quantified by incubating adult females in containers holding 150 to 1000 ml, 0.45 pm filtered seatvater enriched with diatom or non-diatom (control, usually a dinoflagellate) diets. Algae were cultured in F/2 (diatoms) and K (non-diatoms) media (Guillard & Ryther 1962, Keller et al. 1967) and were given in excess (10' to 10' cells ml-') to copepods. Experiments ran for 4 to 40 d, depending on the copepod species and diets. Each day, copepods were transferred to new containers with fresh media and eggs were counted and left undisturbed for 48 to 72 h to determine hatching success. Details of preparation of phytoplankton extracts are given elsewhere (Poulet et al. 1994, Uye 1996). Tests demonstrating that culture media, bacteria in cultures and anoxia did not affect hatching had already been conducted (Ianora et al. 1996, Uye 1996). Among the 37 diatom-copepod combinations examined, there were 4 categories of responses (Table 1, Fig. 1). Except for 1 combination (Category IV), where there was no negative effect, diatoms supported either lower copepod fecundity (Category 111) or hatching success (Category 11) or both (Category I) , when compared to non-diatom diets (p i 0.01). Thus, while diatoms may provide a source of energy and materials for copepod growth (Vidal 1980), they often reduce fecundity and/or hatching success. These observations constitute the paradox of diatom-copepod interactions in the pelagic food web. How can diatoms support copepod development yet depress their reproductive potential? The results in Table 1 show that diatoms reduced fecundity, on average, by 87 % (Categories I and 111) and hatching success by 80% (Categories I and 11) with time. Non-diatom diets in controls (Table 2) induced negligible changes in both fecundity (+ 16 %) and hatching success (-4 %). Among cultured clones, the same diatom species showed considerable intraspecific differences in their impact (e.g. Skeletonema costatum, Phaeodactylum tncornutum), reflecting species-specific feeding behaviors or variable intracellular composition of the algae. For example, S. costatum reduced fecundity and hatching in Acartia clausi, fecundity but not hatching in Calanus helgolandicus, and neither of the two in C. finmarchicus. Chaudron et al. (1996) have shown that a decrease in egg viability was significantly correlated to diatom cell concentrations in diets. In the present study, hatching success was affected at even lower diatom concentrations of 102 cells ml-' (Fig. 2). In temperate waters, cell Control l