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Strain-Related Physiological and Behavioral Effects of Skeletonema Marinoi on Three Common Planktonic Copepods

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Strain-Related Physiological and Behavioral Effects of Skeletonema Marinoi on Three Common Planktonic Copepods Strain-related physiological and behavioral effects of Skeletonema marinoi on three common planktonic copepods The Harvard community has made this article openly available. Please share how this access benefits you. Your story matters Citation Md Amin, Roswati, Marja Koski, Ulf Båmstedt, and Charles Vidoudez. 2011. “Strain-related physiological and behavioral effects of Skeletonema marinoi on three common planktonic copepods.” Marine Biology 158 (1): 1965-1980. doi:10.1007/s00227-011-1706-7. http://dx.doi.org/10.1007/s00227-011-1706-7. Published Version doi:10.1007/s00227-011-1706-7 Citable link http://nrs.harvard.edu/urn-3:HUL.InstRepos:11879558 Terms of Use This article was downloaded from Harvard University’s DASH repository, and is made available under the terms and conditions applicable to Other Posted Material, as set forth at http:// nrs.harvard.edu/urn-3:HUL.InstRepos:dash.current.terms-of- use#LAA Mar Biol (2011) 158:1965–1980 DOI 10.1007/s00227-011-1706-7 ORIGINAL PAPER Strain-related physiological and behavioral effects of Skeletonema marinoi on three common planktonic copepods Roswati Md Amin • Marja Koski • Ulf Ba˚mstedt • Charles Vidoudez Received: 9 February 2011 / Accepted: 16 April 2011 / Published online: 6 May 2011 Ó The Author(s) 2011. This article is published with open access at Springerlink.com Abstract Three strains of the chain-forming diatom positive effect on either egg production (A. tonsa)or Skeletonema marinoi, differing in their production of hatching success (P. elongatus), while other measured polyunsaturated aldehydes (PUA) and nutritional food compounds (PUA, other long-chain polyunsaturated fatty components, were used in experiments on feeding, egg acids) of the algae had no obvious effects. Our results production, hatching success, pellet production, and demonstrate that differences between strains of a given behavior of three common planktonic copepods: Acartia diatom species can generate effects on copepod physiol- tonsa, Pseudocalanus elongatus, and Temora longicornis. ogy, which are as large as those induced by different algae The three different diatom strains (9B, 1G, and 7J) induced species or groups. This emphasizes the need to identify the widely different effects on Acartia tonsa physiology, and specific characteristics of local diatoms together with the the 9B strain induced different effects for the three cope- interacting effects of different mineral, biochemical, and pods. In contrast, different strains induced no or small toxic compounds and their potential implications on alterations in the distribution, swimming behavior, and different copepod species. turning frequency of the copepods. 22:6(n-3) fatty acid (DHA) and sterol content of the diet typically showed a Introduction Communicated by X. Irigoien. Negative effects of harmful phytoplankton on grazers, R. Md Amin (&) Á U. Ba˚mstedt ranging from feeding inhibition and physiological inca- Umea˚ Marine Sciences Centre, Umea˚ University, pacitation to reduction in egg production and egg hatching Norrbyn, 91020 Ho¨rnefors, Sweden rates, are common (see Turner et al. 2001 and references e-mail: [email protected]; therein). Traditionally, diatoms have been considered as a [email protected] basis for a short and effective food chain leading to a high R. Md Amin Á U. Ba˚mstedt fish production (Steele 1974); a view which is confirmed in Department of Ecology and Environmental Sciences, a number of more recent field studies (Irigoien et al. 2002 Umea˚ University, 90187 Umea˚, Sweden and references therein). During the last 15 years, however, R. Md Amin this view has been challenged by studies showing reduced Department of Marine Science, Faculty of Maritime Studies copepod hatching success and/or egg production on dia- and Marine Science, Universiti Malaysia Terengganu, tom-dominated diets (e.g., Miralto et al. 1999; Dutz et al. 21030 Kuala, Terengganu, Malaysia 2008). Several mechanisms have been suggested to cause M. Koski these negative effects. Firstly, inhibitory chemical com- National Institute of Aquatic Resources, Technical University pounds, identified as polyunsaturated aldehydes (PUA), of Denmark, Kavalerga˚rden 6, 2920 Charlettenlund, Denmark have been shown to block embryogenesis in copepods and sea urchins and have antiproliferative and apoptotic effects C. Vidoudez Departement of organismic and evolutionary biology, Harvard on human carcinoma cells (Miralto et al. 1999). These University, 16 Divinity Ave, Cambridge, MA 02138, USA compounds have been detected in many diatoms (Miralto 123 1966 Mar Biol (2011) 158:1965–1980 et al. 1999; Wichard et al. 2007), including several strains locate the high resource patch (Buskey 1984; Tiselius and of the Skeletonema marinoi (recently separated from Jonsson 1990; Tiselius 1992). Some copepod species are Skeletonema costatum, Sarno et al. 2005), which is a believed to decrease their swimming speed or jump fre- common spring bloom diatom in the Baltic Sea, particu- quency when encountering a patch of high food concen- larly in eutrophic areas (Ask et al. 2006). Secondly, tration (Acarti tonsa, Tiselius 1992; Temora longicornis, nutritional inadequacy of diatoms, such as fatty acid or and Pseudocalanus elongatus, Tiselius and Jonsson 1990) sterol, have also been observed to induce low production suggesting that they may be using some type of ‘‘area- rate and hatching success of copepod eggs (Jo´nasdo´ttir restricted search’’ behavior (Leising 2002). Studies on 1994;Jo´nasdo´ttir et al. 2009). Recent findings have added behavioral adaptation of zooplankton aggregation and possible explanations for the negative effects of diatoms, swimming when the food patches consist of a potentially such as a rapid depletion of polyunsaturated fatty acids toxic or harmful algae are rare. However, by analyzing the (especially eicosapentaenois acid EPA) caused by the PUA behavioral response of copepods to a high concentration of production upon mechanical wounding (Wichard et al. toxic Karenia brevis, Cohen et al. (2007) showed that 2007), a compound inducing oxidative stress (Fontana Temora turbinata actively avoided dense patches of this et al. 2007a, b), and a low assimilation efficiency of species. Pierson et al. (2005) found a similar pattern with essential compound with a shorter residence time in Calanus pacificus females, which strongly avoided the copepod guts (Dutz et al. 2008). Still, the exact mecha- layer with a high diatom concentration, which was nisms remain unknown with numerous inconsistencies in suggested to result in a high reproductive success. the results from different investigations. Motivation of this study was to investigate the strain- Typically, the effect of diatoms on the feeding or and species-specific effect of S. marinoi on copepod reproduction of copepods can vary greatly among species physiology and behavior, in relation to both nutritional and is situation specific, due to differences in the species quality and toxicity of the algae. Specifically, we investi- and genetic composition of the bloom (see Turner and gated the strain-specific effect of S. marinoi on feeding, Tester 1989; Rynearson et al. 2006) or differences in egg production, and hatching of three common planktonic nutritional requirements of the copepod (Hasset 2004). calanoid copepods, A. tonsa, P. elongatus, and T. longi- Variation in inhibitory effects of diatoms does also occur at cornis. We analyzed copepod behavior in order to see the intraspecific strain level (Ask et al. 2006; Koski et al. whether copepods alter their distribution and swimming 2008; Dutz et al. 2008). For instance, different strains of behavior as a response to different biochemical properties Thalassiosira rotula have been observed to have both and PUA content of the alga. Our results bring new detailed positive and negative effects on copepods development information on copepod–diatom interactions in the level of (Koski et al. 2008) and different strains of Skeletonema species and strains, as well as provide one of the few costatum induced variable hatching success of Eurytemora existing data sets where both algae nutritional and toxic affinis (Ask et al. 2006). Further, S. marinoi in culture has compounds, as well as copepods ingestion of these, are also been observed to release pronounced bursts of PUAs measured. (heptadienal and octadienal) that are strongly dependent on the growth phase (Vidoudez and Pohnert 2008). Recently, Taylor et al. (2009) isolated nine different strains of Materials and methods S. marinoi in the Gullmar Fjord, Skagerrak and reported large differences in the PUA production between seasons. Algae and copepods The clones isolated showed different physiological responses and degree of genetic heterogeneity indicating We used three copepod species and three Skeletonema that different populations succeed each other in the fjord marinoi strains, as well as Rhodomonas sp., which served (Saravanan and Godhe 2010). These observations indicate as a good quality control food. All algae were offered to the that there can be differences in the toxic and biochemical copepods as a single food source, at a concentration of ca. properties of diatoms depending on strains, genetic vari- 200 lgCl-1. All three copepod species, Acartia tonsa, ability, growth stage of the algae, and season. Temora longicornis, and Pseudocalanus elongatus, were In nature, phytoplankton cells are patchily distributed tested with a chain forming S. marinoi strain GF04-9B (9B; (Daro 1988) over a distance of a few centimeters to meters
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