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Oxyrrhis Marina-Based Models As a Tool to Interpret Protozoan Population Dynamics

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Oxyrrhis Marina-Based Models As a Tool to Interpret Protozoan Population Dynamics JOURNAL OF PLANKTON RESEARCH j VOLUME 33 j NUMBER 4 j PAGES 651–663 j 2011 Oxyrrhis marina-based models as a tool to interpret protozoan population dynamics KEITH DAVIDSON 1*, FOTOON SAYEGH 2 AND DAVID J. S. MONTAGNES 3 1 2 SCOTTISH ASSOCIATION FOR MARINE SCIENCE, SCOTTISH MARINE INSTITUTE, OBAN, ARGYLL PA37 1QA, UK, PO BOX 100569, JEDDAH 21311, KINGDOM 3 OF SAUDI ARABIA AND SCHOOL OF BIOLOGICAL SCIENCES, UNIVERSITY OF LIVERPOOL, BIOSCIENCES BUILDING, CROWN STREET, LIVERPOOL L69 7ZB, UK Downloaded from https://academic.oup.com/plankt/article/33/4/651/1473431 by guest on 28 September 2021 *CORRESPONDING AUTHOR: [email protected] Received May 18, 2010; accepted in principle June 22, 2010; accepted for publication July 29, 2010 Corresponding editor: John Dolan Oxyrrhis marina-based experiments have frequently been used to underpin the construction and, or, parameterization of protozoan mathematical models. Initially, we examine the suitability and limitations of O. marina for this task. Subsequently, we summarize the range of aut- and synecological modelling studies based on O. marina, examining the questions asked and conclusions drawn from these, along with the range of processes and functions employed within the models. Finally, we discuss future modelling directions based on studies of O. marina. KEYWORDS: dinoflagellate; experimental design; Oxyrrhis marina; models INTRODUCTION Oxyrrhis marina, that can act as a model for others and With improved understanding of the pivotal role that the insights that have been obtained from mathematical protozoa play within microbial food webs (Azam et al., models based on its study. 1983; Pomeroy et al., 2007), an increasing body of exper- The heterotrophic flagellate O. marina is an ideal can- imental work has investigated their response to a range didate organism for the experimental study and model- of environmental conditions. Knowledge of the func- ling of the natural and theoretical population dynamics tional relationships that underpin protozoan growth and of protozoan predators. It is easy to find, isolate, main- grazing, in turn, allows us to derive mathematical tain in culture and manipulate in the laboratory and models that represent their behaviour. Such protozoa- has been maintained in culture for over 50 years in a specific modelling studies provide a means of under- number of culture collections (see Montagnes et al., standing predator–prey interactions than could not be 2011a). Oxyrrhis marina is, therefore, often a natural achieved from observation alone. Furthermore, the specific inclusion of protozoa within more general choice as a model organism and is extensively used for population and ecosystem models allows us to assess experimental studies, some of which have been employed their role in the natural environment. Finally, as proto- to develop or parameterize mathematical models. Within zoa exhibit rapid generation times and are easily this paper, we review the literature to: (i) examine the manipulated, they are an excellent tool for population limitation of using O. marina as a model organism; (ii) dynamic studies and model parameter generation in indicate the breadth of responses and functions that are general. Protozoa have, therefore, for a considerable available for its use, and thus facilitates mathematical time, been used as the basis for mathematical models of population growth (e.g. Gause et al., 1936; Painting model development; (iii) summarize modelling studies et al., 1993; Fenton et al., 2010). Inevitably, such models that have been conducted with O. marina, and briefly are derived for the species that we can grow in the review the questions asked and conclusions drawn from laboratory, and for planktonic protozoa these have these and finally (iv) discuss continued directions of proven to be few. This paper is about one such species, research for modelling studies using O. marina. doi:10.1093/plankt/fbq105, available online at www.plankt.oxfordjournals.org. Advance Access publication August 26, 2010 # The Author 2010. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected] JOURNAL OF PLANKTON RESEARCH j VOLUME 33 j NUMBER 4 j PAGES 651–663 j 2011 TO WHAT EXTENT IS OXYRRHIS Capriulo, 1990). Examples of such an approach include MARINA AREPRESENTATIVE the semi-benthic rock pool dwelling Stombidium sulcatum MODEL ORGANISM? (S. inclinatum;seeModeo et al., 2003) that has been exten- sively used to represent planktonic ciliates and the fre- Meta analysis studies (e.g. Hansen et al., 1997) suggest quently studied mixotrophic chrysophyte Ochromonas danica, that O. marina is representative of the dinoflagellates. which was originally isolated from an acidic moor However, phagotrophic protozoa are diverse and abun- (Pringsheim, 1955). There is, thus, considerable pre- dant organisms in aquatic environments, including taxa cedence for using taxa like O. marina as model pelagic typically with a size range of 2–200 mm(Montagnes organisms, mainly because they are easy to grow, maintain et al., 2008a). Hence, no single species or even genus and collect, as indicated above. We, therefore again, will be representative of the functional group, and support the past and continued use of the O. marina,with Downloaded from https://academic.oup.com/plankt/article/33/4/651/1473431 by guest on 28 September 2021 championing O. marina as a representative of the hetero- the codicil that it is not necessarily typical of open water trophic dinoflagellates or even heterotrophic protists en taxa and should, ultimately, be compared to them. mass raises some reservations. Therefore, we first con- sider factors that may limit the general applicability of O. marina-based results to phagotrophic protozoa. Taxonomy Oxyrrhis marina is unlikely to be a single species, and there are strain-differences in eco-physiological Mode of nutrition responses (Lowe et al., 2005a, 2010). There are serious Oxyrrhis marina is a raptorial feeder that directly engulfs implications regarding this point, related to population its prey. Although protozoa exhibit a range of nutri- studies. For instance, the growth response of O. marina tional modes (Montagnes et al., 2008a), many, and poss- strains differs based on responses to: salinity (Lowe et al., ibly most, of the protozoa in aquatic pelagic ecosystems 2005a), prey concentration and type, and temperature (e.g. ciliates, flagellates) also engulf their prey, and thus (Montagnes, unpublished results). However, such strain- O. marina might be considered directly comparable to specific responses are far from unique to O. marina; e.g. these. Furthermore, anecdotal data suggest that O. marina similar strain-specific differences occur in a model fresh- ingests prey between 1 and 12 mm, indicating that its water ciliate, Urotrichia (Weisse and Montagnes, 1998). predator:prey size ratio includes, but also exceeds, the Thus, modellers must simply be aware of these differ- approximate 10:1 ratio predicted by others (e.g. Azam ences and consider them when interpreting results. In et al., 1983). Thus, as a first approximation, we support fact, as strain differences are becoming topical in eco- the use of O. marina as a model organism in this sense. logical research (see Weisse and Montagnes, 1998), this “problem” can become an asset, and modellers will undoubtedly begin to use the responses of the various Habitat strains to examine potential strain–succession, as we are Oxyrrhis marina is rarely seen in pelagic samples, at present doing (Yang et al., 2011). Finally, modelling although “red-tide” blooms occur in large bays, reach- studies based on O. marina typically use defined strains, ing up to 105 cells mL21, and it can regularly be found and we are exceptionally fortunate with O. marina that in some estuaries at abundances of 10–100 mL21 several commercial and personal culture collections (Johnson et al., 2003; Begun et al., 2004; Jeong et al., have maintained these (Lowe et al., 2011). Hence, not- 2004). In contrast, O. marina is typically found in shallow withstanding the caveats highlighted above, and the rec- waters associated with the shoreline, such as splash ognition that further comparative studies of the pools and tide pools (Johnson, 2000; Kimmance et al., behaviour of O. marina and other planktonic protozoa 2006). Still, O. marina is planktonic, not benthic, and in are required, O. marina seems fit for purpose as a repre- mixed cultures remains well distributed (Davidson, sentative protozoan, from which mathematical models Montagnes, unpublished results), although it may can be derived. accumulate at mid-water column interfaces (Menden- Deuer and Gru¨nbaum, 2006).Thus,again,inthissense,it seems an appropriate model organism for planktonic pro- OXYRRHIS MARINA-BASED cesses. Furthermore, using protists associated with very MATHEMATICAL MODELS shallow waters to model planktonic systems is not uncom- mon; much of the earlier work on protozoa, used to obtain We, therefore, now turn to those studies that have rate processes and conversion factors for pelagic ecosystem derived or parameterized mathematical models based models, has been obtained from semi-benthic species (e.g. on O. marina. Broadly, these fall into two categories: 652 K. DAVIDSON ET AL. j OXYRRHIS MARINA-BASED MODELS Table I: Studies that determine or apply O. marina-based equations and their functional forms Selected works that employ the Equation type and number Equation (see caption for symbols) function 1. Functional response I  p Kimmance et al. (2006); I ¼ max kI þ p Strom (1993) r  p 2. Numerical response r ¼ max Jeong et al. (2008) kr þ p r ðp À p0Þ 3. Numerical response with threshold prey level (p0) r ¼ max Kimmance et al. (2006); k þðp À p0Þ included. r Strom (1993) I  p 4. Functional response modified by ambient I ¼ max  aðT À bÞc Kimmance et al. (2006) kI þ p temperature 0 rmax ðp À p Þ 5. Numerical response modified by ambient r ¼  aT Kimmance et al. (2006) Downloaded from https://academic.oup.com/plankt/article/33/4/651/1473431 by guest on 28 September 2021 k þðp À p0Þ temperature r v  p 6.
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