Do Meiofauna Control Red Tides?

The protected waters of the Chiloe inland sea in the Region de Los Lagos are the epicentre of aquacultural production in Chile, with large portions of the coast used for cultivating salmonids, bivalves and algae. Furthermore, a large number of other marine species are harvested from natural populations, including filter-feeding bivalves such as clams which are susceptible to red-tide events. This area is bordered on the western side by the island of Chiloe and on the eastern side by the fjords of the Corrdillera de Los Andes.

Red-tides, referred to in the literature as Harmful algal blooms (HABs), are phytoplankton blooms that occur in coastal waters that have the potential to cause detrimental physiological effects on marine organisms, including mortality (Hallegraeff, 2003). The toxic compounds produced by the phytoplankton can be transmitted and biomagnified by the food chain with the potential for severe health problems or mortality in human consumers (Sellner et al., 2003). Beyond the immediate public health issues the presence of red-tides in an area leads to the closure of fisheries, export bans and the subsequent economic impacts on the local economy.

HAB events have increased in frequency, duration, intensity and geographic extent over recent decades (Hallegraeff, 2003; Sellner et al., 2003). Dinoflagellates of the genus Alexandrium, which cause Paralytic Shellfish Poisoning (PSP) (Hallegraeff, 2003) are among the principal red-tide species in the phytoplankton. Up until the 1970’s these species were confined to coastal areas in the northern hemisphere; Europe, North America and Japan. However since then they have spread to the southern hemisphere, including south-east Asia, Australasia, southern Africa and South America (Hallegraeff, 2003).

Alexandrium catenella was first recorded in Chile, in the Magallanes region (52ºS) in 1972 and has over subsequent decades spread north through the channels and fjords systems of southern Chile, with outbreaks now occurring as far north as the Los Lagos region (42ºS) (Guzmán et al., 2002; Clément et al., 2009; Mardones et al., 2010). These outbreaks have affected both the natural and aquacultural systems that are so important to the local economy in southern Chile, and have had consequences for human health, both locally and nationally. (Clément & Guzmán, 1989; Uribe et al., 1997; Molinet et al., 2003; Seguel et al., 2005; Fuentes et al., 2008; Clément et al., 2009).

Like many planktonic dinoflagellate species A. catenella produces cysts. These cysts are the resting stage of the dinoflagelate life cycle, and are produced by sexual reproduction during the peak of the bloom (Dale 1983). After encystment the cysts sink through the water column and accumulate in the sediment where they form a seed bank and a future source of inital individuals for the formation of subsequent blooms (Kremp, 2001; Genovesi et al., 2008). Cysts can remain viable in the sediment for five to ten years, or maybe longer (Anderson et al., 2003). Thus the cyst population in the sediments may be an important factor in determining the frequency and magnitude of future blooms (Anderson et al., 2014), and factors that may control cyst populations in the sediment are an important line of research in studying bloom dynamics (Marcus & Boero, 1998).

Meiofauna, organisms between 45 and 1000 μm are a diverse and abundant component of the benthic ecosystem (Giere, 2009). A diverse array of trophic guilds are represented within the meiofauna (Hicks & Coull, 1983; Boaden, 1995; Moens & Vincx, 1997; Giere, 2009) and it is prefectly possible that A. catenella cysts form part of the diet for some meiofaunal organisms (Pati et al., 1999; Franco et al., 2008). When cysts are consumed by deposit feeding macrofaunal organisms, invertebrates larger than 1000 μm, they generally pass through the gut without being digested. Thus macrofauna are generally responsable for the redistribution of cysts in the sediment column, but do not significantly alter the population of Alexandrium cysts in the sediment (Piot et al., 2008; Shull et al., 2014). Meiofauna, however, may potentially feed on cysts in three ways, they may swallow the cyst whole, they may pierce the cyst and suck-out the contents, or they may masticate and break-up the cyst. If the meiofauna are swallowing the cyst whole it may simply pass through the gut undigested, and as with the macrofauna have no effect of the population dynamics of A catenella. With the other two feeding modes however, if the mode is sufficiently common or practiced by an abundant species there exists the potential for the meiofaunal assemblage to have a significant effect on the population dynamics of A. catenella. Some meiofaunal organisms have piercing mouthparts or mandibles which could be used for breaking open the cysts of A. catenella (Pati et al., 1999). For example, there are nematode species such as those in the family Oncholaimidae that have a large dorsal tooth and smaller ventral teeth, these are used to prise open diatoms and suck-out the contents (Nehring, 1992; Leduc, 2009), it is therefore conceivable that the same method could be used to break open a cyst. Other nematode species have a buccal cavity lined with flexible mandibles capable of breaking open diatoms (Moens & Vincx, 1997). Harpacticoid copepods are also abundant members of the meiofauna and are though to be primarily herbivores feeding on the microphytobenthos (Azovsky et al., 2005; De Troch et al., 2012; Rzeznik-Orignac & Fichet, 2012), again it is conceivable that if the have the capacity to break open diatoms and feed on their contents. Diatoms and dinoflagellates from part of the diet of many other meiofaunal species, including ciliates (Fenchel, 1968), turbellarians (Boaden, 1995), kinorhynchs (Higgins, 1988), tardigrades (Guidetti et al., 2012), ostracods (Buffan-Dubau & Carman, 2000), halacarid mites (Green & MacQuitty, 1987), interstitial polychaetes and oligochaetes (Giere, 2009). Organisms that are physically capable of breaking open diatom frustules should in theory also be capable of breaking open A. catenella cysts.

The resting stages, eggs and cysts of various types, of many planktonic species are to be found in sediments, forming part of the “temporary meiofauna” and thus may be subject to interactions with the “permanent” meiofauna (Boero et al., 1996; Pati et al., 1999). Thus, whilst the focus of this study will be the interactions between meiofauna and A. catenella, the results may suggest a wider ecological phenomena that may provide insight into the population dynamics of a wide range of planktonic populations the wider planktonic ecosystem, and the role of benthic-pelagic coupling in marine ecosystem functioning (Marcus & Boero, 1998).

In summary, red-tides are a significant threat to both human health and the economy. Dinoflagelate species that form red-tides, such as A. catenella, form cysts as a normal part of their life-cycle which allows the populations to persist when conditions are less than optimal. The cysts form a seed-bank in marine sediments which are the source of future blooms. The abiotic and biotic conditions in the sediments will determine the survival of those cysts and significantly influence A. catenella population and bloom dynamics. One potential biotic interaction that may occur in the sediments is the predation of cysts by meiofaunal organisms. Given the high diversity and abundance of meiofaunal organisms it is possible that certain members of the meiofaunal assemblage could significantly influence the population dynamics of A. catenella and thus the frequency and intensity of blooms. The hypotheses proposed in this project would explore the trophic interactions between meiofauna and A. catenella and try to determine if they do indeed influence A. catenella population dynamics.

References

Anderson, D.M.; Fukuyo, Y & Matsuoka, K. (2003) Cyst methodologies. In: Hallegraeff, G.; Anderson, D. & Cembella, A. (eds.) Manual on Harmful Microalgae. UNESCO Publishing, 793 pp.

Anderson, D.; Keafer, B.; Kleindinst, J.; McGillicuddy Jr., D.; Martin, J.; Norton, K.; Pilskaln, C.; Smith, J.; Sherwood, C. & Butman, B. (2014) Alexandrium fundyense cysts in the Gulf of Maine: Long-term time series of abundance and distribution, and linkages to past and future blooms. Deep-Sea Research II, 103:6-26.

Azovsky, A.; Saburova, M.; Chertoprood, E. & Polikarpov, I. (2005) Selective feeding of littoral harpacticoids on diatom algae: hungry gourmands? Marine Biology, 148:327-337.

Boaden, P. (1995) Where Turbellaria? Concerning knowledge and ignorance of marine turbellarian ecology. Hydrobiologia, 305:91-99.

Boero F., Belmonte G., Fanelli G., Piraino S. & Rubino F. (1996) The continuity of living matter and the discontinuities of its components: do plankton and benthos really exist? Trends in Ecology and Evolution, 11:177-180.

Buffan-Dubau, E. & Carman, K. (2000) Diel feeding behavior of meiofauna and their relationships with microalgal resources. Limnology and Oceanography, 45:381-395.

Clément, A & Guzmán, L. (1989) Red tide in Chilean fjords. In: Okaichi, T.; Anderson, D.M. & Nemoto, T. (eds.) Red Tides Biology, Environmental Science, and Toxicology. Elsevier, New York pp. 121-124.

Clément, A.; Mardones. J.; Fuica. N.; Rojas. X. & Aparicio. C. (2009) Mareas Rojas en el mar interior de la macrozona sur. In: Simposio de Microalgas, XXIX Congreso de Ciencias del Mar, p.80.

Dale, B. (1983) Dinoflagellate resting cyst: “benthic plankton”. In: Fryxell, G.A. (ed.), Survival Strategies of the Algae. Cambridge University Press. pp. 69-137.

De Troch, M.; Vergaerde, I.; Cnudde, C.; Vanormelingen, P.; Vyverman, W. & Vincx, M. (2012) The taste of diatoms: the role of diatom growth phase characteristics and associated bacteria for benthic copepod grazing. Aquatic Microbial Ecology, 67:47-58.

Faust, M. & Gulledge, R. (1996) Associations of microalgae and meiofauna in floating detritus at a mangrove island, Twin Cays, Belize. Journal of Experimental Marine Biology and Ecology, 197:159-175.

Fenchel, T. (1968) The ecology of marine microbenthos II. The food of marine benthic ciliates. Ophelia, 5:73-121.

Franco, M.; Soetaert, K.; Costa, M.; Vincx, M. & Vanaverbeke, J. (2008) Uptake of phytodetritus by meiobenthos using 13C labelled diatoms and Phaeocystis in two contrasting sediments from the North Sea. Journal of Experimental Marine Biology and Ecology, 362:1-8.

Fuentes, C.; Clement, A. & Aguilera, A. (2008). Summer Alexandrium catenella bloom and the impact on fish farming in the XI Aysén region, Chile. In: Moustrup, O. et al. (eds). Proceeding of the International Conference on Harmful Algae. International Society for the Study of Harmful Algae and Intergovernmental Oceanographic Commission of UNESCO. Copenhagen pp. 183-186.

Genovesi, B.; Masseret, E.; Shin-Grzebyk, M.-S.; et al. (2008) Co-occurrence of two Alexandrium species in Thau Lagoon. Harmful Algae News, 37:1-2.

Giere, O. (2009) Meiobenthology. The Microscopic Motile Fauna of Aquatic Sediments. Springer-Verlag, Berlin, pp. 527

Green, J. & MacQuitty, M. (1987) Halacarid Mites. E.J. Brill/Dr. W. Backhuys, London. pp. 178.

Guidetti, R.; Altiero, T.; Marchioro, T.; Amade, L.; Avdonina, A.; Bertolani, R. & Rebecchi, L. (2012) Form and function of the feeding apparatus in Eutardigrada (Tardigrada). Zoomorphology, 131:127-148.

Guzmán, L.; Pacheco, H.; Pizarro, G. & Alarcón, C. (2002) Alexandrium catenella y Veneno Paralizante de los Mariscos en Chile. In: Sar, E.; Ferrario, M. E. & Reguera, B. (eds.), Floraciones Algales Nocivas en el Cono Sur Americano. Instituto Español de Oceanografía, pp. 235-255.

Hallegraeff, G. (2003) Harmful algal blooms: a global overview. In: Hallegraeff, G.; Anderson, D. &Cembella, A (eds.) Manual on Harmful Microalgae. UNESCO Publishing, 793 pp.

Hicks, G. & Coull, B. (1983) The ecology of marine meiobenthic harpacticoid copepods. Oceanography and Marine Biology Annual Review, 21:67-175.

Higgins, R.P. (1988) Kinorhyncha. In: Higgins, R. & Thiel, H. (eds.), Introduction to the Study of Meiofauna. Smithsonian Institution Press, Washington D.C. pp. 488

Kremp, A. (2001) Effects of cyst resuspension on germination and seeding of two bloom-forming dinoflagellates in the Baltic Sea. Marine Ecology Progress Series, 216:57-66.

Leduc, D. (2009) Description of Oncholaimus moanae sp. nov. (Nematoda: Oncholaimidae), with notes on feeding ecology based on isotopic and fatty acid composition. Journal of the Marine Biological Association of the United Kingdom, 89:337-344.

Marcus, N. & Boero, F. (1998) Minireview: The importance of benthic-pelagic coupling and the forgotten role of life cycles in coastal aquatic systems. Limnology and Oceanography, 43:763-768.

Mardones, J.; Clément, A.; Rojas, X. & Aparicio, C. (2010) Alexandrium catenella during 2009 in Chilean waters, and recent expansion to coastal ocean. Harmful Algae News, 41:8-9.

Moens, T. & Vincx, M. (1997) Observations on the feeding ecology of estuarine nematodes. Journal of the Marine Biological Association of the United Kingdom, 77:211-227.

Molinet C.; Lafon A.; Lembeye G. & Moreno C. (2003). Patrones de distribución espacial y temporal de floraciones de Alexandrium catenella (Whoedon & Kofoid) Balech 1985, en aguas interiores de la Patagonia noroccidental de Chile. Revista Chilena de Historia Natural, 76:681-698.

Nehring, S. (1992). Die Vegetarier unter den freilebenden Nematoden. 1. Die Aufwuchsfresser. Mikrokosmos, 81:135-140.

Pati, A.; Belmonte, G.; Ceccherelli, V. & Boero, F. (1999) The inactive temporary component: an unexplored fraction of meiobenthos. Marine Biology, 134:419-427.

Piot, A.; Rochon, A.; Stora, G. & Desrosiers, G. (2008) Experimental study on the influence of bioturbation performed by Nephtys caeca (Fabricius) and Nereis virens (Sars) annelidae on the distribution of dinoflagellate cysts in the sediment. Journal of Experimental Marine Biology and Ecology, 359:92-101.

Rzeznik-Orignac, J. & Fichet, D. (2012) Experimental estimation of assimilation rates of meiofauna feeding on benthic diatoms 14C-labelled. Journal of Experimental Marine Biology and Ecology, 432-433:179-185.

Seguel, M.; Tocornal M. & Sfeir A. (2005) Floraciones algales nocivas en los canales y fiordos del sur de Chile. Ciencias de Tecnología Marina, 28:5-13.

Sellner, K.; Doucette, G. & Kirkpatrick, G. (2003) Harmful algae blooms: causes, impacts and detection. Journal of Industrial Microbiology and Biotechnology, 30:383-406.

Shull, D.; Kremp, A. & Mayer, L. (2014) Bioturbation, germination and deposition of Alexandrium fundyense cysts in the Gulf of Maine. Deep-Sea Research II, 103:66-78.

Uribe, J.C.; Guzmán, L.; Pizarro, G.; Alarcón, C. & Iriarte, J.L. (1997) Monitoreo de la Marea Roja en las aguas interiores de la XII región. Fondo de Investigación Pesquera, 204 pp.