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Mini-review
Ecological roles of zoosporic parasites in blue carbon ecosystems Frank H. GLEASONa,*, Floris VAN OGTROPb, Osu LILJEa, Anthony W.D. LARKUMa a
School of Biological Sciences F01, University of Sydney, Sydney, NSW 2006, Australia Faculty of Agriculture and Environment C81, University of Sydney, Sydney, NSW 2006, Australia
b
article info
abstract
Article history:
Pathosystems describe the relationships between parasites, hosts and the environment.
Received 22 March 2013
Generally these systems remain in a dynamic equilibrium over time. In this review we
Revision received 15 May 2013
examine some of the evidence for the potential impacts of change in dynamic equilibrium
Accepted 15 May 2013
in blue carbon ecosystems and the relationships to the amount of stored carbon. Blue
Available online 19 July 2013
carbon ecosystems are marine and estuarine ecosystems along the coasts. Virulent
Corresponding editor: € rlocher Felix Ba
pathogens can be introduced into ecosystems along with non-native hosts. Alteration of environmental conditions, such as temperature, pH and salinity, may cause parasites to dominate the pathosystems resulting in significant decreases in productivity and pop-
Keywords:
ulation sizes of producer hosts and in changes in the overall species composition and
Brown algae
function in these ecosystems. Such changes in blue carbon ecosystems may result in
Labyrinthulomycota
accelerated release of carbon dioxide back into the ocean and atmosphere, which could
Non-native species
then drive further changes in the global climate. The resiliency of these ecosystems is not
Oomycota
known. However, recent evidence suggests that significant proportions of blue carbon
Pathosystems
ecosystems have already disappeared.
Physical factors
ª 2013 Elsevier Ltd and The British Mycological Society. All rights reserved.
Phytoplankton Population declines Red algae Seagrasses Seaweeds
Introduction Conservation in blue carbon ecosystems Recently the International Working Group on Coastal Blue Carbon concluded that coastal carbon deposits need to be considered in national emission inventories, because continued degradation of blue carbon ecosystems could result in further
increases in carbon dioxide emissions into the atmosphere (Copertino and Da, 2011). Blue carbon ecosystems are marine and estuarine ecosystems which occur along the coasts of all continents and which contain populations of highly productive species of producers such as mangroves, seagrasses, large seaweeds, phytoplankton and corals, and significant carbon sinks. Sediments in salt marshes, seagrass meadows, mangrove forests and subtidal benthic ecosystems are known to provide
* Corresponding author. Tel.: þ61 299712071. E-mail address:
[email protected] (F.H. Gleason). 1754-5048/$ e see front matter ª 2013 Elsevier Ltd and The British Mycological Society. All rights reserved. http://dx.doi.org/10.1016/j.funeco.2013.06.002
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important carbon sinks where refractive carbon is buried for long periods (Fourqurean et al., 2012). In particular, seagrass meadows are considered among the most productive ecosystems on earth, and the carbon sink capacity of seagrass meadows is exceptional (Orth et al., 2006; Duarte et al., 2010, 2013). Seagrasses support high biodiversity habitats and account for approximately 20 % of the total carbon sequestration in marine sediments. The amount of organic carbon stored in healthy living seagrass biomass is estimated at 2.52 Mg C ha1 on average, much of which is buried in the soil as rhizomes and roots (Fourqurean et al., 2012). If pathosystems are not in equilibrium and disease results in the death of seagrass populations, much of this carbon could be released into the ocean and the atmosphere. Seagrass meadows currently are estimated to bury approximately 27.4 Tg C yr1 in total globally. If all of the organic carbon in seagrass biomass and the top metre of soils were to be remineralized, present rate of loss could result in release of up to 299 Tg C yr1 (Fourqurean et al., 2012). According to Copertino and Da (2011) the carbon sinks in many of these ecosystems presently have insufficient environmental protection. In fact, many blue carbon ecosystems are disappearing at a rapid rate (Copertino and Da, 2011). For example, Waycott et al. (2009) estimated that 29 % of all known seagrass area in the world disappeared between 1879 and 2009, and the rate of loss is accelerating. Some of this loss is due to total habitat destruction, while other losses are due to environmental factors. The significance of the rapid rates of loss of seagrass populations was highlighted again very recently by Bockelmann et al. (2013). Seagrass populations are particularly sensitive to increasing anthropogenic influences in coastal ecosystems (Orth et al., 2006), but environmental changes are seriously impacting the distributions and population densities of many other marine species as well (Schiel et al., 2004; Polovina et al., 2011). Examples of endangered ecosystems near Sydney Australia are shown in Figs 1e3. In this review we consider the potential roles of zoosporic parasites in reduction in size of populations of producers and
Fig 1 e Botany Bay. An endangered blue carbon ecosystem near Sydney, Australia. Seagrass communities are visible under water in a shallow region of the bay.
F.H. Gleason et al.
subsequent loss of carbon sinks in marine ecosystems. We use the pathosystems model for analysis of host-parasite dynamics. We discuss examples of specific hosts infected by zoosporic parasites. Finally we discuss the effects of physical factors and introduction of non-native species on hostparasite dynamics.
Zoosporic parasites Parasites include a large number of species, play critical roles in ecology and often face extinction when the structure and function of ecosystems change (Dobson and Hudson, 1986; mez, 2011). Nevertheless, Lafferty et al., 2008; Nichols and Go parasitism is a significant biotic factor which is rarely considered in reviews of the global environmental crisis (Nichols mez, 2011). In particular, parasites are thought to play and Go important roles in the carbon cycle, especially the microbial loop, in all aquatic ecosystems but research on this topic has been limited (Sime-Ngando, 2012). Zoosporic parasites are eukaryotic microorganisms (microparasites) which propagate by motile (flagellated) zoospores. In this paper we focus on some of the important zoosporic parasites (consumers) of populations of seagrasses and macro-algae (producers) in blue carbon ecosystems, their roles in population declines of dominant species and their potential roles in disease and population dynamics (1) from the perspective at the time of the third International Congress of Plant Pathology (Andrews, 1979) and (2) from the present perspective considering continuous global climate change, as adopted by the International Working Group on Coastal Blue Carbon (Copertino and Da, 2011). Some examples of zoosporic parasites in the Chytridiomycota, Oomycota, Hyphochytriomycota, Labyrinthulomycota and Phytomyxea are included.
Pathosystems Robinson (1976) introduced the concept of a pathosystem for the study of disease in terrestrial plants. A pathosystem is defined as the component of an ecosystem which involves parasitism. At the third International Congress of Plant Pathology in Munich, Andrews (1979) suggested that many of the concepts used in the study of the pathology of terrestrial plants be introduced into the study of the role of disease in marine seaweed ecosystems. In particular, Andrews (1979) proposed the use of the “pathosystem” concept in marine ecology. Here we use the pathosystems approach to analyse host-parasite relationships for hosts (producers: flowering plants, macroalgae and phytoplankton) and zoosporic parasites (consumers: true fungi, heterotrophic stramenopiles and protists) in marine ecosystems and relate this to the potential loss of blue carbon stores. Pathosystems are dynamic systems involving populations of hosts and parasites (Robinson, 1976). A dynamic system can remain stable only if it retains system balance or equilibrium which is achieved by systems controls. Systems controls involve communications between the component parts of the system. We would expect populations of parasites and hosts in pathosystems to remain in dynamic equilibrium as long as the systems controls are operating correctly. If the systems controls cannot operate, the equilibrium cannot be maintained, and relative
Ecological roles of zoosporic parasites
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Fig 2 e Narrabeen Lagoon, near Sydney, Australia. Extensive seagrass beds are found just under the water’s surface in this shallow lagoon. Exchange of water between the lagoon and the ocean is minimal.
population sizes will change. Systems controls include weapons which parasites use to attack their hosts (such as digestive enzymes), and defences used by hosts to prevent infection (such as an immune system). The equilibrium can also be changed by the introduction of new, more virulent genotypes of parasites. The interaction between biological factors thus controls equilibrium in pathosystems. Furthermore, physical factors also impact both host and parasite populations (Robinson, 1976) and often differently. This relationship is frequently represented graphically by the disease triangle.
Examples of large-scale population declines Some examples of sudden declines in population sizes (mass mortality) for species at the producer trophic level in blue carbon ecosystems are briefly described here. During the 1930’s wasting disease of seagrasses killed up to 90 % of the Zostera marina plants at many sites along the Atlantic coasts of North America and Europe (Muehlstein, 1989). Robblee et al. (1991) estimated a loss of up to 90 % of Thalassia testudinum plants from some sites in Florida Bay between 1987
Fig 3 e Long Reef headlands, near Sydney, Australia. Extensive beds of brown algae grow in the subtidal zone next to the rock platform.
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and 1990. Some species of large brown and red algae have also been affected. In 1957e1958 many Macrocystis pyrifera plants disappeared from extensive kelp beds near Point Loma, California (Vadas, 1979). Cole and Babcock (1996) reported mass mortality in 1992e1993 among Ecklonia radiata plants from the kelp beds near Goat Island off the coast of the North Island, New Zealand. Several species of Pythium frequently cause the death of Porphyra plants along the coasts of North America and in seaweed farms off the coasts of Japan, Korea and China (Hwang et al., 2009). Fortunately all of these ecosystems recovered, at least to some degree. If they had not, these ecological disasters could have resulted in the loss of many species and therefore ecosystem diversity and function. Not only are entire ecosystems threatened, but there have also been significant changes in species composition within many ecosystems. Increasing temperatures in the ocean as a result of both local and global climate change is considered a cardinal abiotic factor. For example, Schiel et al. (2004) correlated extensive changes in distribution and abundance of marine benthic species with increases in temperature over 10 yr along a 2 km section of the rocky coastline in California.
Significant diseases of producers in marine ecosystems Brown algal hosts (Phylum Phaeophyta) e parasites in the Phyla Chytridiomycota, Hyphochytriomycota, Oomycota and Phytomyxea Brown algae are a special group of primary producers in coastal ecosystems: in size alone some kelps outstrip many of the other algae and can vie with the tallest land plants in terms of length. However, they range down in size to small filaments (Schiel and Foster, 2006). Schiel and Foster (2006) estimate that there are 100 species of kelps and 500 species of somewhat smaller fucoids worldwide. The large and dominant canopy species form ecosystems which shelter many smaller organisms. The small filamentous species grow adventitiously and provide models for host-parasite interactions (Gachon et al., 2006, 2010). The life cycles of kelps are characterized by heteromorphic alternation of generations including haploid spores, microscopic gametophytes, diploid embryos and macroscopic sporophyte stages. In the life cycle of fucoids the male and female gametes are the only haploid stages, giving rise to the mature, adult, diploid phase. Schiel and Foster (2006) provide a summary diagram comparing the life cycles of these and other families of brown algae. We would expect free living microscopic and macroscopic stages to have different resource requirements and environmental needs, but mortality is high in all of the microscopic stages, both haploid and diploid stages (Schiel and Foster, 2006). A complete understanding of the biology of brown algae requires research on the effects of environmental factors on all stages which are necessary for reproduction. € ller et al. (1999), Ku € pper and Mu € ller (1999) and Maier Mu et al. (2000) documented infection of a wide range of species
F.H. Gleason et al.
from many orders of brown algae by zoosporic parasites from different phyla. Intensive studies of infection were conducted with filamentous hosts in culture. For example, Eurychasma dicksonii (Oomycota), Anisolpidium rosenvingei (Hyphochytriomycota) and Chytridium polysiphoniae (Chytridiomycota) infect Pylaiella littoralis, and Maullinia ectocarpii (Phytomyxea) infects Ectocarpus siliculosus. Epidemics of these diseases have been documented at some sites along the coasts but the aetiology of these diseases requires further research. Both vegetative and reproductive cells in the gametophyte and sporophyte stages of these hosts can be infected by these parasites. Also the filaments of these hosts can be fragmented by infection which may facilitate dispersal of both the parasite and the host. Recently, Aguilera et al. (1988) and Goecke et al. (2012) reported a new phytomyxean species closely related to Maullinia which causes the formation of galls on the blades of the bull kelp Durvillaea antarctica in Chile. It is possible that this parasite interferes with reproduction in Durvillaea because this host has a fucoid life cycle with conceptacles in the blades. Gachon et al. (2006) found that infection of cells of P. littoralis by C. polysiphoniae strongly affected the regulation of energy dissipation from the algal antenna apparatus and reduced the rate of photosynthesis in the laboratory. Quantitative studies on the effects of these parasites on reproductive and photosynthetic rates at the population level are lacking.
Seagrass hosts (Phylum Angiospermae) e parasites in the Phyla Phytomyxea and Labyrinthulomycota Seagrasses are flowering plants which are capable of growth while fully submerged in temperate and tropical marine coastal habitats around the world (Waycott et al., 2009). Like other flowering plants, they produce seeds and pollen. However, pollination and fertilization occur in water rather than in terrestrial environments. Pollen grains are commonly used as baits for isolation of saprotrophic species of Thraustochytrium (Labyrinthulomycota) and related genera in marine ecosystems, and both pollen and seeds are commonly used as baits for many genera of Chytridiomycota and Oomycota in all aquatic ecosystems (Sparrow, 1960). We would, therefore, expect both the male gametophyte and young sporophyte stages of seagrasses to be potentially susceptible to attack by zoosporic parasites. However, this has not been carefully studied. Walker and Campbell (2009) recently reported Plasmodiophora diplantherae in specimens of Halodule wrightii collected at three sites in northern central Gulf of Mexico. Vergeer and den Hartog (1994) found a worldwide distribution of this pathogen. Gall formation is conspicuous in infected shoots of both H. wrightii and Zostera spp. Infected plants appear dwarfed because internodes are unable to elongate, and swell up to form galls instead. Growth of leaves and inflorescences appears relatively normal in infected plants (den Hartog, 1987). P. diplantherae is spread to new hosts by primary zoospores across short distances (Neuhauser et al., 2011). Because of the poor development of roots these seagrass plants are easily uprooted by the motion of currents. In this case carbon from their roots cannot be added to the carbon pool in the sediments. Furthermore, both viable seeds and resistant
Ecological roles of zoosporic parasites
sporangia (of the parasite) on the leaves of the floating host plants can be carried to new ecosystems by the currents resulting in new infections. Some species in the genus Labyrinthula are known to cause wasting disease of seagrasses. For example, Labyrinthula zosterae causes this disease in Z. marina (Muehlstein et al., 1991). Application of Koch’s postulates confirmed that L. zosterae is a primary pathogen (Ralph and Short, 2002). Z. marina is a pantemperate northern hemisphere seagrass which has experienced wasting disease in Japan, west and east coasts of North America and Europe (Short et al., 1993). Vergeer and den Hartog (1994) isolated Labyrinthula spp. from all species of seagrasses which they collected from many parts of the world, mostly from lesions on the leaves. These host species belong to Zostera, Heterozostera, Posidonia, Halodule, Cymodocea, Syringodium, Thalassodendron, Ruppia, Thalassia and Halophila. Some isolates of Labyrinthula spp. appear to be host specific. However, most of the beds from which this material was collected appeared healthy. This suggests that other environmental factors may be involved in the expression of symptoms of this disease. The symptoms of this disease begin with small black-brown spots, streaks and blackened lesions on the surface of the leaves, and then the parasites subsequently spread inside the leaf tissue leading to the death of the host. Labyrinthula is transmitted to new hosts by direct contact between plants or by drifting plant parts (Ralph and Short, 2002). More recently the presence of Labyrinthula was assessed in 18 seagrass meadows in the Balearic Islands in the western Mediterranean (Garcias-Bonet et al., 2011). This protist was present in 70 % of the specimens of Posidonia, Cymodocea and Zostera collected from these meadows. Cross-infection experiments using isolates of Labyrinthula from both Europe and North America indicated that these pathogens can infect seagrasses in different genera and, therefore, have wide host ranges, in contrast to data from earlier studies. Data from Vergeer and den Hartog (1994) and Garcias-Bonet et al. (2011) suggest that species of Labyrinthula are omnipresent in many coastal marine ecosystems and are facultative parasites and saprotrophs. Some isolates of Labyrinthula can be grown with bacteria or synthetic media as a food source (Sykes and Porter, 1973; Wahid et al., 2007). Other ecotypes of Labyrinthula grow on detritus (Amon, 1978). Infection of T. testudinum by a species of Labyrinthula endemic to Florida Bay impaired photosynthesis in leaf tissues (Durako and Kuss, 1994). The photosynthetic efficiency of leaves of Z. marina was reduced by infection with L. zosterae in New Hampshire as well (Ralph and Short, 2002). In L. zosterae the quantum yield of photosynthesis decreased directly with the progression of the disease. Although data have been collected from individual plants in the laboratory, the effect of this disease on photosynthesis at the population level is unknown. However, we expect that infection by parasites together with unfavourable physical conditions for growth could substantially decrease photosynthetic rates in seagrass populations in what should be highly productive ecosystems and may result in a net change in rates of carbon dioxide emissions from these ecosystems. However, this hypothesis needs to be tested in field studies.
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Red algal hosts (Rhodophyta) e parasites in the phylum Oomycota Several species of Oomycota are common parasites of red algae. Some of the larger red algae, such as Chondrus crispus, Palmatria mollis and Porphyra yezoensis, can be dominant species in intertidal and subtidal zones. Many red algae are harvested from natural habitats or are grown in mariculture for commercial products. For example, the red alga, Porphyra (nori), is an important food item in the Far East. P. yezoensis is infected by two species of Oomycota simultaneously, Pythium porphyrae and Olpidiopsis sp. (Kazama, 1979; Ding and Ma, 2005). As the infection progresses P. porphyrae begins to predominate. These parasites are spread to new hosts by biflagellate zoospores. The red rot disease caused by P. porphyrae can cause the death of its host within a few days. Characteristic symptoms include disease spots and infected holes in the fronds (leafy thalli). The conchocelis phase is not infected. High temperature, low salinity and high densities of plants in farms tend to promote the disease. Pythium survives environmental extremes by production of resistant oospores which are distributed in sediment in the sea floor over a wide area around the Porphyra farms near Japan (Kawamura and Yokoo, 2005). The species of Porphyra along the coasts of Japan and North China are winter annuals, while in North America they are summer annuals. Pythium species cause similar diseases along the Pacific and Atlantic coasts of North America. Since P. porphyrae can easily be grown in culture it is considered to be a facultative parasite. Petersenia pollagaster is an endobiotic parasite of Chondrus crispus, especially in mariculture facilities in Nova Scotia, Canada (Molina, 1986; Molina et al., 1988). This parasite invades cortical and subcortical tissues and causes lesions on the tips of the blades. Molina (1986) inoculated uninfected host plants with zoospores and studied the life cycle in the laboratory with the electron microscope. Laboratory experiments indicated a strong relationship between temperature and infection rate. Maximum numbers of lesions are formed between 15 and 20 C. In the field the disease occurs in late summer and early autumn. Petersenia palmariae is an endobiotic parasite which infects the fronds of P. mollis along the west coast of Vancouver Island, Canada (Van der Meer and Pueschel, 1985). This parasite will not grow at low temperatures.
Phytoplankton hosts e parasites in the phyla Oomycota and Phytomyxea Diatoms (Bacillariophyta) are relatively recalcitrant, inedible microorganisms, but their carbon can be returned to the ecosystem by the Mycoloop prior to sinking (Kagami et al., 2007). Reports of zoosporic parasites of diatoms in marine environments include: (1) Ectrogella perforans (Oomycota), a parasite of Licmophora hyalina (pennate diatom) near Goa, India (Raghukumar, 1980), (2) Lagenisma coscinodisci (Oomycota), a parasite of Coscinodiscus sp. (centric diatom) in Puget Sound, USA (Gotelli, 1971), (3) an unidentified heterotrophic stramenopile, a parasite of the bloom-forming diatom Pseudo-nitzschia sp. near Prince Edward Island, Canada (Hanic et al., 2009) and (4) two species of Phagomyxa (Phytomyxea),
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parasites of Bellerochea malleus and Odontella sinensis (centric diatoms) in the North Sea (Schnepf et al., 2000). Whether heterotrophic stramenopiles and plasmodiophorids can prevent addition of a significant amount of carbon into marine snow during sinking is not known. Several species of Oomycota and Labyrinthulomycota have also been reported to infect marine filamentous green algae (Chlorophyta) along the coast (Raghukumar, 1987). The hosts include species of Cladophora, Rhizoclonium and Chaetomorpha.
Some physical factors implicated in climate change Temperature At present the mean temperatures of both the atmosphere and the ocean surface are gradually increasing at the global scale primarily due to the combustion of fossil fuel (Orth et al., 2006; Doney et al., 2012; Fourqurean et al., 2012). Changes in temperature can alter the composition of communities. Schiel et al. (2004) studied the effect of a large increase in temperature on the composition of benthic algal communities near a thermal outfall from a power generating station in California. Significant changes in composition were documented but the temperature range for growth of each of the individual species remains to be determined. Although shifts in distribution of brown algae into cooler waters have been observed with global warming (Polovina et al., 2011), comprehensive quantitative data are not yet available. Bockelmann et al. (2013) provided some evidence that prevalence of infection and abundance of Labyrinthula increases during the warm spring and summer months. Increases in temperature of ocean water also stimulates red rot disease of Porphyra as previously discussed.
pH At present carbon dioxide levels in the atmosphere are increasing (Orth et al., 2006; Doney et al., 2012; Fourqurean et al., 2102). When carbon dioxide dissolves into water, the pH decreases. Another cause of acidification in the ocean is acid effluents from rivers. One example of the effect of pH on pathosystems is provided by Park et al. (2006). Park et al. (2006) found that Pythium parasites of Porphyra could adapt well to growth at pH 4. When acid fungicides were added to seawater to attempt to control the red rot disease in Porphyra farms, the growth of Pythium was stimulated while the growth of Porphyra was inhibited.
F.H. Gleason et al.
organism has a specific range of salinities for growth and survival. Therefore, changes in salinity could affect species composition, richness and abundance. This topic has been recently reviewed by Logares et al. (2009). Changes in salinity have long been suspected to be a factor in expression of the symptoms of wasting disease of seagrasses. Trevathan et al. (2011) evaluated the impacts of hypersalinity for 7 d on the early stages of infection in T. testudinum by assessing changes in cellular physiology and metabolism in the laboratory. After infection by Labyrinthula sp. the occurrence of wasting disease was significantly lower in the hypersalinity treatments.
Light Light intensity affects the rates of photosynthesis in producers. Estuarine light conditions may change as a result of changes in turbidity due to increase in river discharge or due to increased storm intensities which can stir up bottom sediment (Paerl et al., 2006). Biotrophic parasites could be indirectly affected if the producer (host) is its sole food source. Light limitation inhibits both epidemic development and survival of parasites in the Asterionella-Rhizophydium association in freshwater lakes (Bruning, 1991). Also, zoospores of marine zoosporic parasites can be phototactic (Kazama, 1972), so that they remain in the euphotic zone along with their hosts. Sedimentation reduces light intensity in aquatic ecosystems.
Introduction of non-native species Peeler et al. (2011) discussed the recent emergence of infectious diseases caused by Saprolegnia spp. and other zoosporic parasites in bony fish, amphibian and crayfish hosts in freshwater ecosystems throughout Europe. Species of Perkinsus infect marine molluscs throughout the world (Villalba et al., 2004) especially in oyster farms. The resulting disease, Perkisosis, often causes epidemics in populations of many species of bivalves. The spread of these diseases are examples of the results of the introduction of non-native hosts carrying parasites into new environments for commercial purposes or inadvertently through the worldwide animal trade. The introduction of non-native species carrying parasites drives disease emergence by extending the geographical range of parasites and their hosts and facilitates host-switching (Peeler et al., 2011). Many of these parasites are generalists with wide host ranges and may become a serious threat to many species in both freshwater and marine ecosystems.
Discussion and future perspectives Salinity Global warming has the potential to change ocean salinities at both local and global scales. There is evidence for changes in salinity at a local estuarine scale due to changing river runoff conditions (Knowles and Cayan, 2002). At a global scale there is evidence that salinity is decreasing towards the poles and increasing towards the equator (Harvell et al., 2002; Curry et al., 2003; Doney et al., 2012). Furthermore, the melting of polar ice caps is releasing freshwater into the oceans. Each
In pathosystems, if the parasites and their hosts react differently to environmental parameters, large changes in biotic and abiotic factors could shift the equilibrium to favour either the parasite or the host populations (Robinson, 1976). Introduction of new virulent genotypes into populations of parasites could shift the equilibrium as well and subsequently increase prevalence of disease (Peeler et al., 2011; Fisher et al., 2012). Therefore, the introduction of non-native parasites and climate change could lead to pandemics, reduction in
Ecological roles of zoosporic parasites
community complexity, large changes in community structure and function and even extinction in extreme cases. Since pathosystems in blue carbon ecosystems have rarely been studied, it is difficult to predict the extent of extinction. Climate change also impacts the capacity of blue carbon ecosystems to store carbon. Furthermore, if carbon stored in these ecosystems is re-mineralized, carbon dioxide may potentially be reassimilated into the oceans and atmosphere (Fourqurean et al., 2012), which in turn may accelerate global warming. Unfortunately at this time quantitative data on the export of carbon into sinks is not available at the macro scale. Importantly, there is evidence to suggest that climate warming will cause more frequent or sever disease in host populations (Harvell et al., 2002). Some of the characteristics of fungi and fungal-like organisms which are considered to cause emerging infectious diseases, in the model proposed by Fisher et al. (2012), have also been documented in some species of zooporic parasites observed in blue carbon ecosystems. Some of the known species in the genus Labyrinthula are good examples. These parasites are rapidly spread by motile zoospores and amoeboid spindle cells in an ectoplasmic net (Muehlstein et al., 1991). Species of the genus Labyrinthula grow and survive in extreme environments with many substrates and in variable temperatures and salinities, such as around the Great Salt Lake in Utah, USA (Amon, 1978). Although thick walled cysts have rarely been seen, the spindle cells themselves must be resistant to environmental extremes. Some ecotypes of Labyrinthula are virulent and the host range in the Mediterranean Sea appears to be broad (GarciasBonet et al., 2011). Bockelmann et al. (2013) found strong spatial and temporal variations in the prevalence of wasting disease of Z. marina and abundance of the pathogen, Labyrinthula zosterae in ecosystems in northern Europe. In the study of epidemiology it is important to define host specificity including primary and alternative hosts and reservoirs. The physiology of zoospores of true fungi was recently reviewed by Gleason and Lillje (2009). Zoospores are essentially weapons of mass destruction. They are released in large numbers and can swim for several hours. Some studies indicate that they are chemotactic and can navigate from the point of release to the surface of a utilizable substrate along a chemical gradient. Thus, they can efficiently find uninfected hosts. Once they attach to their hosts they release digestive enzymes causing damage to the host tissues. Zoospores are not the only vehicles for dispersal. For example, cysts of Chytridiomycota and Phytomyxea remain attached to floating debris. Unfortunately, we expect that the kinds of sudden declines in population sizes of producers in marine ecosystems we described earlier in this paper are likely to occur more frequently in the future considering the accelerated rate of climate change. For this reason, marine ecologists need to monitor populations of producers and be able to predict epidemics so that they can intervene before the ecosystem gets out of control. According to Orth et al. (2006), monitoring programs have been increased in many parts of the world but they are still inadequate in our opinion. For example, monitoring programs should estimate the incidence and rate of spread of the incidence of infectious diseases caused by all
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groups of zoosporic parasites, particularly those discussed in this review. Furthermore, monitoring programs should monitor physical parameters at the micro-scale level, because global climate changes can impact ecosystems at any level. There are a number of significant knowledge gaps in our understanding of the dynamics of carbon flow in blue carbon ecosystems which need attention. One of these is the differences in the patterns of metabolism among eukaryotic microorganisms in aerobic and anaerobic zones. The parasites considered in this review are found growing in aerobic zones. Here they can re-mineralize their substrata before they sink into the anoxic zones. Roots of seagrasses, tissues of large algae, marine snow and detritus contribute to carbon sinks. The rates of decomposition in anoxic zones are considered to be very slow, but in fact these rates have not been accurately measured at the macro scale. If the rate of decomposition of seagrasses by Labrinthula increases with ocean temperature as has been suggested by Bockelmann et al. (2013), then we would expect less addition of carbon to the sediments by their roots. If virulent ecotypes of Labyrinthula cause a large-scale loss in populations of seagrasses, this could have a significant effect on stored carbon pools. More models for studying the functions of parasites in food webs in general are urgently needed. Fortunately, models for predicting the spread of emerging infectious diseases (EIDs) in both freshwater and terrestrial environments are presently under construction (Grami et al., 2011; Fisher et al., 2012). These models will aid in predicting the onset of epidemics and understanding the impact of climate change on the balance between the growth of hosts and parasites. One application of modelling has been implemented recently in the north Pacific Ocean. Park et al. (2006) have developed molecular techniques for counting Pythium zoospores in seawater near Porphyra farms. Since the incidence of the red rot disease is proportional to the size of the zoospore inoculum, Hwang et al. (2009) developed a procedure designed to predict outbreaks of this disease based on densities of zoospores. Finally, we need to develop new methods such epifluorescent staining and CARDFISH to enable identification of parasites on their hosts (Jobard et al., 2010). Global climate change, environmental deterioration, eutrophication and introduction of non-native parasites appear to be driving the spread of EIDs and invasive species in many freshwater, marine and terrestrial ecosystems (Villalba et al., 2004; Peeler et al., 2011; Fisher et al., 2012). If some of the parasites in blue carbon ecosystems are in fact emerging infectious diseases, and if their spread is accelerated by global climate changes and introduction of non-native virulent species, we would predict that their frequency in marine communities will increase in the near future. However, data to support these hypotheses are currently lacking. It is, therefore, imperative that we carefully monitor these changes and understand how they impact the balance between host and parasite populations in these pathosystems. The purpose of this paper was not to provide an extensive list of all hosts infected by zoosporic parasites, rather we selected examples of parasites of large producers which have been carefully studied and which are thought to cause epidemics. There are many reports of other parasites and hosts which have not been as carefully documented. Whether any
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of these other hosts can provide reservoirs for parasites is not known. Further research is needed.
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