Hans-Uwe Dahms^1*, Bong-Rae Kim² and Hyung-Uk Park^1,2

¹ Environmental Laboratory, Green Life Science Department,

Sangmyung University, 7 Hongji-dong, Jongno-gu, Seoul 110-743, South Korea.

² NFRDI, National Fisheries Research and Development Institute,

Inland Fisheries Research Institute, Gyeonggi-do 114-3, South Korea. e-mail: marc436@yahoo.com*

Introduction

In the coming decades, the marine environment will be subject to profound changes, such as elevation of water temperature. The effects of such changes are likely to be manifested in microbial biofilms that cover all man-made or natural surfaces in the aquatic environment, which are subjected to biofouling by different species of microorganisms (Dahms et al., 2007). In the process of marine biofouling, microorganisms play an important role by inducing or inhibiting settlement and metamorphosis of invertebrate larvae and algal spores (Dobretsov et al., 2006). Both micro- and macrofouling in the world’ oceans cause huge economic losses in the maintenance of mariculture, shipping facilities, vessels, and seawater pipelines. Moreover, an increase in biofouling subsequently increases ship fuel consumption and causes an increase in the emission of CO2, NO2 and SO2 gases. Large-scale increase in the emission of such green house gases can lead to considerable environmental damage by fostering global climate changes (Qian et al., 2007).

Recent anthropogenically caused climate changes, which are only a fraction of predicted changes in the coming decades, have already triggered significant responses in the Earth’s biota. These climatic changes are mediated primarily by greenhouse gas emissions. Atmospheric greenhouse gases trap some of the heat energy that would otherwise reradiate to space, heating up the planet in the process (Fig. 1). Ocean warming results in ice melting and increase of freshwater input, affecting nutrient input and causing a decrease of salinity in coastal regions. Increasing temperatures affect atmospheric circulation, resulting in increased up and down welling and storm intensity as well as precipitation. It has been suggested that global warming also changes El-Nino and La-Nina-like conditions that have tremendous effects on marine life (Gorcau et al., 2005) and the earth’s climate (Hughes, 2003). An increase in atmospheric carbon dioxide (CO2) leads to an increase in its concentration in the oceans, where about 30% of modern CO2 emissions are stored. Continuous uptake of CO2 via the sea surface/ atmosphere interface is expected to decrease oceanic pH (Fig. 2). Decrease in pH will have a striking effect on marine calcifying organisms, while soft-bodied organisms may take an advantage of such changes. An increase in atmospheric CO2 will also deplete the ozone layer which will elevate UV radiation fluxes (Dobretsov et al., 2005; Dahms et al., 2011). The number of publications that investigate the effect of global climate change on marine communities is increasing. There are no publications about the expected effect of global climate change on biofilms (or microfouling) that cover all substrates in aquatic systems.

Fig. 1. Global warming caused by several anthropogenic activities [Credit: www.whoi.edu]

Fig. 2. Ocean acidification caused by several anthropogenic acids [Credit: www.whoi.edu]

Response of microbes to temperature and salinity

There is not much information about the effect of heat on biofouling species but it is likely that species living close to their thermal limit will be stressed and eventually die due to  global warming. It is also likely that cold-water biofouling species will be replaced by warm - water species. Global warming intensifies the frequency of El-Nino and La-Nina-like conditions, which will have a tremendous effect on marine ecosystems (Fig. 3). Elevated temperatures during La-Nina/ EI-Nino events severely affect coral reefs and cause coral bleaching and mortality (Hughes, 2003). On the contrary, other species such as shrimps and scallops reproduce and survive El-Nino events better. The flow anomalies during El-Nino events have resulted in anomalous northward transport of plankton by as much as 350 km/ month. This may lead to an increase in biological invasions of warm water species and a decrease in the number of cold-water species. Elevated temperatures increase growth and the photosynthetic rate of some harmful phytoplankton species. But El-Nino events result in a critical reduction of surface nutrients that are necessary for the phytoplankton growth and subsequently affect microbiota in their growth and blooming. Therefore, high intensity of El-Nino-like conditions in future will significantly change diversity and composition of marine communities including microbial communities. 

Elevated temperature

Elevated temperature can also accelerate the transmittance of diseases between species and increase the competition between species (Fig. 4). For example, the coral pathogen Vibrio shiloi invades the tissues of the host corals Oculina patagonica and causes their bleaching (Israel et al., 2001). Relatively higher water temperatures (about 28°C) will increase the infection rate by the pathogen, while low temperatures (about 16°C) will prevent bacterial growth. Thus, global warming may promote the infection of O. patagonica by V. shiloi which may significantly affect the distribution of this coral.

Salinity dilution

Global climate change resulting in ice melting and increase of freshwater input in coastal areas will lead to a decrease of salinity in shallow waters and can affect microbial consortia due to their differential sensitivity to osmotic stress (Fig. 4).

Response to CO2 and acidification

Due to anthropogenic activity CO2 concentrations in the atmosphere are increasing (Fig. 2). Because the oceans are in equilibrium with the atmosphere, the predicted increase of atmospheric CO2 concentrations is expected to increase CO2 concentrations in the oceans, despite the fact that elevated temperature and lower pH (associated with an increase of  atmospheric CO2) will decrease the solubility of CO2 in seawater. In any case, it is expected that over the next millennium, the oceans will absorb approximately 90% of the CO2 emitted to the atmosphere. Increasing CO2 concentrations in the marine environment are not expected to increase the productivity of marine algae. These are carbon-saturated and elevated CO2 concentrations are not likely to enhance their growth. CO2 dissolved in the ocean reacts with water to form carbonic acid resulting in ocean acidification. Reduction of pH due to an increase of CO2 concentrations will have profound effects on the physiological reactions of marine organisms. Experiments suggested that short-term elevations of CO2 resulted in reductions of protein synthesis and ion exchange in invertebrate cells.

Sea level rise and hydrodynamics

Intertidal areas may disappear by 20-70% over the next 100 years due to increased anthropogenic activity and because of a decrease of habitat availability. Since most biofouling species are fast growing on any anthropogenic structure, they will not be affected too much by sea level rises. Both negative and positive effects of sea level rise and hydrodynamics will affect the recruitment of species and will have a dramatic effect on biofouling communities, including microbial biofilms.

Fig. 3. Change of global oceanic circulation patterns [Credit: www.whoi.edu]

Fig. 4. Elements of a triangle model that demarcate environmental effects on biofilms that affect

larval settlement in marine substrata [after Qian et al., 2007]

Response to UV radiation

An increase of CO2 emissions will likely lead to further depletion of the ozone layer (Fig. 1). UVR affects primary producers by damaging organic molecules (DNA, RNA) and the inhibition of photosynthesis (Dahms et al., 2011). UVR has also an indirect effect on the recruitment of algal spores and invertebrate larvae, due to its effects on bacterial communities in biofilms, which in turn may influence the settlement of propagules (Qian et al., 2007). This will ultimately cause an alteration of species composition of biofouling communities.

Additionally, climate change may affect the interactions between biofouling species by changing competitor and predator-prey interactions. This includes climate driven changes in the abundance of species, which in turn affects species distribution, biodiversity, productivity, and microevolution. Global climate change can affect biofouling communities indirectly via the modification of chemical cues that are necessary for successful larval and spore settlement. It has been shown that microbial consortia in the form of biofilms are the major mediators of invertebrate larvae and algal spore settlement (Qian et al., 2007). Different species of bacteria, diatoms and fungi in biofilms can induce, inhibit or have no effect on larval and algal settlement (Dahms et al., 2006). The resulting effect of multi-species biofilms on larval settlement depends on species composition of biofilms and densities of different groups of microorganisms.  The same microorganisms are able to produce different secondary metabolites under the same culture conditions. For example, bacteria were inhibitive to the larvae of Balanus amphitrite at seawater salinities of 35 and 45 PSU, but induced their settlement at 15 and 25 PSU. Environmental changes can modify the density and the composition of microbial  communities, which in turn can change larval settlement. In the laboratory, larvae of different species responded differently to biofilms developed in different environmental conditions. Biofilms that were developing at relatively high temperature stimulated the settlement of the barnacle B. amphitrite. In contrast, the same biofilms had no effect on the larval settlement of the polychaete Hydroides elegans. These examples indicate that climate change may affect biofilm density, composition, production of metabolites and their effect on the recruitment of propagules, which will finally change the composition of biofouling communities (Dobretsov et al., 2006).

Directions for upcoming research

Microbial communities, besides other marine biota, are expected to show drastic changes in response to present and coming climate changes worldwide. Since studies on global climate changes on biofilms are rare, particularly in the natural environment, it will be necessary to investigate those effects in order to simulate their effects on natural biota as well as that in aquaculture or in anthropogenic systems. Elevated temperatures, low salinity, high wave turbulence and low pH due to increased CO2 concentrations are main factors associated with global climate change. Any of them, separate or in combination, will affect the development of biofouling communities (Fig. 4). Based on the analysis of available literature, we can assume that the most drastic changes in biofouling communities are going to happen because of elevated seawater temperature and decreased pH. Possibly, in polar and temperate regions, cold-water microbiota will be replaced by alien warm-water biota. Recently, biocides and antifouling compounds have been tested using single species of microbes (Dobretsov et al., 2006). To  predict changes in biofilms will, however, require the development of new bioassay techniques that include several target species from different phylogenetic groups. Replacement of cold-water strains and an increase of invasive warm-water strains due to global climate change will also affect the aquaculture of marine species. The aquaculture of shellfish, such as abalone, oyster, and mussel will be affected not only because of changes in their settlement but also by  pathogenic microorganisms in biofilms. In addition, UVR, acidification and elevated water temperatures affect resources of invading species. Such effects should be properly investigated  and future predictions and recommendations should be made. Marine organisms can respond differently to multiple stressors and the combined effect of two or more variables will be different from the effect of an individual stressor (Dahms et al., 2006). The impact of one factor can either be strengthened or weakened by another factor and the combined effect of two and more stressors may push an individual beyond a threshold that would not be reached by a single stressor. For example, high levels of UV radiation have no effect on the survival of algal spores in warm water, while spores died in treatments with high levels of UV radiation in cold water (Dahms et al., 2011). Since the majority of global change studies deal with a single stressor, it will be necessary in future studies to include effects of multiple stressors associated with global climate change on biofouling communities. Such factors may not only affect microbial consortia but also other biota that are influenced by them. Susceptibility of biofouling organisms to biocides may change due to climate change. Elevated CO2 reduces the tolerance limits of marine organisms to certain biocides via the depression of important physiological pathways. Elevation by 5-10°C of water temperature increases the respiration of microorganisms and their sensitivity to copper. In addition, global climate change can have both direct and indirect impacts on assemblages in biofilms. Composition of microbial biofilms and their production of chemical cues can vary at different environmental conditions (Qian et al., 2007). Therefore, larval and algal spore settlement on biofilms will be affected by global climate change. Due to the lack of appropriate cues, the density of some biofouling species will become low, while other species will dominate biofouling communities. Changes in microbial biofilms may finally affect the entire composition of  biofouling communities. Overall, it seems that global climate change will seriously affect the productivity, development, dynamics, and composition of biofouling communities. Future studies should focus on the impact of climate change on biofouling species, populations and communities and will require multidisciplinary approaches.

References

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