The transfer of exogenous species across habitats and geographical regions may result in the alteration of ecosystem functioning with a loss of biodiversity, and social as well as economic impacts that may be drastic and irreversible. Although only 10% of exogenous species are prone to become invasive, sensu Boudouresque and Verlaque (2002), the rate of transfer is increasing with the increased shipping activity worldwide. The main anthropogenic activities recognized as directly responsible for the transfer of aquatic species are aquaculture and aquarium trade that sometimes transfer species deliberately, and shipping that may inadvertently transfer species with ballast water (BW) (Gollasch 2007).
Shipping remains the main mode of transport of goods across large distances and is a vector of aquatic organism transfer through BW exchanges and fouling on the ship hulls. Over the last decades the industry has grown approximately 3% per year (in million tons loaded) (see Figure 1.3, UNCTAD 2012). Following this exponential growth, the shipping industry is expected to double in magnitude in 22 years; therefore, the threat from aquatic invasive species on ecosystems is projected to increase. Involved stakeholders have identified BW management and BW treatment as essential practices for the protection of the aquatic environments. The International Maritime Organization (IMO) has developed a legal regime to regulate and control BW and the International Convention for the Control and Management of the Ships' Ballast Water and Sediments was adopted in February 2004 (IMO 2004). The convention will enter into force exactly 1 year after at least 30 states representing 35% of the world merchant tonnage will have ratified the convention. To date 36 states, representing 29% of the world tonnage, have ratified the convention (http://www.imo.org/About/Conventions/StatusOfConventions/Pages/Default.aspx). Briefly, once the convention enters into force, ships discharging BW will need to meet the BW performance standards (Regulation D-2). These standards require that BW tanks contain less than:
- 1.A total of 10 viable organisms × m−3 (with a minimum dimension of ≥50 µm)
- 2.A total of 10 viable organisms × mL−1 (10 µm ≥ size range <50 µm)
- 3.A total of 10 cfu × L−1 of Vibrio cholera
- 4.A total of 2500, cfu × L−1 of Escherichia coli
- 5.A total of 1 cfu × mL−1 of intestinal Enterococci
It is expected that most ships will meet these standards by installing an onboard ballast water treatment system (BWTS). However, to test promising treatment technologies (Regulation D-4), ships participating in a program approved by administration (IMO) may not have to comply with the regulation D-2 standards for a period of 5 years from the date of installation of this treatment technology on-board. Also, depending on the BW volume, a ship may adhere to the 95% ballast water exchange at sea (Regulation D-1) for a few more years but will eventually have to reach D-2 standard at a later stage.
To ensure treatment efficiency and the safety for the crew, the ship, and the environment, BWTS developed worldwide must be tested and approved by member states according to guidelines developed by the IMO during land-based and shipboard tests (Regulation D-3—Approval requirements for ballast water management systems) [IMO 2004] and G8 and G9 guidelines [IMO 2008a, 2008b]). These guidelines specify, for example, the test water quality requirements (e.g., minimum density of organisms, TSS, DOC, and salinity ranges). It also includes a mandatory duration of the land-based test (at least 5 days) to ensure that the reduction in the number of organisms is due to the efficacy of the BWTS rather than other factors. It also provides sufficient time for an eventual regrowth of organisms. Considering that land-based testing facilities are located in different parts of the world, and the world maritime traffic involves regions situated at different latitudes with variable water temperatures, it is crucial to understand the influence of temperature on the approval of a BWTS. Nonetheless, the IMO guidelines for testing and approval of BWTS (IMO 2008a, 2008b) do not require taking into account water temperature differences among testing sites and seasons.
In this article, we discuss how temperature affects the fate of organisms in a BW tank and the efficacy of chemical treatments. We further show how temperature can bias the results of BWTS tests and render them incomparable if not taken into account. Finally, we propose to use a reference temperature and a Q10 value to enable comparison between tests and improve the reliability of the application of the Regulation D-3 from the convention.
Effects of temperature on the biological responses of planktonic organisms in ballast water
The composition, abundance, and physiology of plankton communities are strongly linked to water temperature (Ikeda 1970; Vidal 1980; Rose and Caron 2007). Together with salinity and hydrostatic pressure, it is probably the most important physicochemical variable structuring marine ecosystems. The higher reactivity of molecules at higher temperature increases the overall speed of biochemical reactions, causing changes in vital rates such as, but not limited to, hatching time and grazing rates. Nevertheless, all vital rates measured on organisms are not affected similarly (Foster et al. 2011).
The influence of temperature on vital rates of plankton is often reported using Q10 values. Q10 is the factor of increase in the rate of a given reaction/vital rate for each 10° C increase in temperature:
Where R1 is the vital rate measured at temperature T1 and R2 is the vital rate measured at temperature T2 (T2 > T1).
Q10 values for different processes are abundant in the literature for most plankton taxa as for example bacteria (Bronikowski et al. 2001), phytoplankton (Foy and Gibson 1993), crustaceans (Dam and Peterson 1988; Hirst and Bunker 2003), ciliates (Fenchel and Finley, 1983; Nielsen and Kiørboe 1994; Chen et al. 2012), rotifers (Montagnes et al. 2001), jellyfishes (Moller and Riisgard 2007), appendicularians (Lombard et al. 2005), and foraminifers (Lombard et al. 2009). However, in the natural temperature ranges of organisms, the Q10 is very predictable, typically ranging between 1.5 and 3.
Effects on size of organisms
As a direct effect of a mismatch in the temperature dependence of growth and development, the size of the organism at a particular developmental stage is affected. Most of ectotherm organisms fall into the temperature–size rule (TSR), exhibiting smaller body sizes at warmer temperatures. In crustaceans, both eggs and adults decrease size with increasing temperature (Heinle 1969; Uye and Fleminger 1976; Hansen et al. 2010). Although the TSR is mainly true as a within-species rule and would in our case only affect the results of tests between seasons, there is also a general increase in the size of organism along a latitude gradient (Atkinson and Sibly 1997; Hillebrand and Azovsky 2001), with larger animals found in higher latitudes. Taking into account the effect of temperature on organism size, the size limits set by Regulation D-2 could be contested. In fact, some organisms with size ranges close to these limits could fall into one or another size class depending on the temperature at which a BWTS is tested. Small copepod eggs, for example, may be accounted for in the 10 to 50 µm size class in warm waters whereas they may be considered in the greater than or equal to 50 µm size class in colder waters. As the IMO D-2 discharge standard has a factor of 106 in the difference between these 2 sizes fractions, small size copepod eggs are more likely to be ignored in warm water compared to cold waters. Some phytoplankton may not even be considered when analyzed in warmer water as they may fall below the lower limit of 10 µm in minimum dimension—whereas they would be considered in colder waters.
Effects on decay of phytoplankton
High temperature may also affect the mortality rates of phytoplankton in dark BW tanks as they naturally exhibit a higher metabolism at higher temperature (Robinson and Williams 1993). Phytoplankton mortality in closed system such as a BW tank can be indirectly measured by a decrease of chlorophyll a over days of voyage (Drake et al. 2002). When combining the higher natural mortality of phytoplankton and the increased grazing pressure from micro- and mesozooplankton at higher temperature, it is obvious that the number of organisms in the 10 to 50 µm size class will decrease faster at warmer temperatures than in colder temperatures. This eventually results in less viable organisms than mandatory in control tanks after the required 5 days of retention, potentially making tests invalid under the actual guidelines (10 times the D-2 standards is required at discharge in the control tank).
Effects on egg hatching
Eggs of plankton can be an important vector of transfer of aquatic invasive species (Briski et al. 2011). Because of the extreme difficulty to assess the viability of plankton eggs (eggs may hatch over months even in optimal conditions) (Drillet et al. 2011) and the effects of temperature on their hatching time and success (Hansen et al. 2010; McLaren et al. 1969), temperature effects on egg viability and hatching are also of concern, and the efficacy of a BWTS on this vector may therefore not be adequately addressed when testing in cold waters. In addition, at cold temperatures, some eggs (if present) may be produced as resting eggs, and eventually may die if not transferred under suitable temperature conditions (Drillet et al. 2008, Hansen et al. 2010). The effect of temperature on egg development must be accounted for when assessing the efficacy of BWTS to ensure comparability between results and/or facilities.
Effects on chemical treatment of ballast water
The positive effects of increasing temperature on the efficacy of conventional disinfection processes such as ozonation, chlorination, and ultraviolet treatment are well documented (Weber and Levine 1944; Abughararah 1994; Hirata et al. 2001). Most BWTS using active substances for disinfection will dose a neutralizing agent before discharging water back to the sea to remove any residuals of the substance. With the faster decay of the substances in warm waters (Rocarro et al. 2008), a neutralizing agent may hardly be required in warmer regions, whereas it may be a necessity in colder waters. BW treatment protocols must therefore take temperature into account before discharging water at destination. Temperature also affects the formation and decay of disinfection byproducts (DBP) and their assessment by BW test facilities (Rocarro et al. 2008).
Under the D-3 Regulation, BWTS making use of active substances must undergo an environmental risk assessment as part of the final approval process, including an assessment of the environmental risk of DBP concentrations and remaining toxicity at discharge (after 5 retention days). However, a test facility may not detect any toxicity effects caused by the active substance itself on test organisms in warm waters, whereas these effects could still be present after 5 days retention time in colder water. In other cases the higher DBP levels found in warmer waters may cause additional toxicity. This is of concern, as it implies that technology developers using active substances may have an easier or tougher route towards type approval when testing in warm water than in colder waters depending on the type of active substance used (under the actual guidelines).