This indicator is a HELCOM supplementary indicator and is applicable in assessment units shared by Finland and Sweden.
The status of hazardous substances is assessed using several core indicators. Each indicator focuses on one important aspect of the contaminant distribution, levels and effects. Currently, this biological effect indicator is not integrated to the overall assessment of contamination status; however it provides supplementary information and should be considered together with other hazardous substances core indicators in order to evaluate the overall status of hazardous substances in the Baltic Sea.
The marine environment is the ultimate repository for complex mixtures of persistent chemicals. Consequently, organisms are exposed to a range of substances, many of which can cause metabolic disorders and, may affect populations through changes in growth, reproduction, and survival. The perturbations of species or communities as a consequence of exposure to hazardous substances is a prerequisite for environmental quality assessment. A reproduction indicator is important to assess integrated effect of bioavailable contaminants in the environment with strong repercussion at the population level. This goal is included in the BSAP (Concentrations of hazardous substances are close to natural levels) and MSFD (descriptor 8.2). Many effect variables (indicators) are not specific and respond to various environmental stressors. 'Malformed embryos' is an indicator that is comparatively specific and responds mainly to the contaminant exposure.
The amphipod Monoporeia affinis is a keystone species in the Baltic Sea and freshwater ecosystems below the highest coastline. It is one of the most abundant macrofauna species in soft bottoms (10 to 150 m) in the Gulf of Bothnia and the Baltic Proper, provided that oxygen conditions are sufficient (Kuparinen et al. 1996). Amphipods are very important for the oxygenation of the sediment by bioturbation (Lindström 1992), they are also food for fish, such as herring, eelpout, cod and flounder, as well as other invertebrates i.e. Saduria entomon, Halicryptus spinulosus and Bylgides sarsi (Ankar and Sigvaldsdottir 1981, Aneer 1975, Sparrevik and Leonardsson 1995). The Baltic M. affinis populations have decreased dramatically during the last 30 years, and currently the species is nearly absent in the Gulf of Finland and Gulf of Gdansk. The population crash in the year 2000 resulted in dramatically decreased populations in the Gulf of Bothnia (Eriksson Wiklund et al. 2008). Other amphipods used in the monitoring (P. robustoides, G. tigrinus, G. fasciatus) belong to so-called alien species, but they are also important components (30-40% of the total biomass) in the benthic communities in coastal areas of the Baltic Sea (Gulf of Riga, Gulf of Finland, Curonian and Vistula Lagoons) since 1990s and are the main prey for local fish and birds. These species are omnivores, with more than 50 % of detritus in their diet (Berezina 2007). These gammarids are widely used as test indicators for sediment toxicity (Berezina et al. 2017; Strode et al. 2017). All of them have a life span of 1.5 year; mating begins in April-May, embryogenesis takes 2-3 weeks, and juveniles of the 2-3 generations are released during summer (Panov and Berezina 2002; Bacela and Konopacka, 2005, Berezina et al. 2011).
Amphipod embryos are sensitive to sediment toxicity during the embryogenesis and various embryo aberrations can occur in response to toxic exposure. The reproductive endpoints, including embryo development are sensitive to various stress factors, including pollution. Moreover, frequency of malformed embryos is more sensitive to contaminant exposure than other reproduction variables, such as fecundity, sexual maturation and fertilization rate (Sundelin, 1983; Sundelin and Eriksson, 1998). In bioassays, exposure of M. affinis to metals (e.g., As, Cd, Pb) and sediments collected nearby pulp mill discharges caused higher frequencies of malformed and membrane-damaged embryos compared to reference sediments (Sundelin, 1983, 1984, 1989; Blanck et al., 1989; Wiklund et al., 2005).
All amphipod species have a similar embryo development and the method proposed here is applicable to all species. Embryo aberrations (see Table 2 in Löf et al. 2015) are classified as: (1) malformed embryo, with aberrant morphology of extremities and body symmetry (Malf), (2) embryo with damaged membrane (Membr); (3) embryo with arrested development (AD) and (4) dead or partially dead broods (DB). Categories 1 to 3 were found to be most representative of contaminant-induced developmental toxicity and these are the categories used under collective name malformed embryos in the indicator assessment.
The indicator is mainly sensitive to the effects of contaminants, i.e. trace metals and hydrophobic persistent organic contaminants (PHOCs). A metadata analysis for Monoporeia affinis at 42 sites in polluted coastal areas was used to assess the correlation between malformations and industrial waste waters. A significant relationship was found between distance to industrial outlet and malformation rate (Reutgard et al. 2014), confirming earlier studies and linking malformations to in situ exposure (Elmgren et al. 1983, Sundelin and Eriksson 1998, Sundelin et al. 2008b).
Different embryo malformation types arise in the xenobiotic-exposed females. Moreover, some types of embryo aberrations were significantly associated with specific contaminant groups in the sediment (Löf et al. 2015). In particular, occurrence of females with embryo limb malformations was strongly related to elevated concentrations of Cd and PCBs, while females with membrane-damaged embryos occurred at high PAH concentrations. Also, frequency of embryos with arrested development was higher at elevated concentrations of PAHs and metals. Thus, these reproductive aberrations in M. affinis can serve as contaminant-specific indicators of PCB, PAH and heavy metal exposure in biological effect monitoring. Moreover, such aberrations as dead broods and dead eggs may indicate exposure to low oxygen concentrations during the oogenesis (Eriksson-Wiklund and Sundelin 2001, 2004). Whereas a combination of oxygen deficiency and contaminants has been observed to enhance contaminant toxicity (Gorokhova et al 2013), the oxygen deficiency as a sole factor does not give rise to malformed embryos. Food deficiency may also result in low fecundity and arrested development (Sundelin et al. 2008a), but not in other malformation types. More work is, therefore, needed to unambiguously link specific malformations to xenobiotic compounds or contaminant classes in various environmental setting.