Nematodes have been used widely to evaluate soil conditions in agriculture and as long-term indicators of pollution and climate change. The nematode assemblage-level approach to the detection and monitoring of oil pollution effects has been validated in experimental microcosms (Beyrem et al. 2010) and in field studies (Lindgren et al. 2012). In our study, Bunker fuel oil decreased abundance, richness and number of species of natural populations of nematodes from a mangrove ecosystem. Several other studies also reported that oil decreases nematode abundance and species richness, alters community composition and reduces biodiversity (Lv et al. 2011; Beyrem et al. 2010). Little information is available on nematodes in the upper‐littoral zone where mangroves occur. Upper‐littoral zones are rarely sampled, so that composition of species that occur is largely unknown. Furthermore, estuarine nematodes are dispersion‐limited, so that their occurrence is primarily influenced by local and regional environmental conditions (Brustolin et al. 2018).
Oil contamination may increase, decrease or eliminate meiofaunal communities (Mahmoudi et al. 2005; Beyrem et al. 2007; Kang et al. 2016). Most studies reported a reduction in the population of meiofauna immediately following an oil spill. In other studies, benthic communities responded positively and showed no oil-induced mortality (Kang et al. 2014). Factors that could contribute to differential effects of oil on nematode communities include type of oil and dosage, morphological and physiological differences of the nematode taxa and soil conditions (Mahmoudi et al. 2005; Thompson et al. 2007). Oil induced changes alter nematode community composition and reduce biodiversity (Beyrem et al. 2010). In addition, some nematode communities that occur in oil contaminated environments tend to become more oil tolerant over time (Carman et al. 2000).
Oiling and nematode community structure
Nematode assemblages in marine sediments are generally resistant to environmental changes. In our study, oiling decreased nematode abundance and species richness significantly. Nematodes are particularly sensitive to PAHs because of their intimate association with soil particles (Lindgren et al. 2012). Nematodes possess permeable cuticles and lack a protective calcium or silicate casing making them vulnerable to oil penetration (Stringer et al. 2012). Other meiofauna, such as copepods, are more resistant as they possess protective casings. PAHs, which are non-polar and lipophilic, diffuse passively across exposed nematodes membranes (Gauthier et al. 2014). Within the cells, PAHs increase expansion and fluidity of nematode membranes thereby disrupting membrane integrity, cellular function and causing mortality. PAH disruption of cell membranes leads to breakdown of ion-selective barriers, leading to loss of water and salt regulation (Stringer et al. 2012). PAH-induced damage to membranes also contributes to greater sensitivity of nematodes to soil salinity. Furthermore, nitrogenous wastes, which are usually excreted by diffusion through the outer membrane, tend to accumulate in damaged cells, contributing to waste build up and toxicity. For example, benzene increased membrane fluidity in the bacterium, Rhodococcus sp. (Gutierrez et al. 1999). In the mussel, Mytilus edulis, benzene disrupted ion transport and decreased calcium concentrations (Borseth et al. 1995). Furthermore, PAHs which are cytotoxic, cause intracellular damage by preventing the synthesis of proteins that are important for cellular repair and survival (Liuzzi et al. 2012).
In our study, four species of nematodes decreased with oiling (Hemicycliophora ripa, Panagrolaimus sp., Camacolaimus sp. and a species of the Xyalidae). In several other studies, nematode abundance and species richness also decreased when sediment was contaminated with diesel (Lindgren et al. 2012), crude oil (Lv et al. 2011) and lubricating oil (Beyrem et al. 2010). In the sediment, PAHs decrease dissolved oxygen concentrations leading to oxygen stress in nematodes (Carman et al. 2000; Neira et al. 2001). In low oxygen environments, nematode activities such as sediment bioturbation and recycling of organic matter are decreased (Neira et al. 2001; Sundbäck et al. 2010). Other studies showed that addition of the PAH, pyrene, to sediment decreased grazing activity of nematodes (Sundbäck et al. 2010). Reduced grazing activity decreases sediment bioturbation leading to increased soil anoxia (Lindgren et al. 2012). Soil anoxia, induced by oiling, probably contributed to the decrease in abundance and species richness in our study. Oil contamination of the sediment therefore altered nematode community structure, reduced competition and favoured resilient species.
Oil has been shown to enhance the retention of toxins such as heavy metals (Millward et al. 2004). Combination of heavy metals and PAHs therefore further reduce nematode assemblages (Beyrem et al. 2007). In addition, PAHs promote the growth of microalgae which produce mucous exo-polymers. The latter adsorb heavy metals that are present in the sediment, and when consumed, result in greater toxicity to nematodes (Carman et al. 2000). Nematode species vary in their sensitivity to PAHs at sub-lethal concentrations (Carman et al. 2000; Millward et al. 2004). Species that are sensitive decrease with oil contamination (Sundbäck et al. 2010; Lindgren et al. 2012). The elimination of sensitive species by oil was reported in several studies (Mahmoudi et al. 2005; Beyrem et al. 2010; Lv et al. 2011). PAHs are neurotoxic and adversely affect the nervous system of nematodes (Meyer and Williams 2014). PAHs interfere with locomotion, feeding behaviour, brood size, growth, life span and ultimately lead to mortality (Meyer and Williams 2014).
In this study, Ethmolaimus sp. and Camacolaimus sp. were dominant and resilient to oiling. Camacolaimus sp. increased in the O treatment by 78% compared to the C treatment and were characterised as opportunistic (Millward et al. 2004; Mahmoudi et al. 2005). Oiling increased robust and opportunistic species, enabling them to become dominant. Oiling reduced nematode competition and favoured resistant species. In this study, oiling changed the abundance of dominant species and altered nematode community structure.
In the O treatment, Camacolaimus sp.exhibited the highest juvenile abundance, indicating that this species is highly tolerant and resilient to oil contamination (Mahmoudi et al. 2005). In contrast, juvenile abundance of Monhystera sp. was highest in the C treatment and decreased significantly in the O treatment suggesting that reduction in reproductive capacity affects community structure by changing species dominance (Beyrem et al. 2010). In terrestrial and marine environments, hydrocarbon degrading microorganisms that are capable of metabolizing oil compounds are ubiquitous (ITOPF 2014). In this study, it was assumed that these microorganisms increased in the sediment of oil treated microcosms. Degradation of PAHs occurs at different rates and is dependent on the structure of the PAH and the species of microorganisms.
Oiling with fertiliser amendment
The addition of fertilisers to oil contaminated sediment is effective in bioremediation. Fertilisers provide sources of energy for PAH degrading microorganisms. Nutrient addition accelerates the degradation process in mangrove sediments (Xu et al. 2005). Generally, the addition of fertiliser to oiled sediments increases nematode abundance and species richness significantly (Eisentraeger et al. 2002). In our study, three genera (Rhabditis, Koerneria and Rotylenchus), which were absent in the O, but present in the O+F and C treatments, were characterised as oil-sensitive. Survival of these species was attributed to the addition of fertiliser. The addition of fertiliser also increased nematode abundance of Ethmolaimus sp. and Camacolaimus sp. Furthermore, the addition of fertiliser increased reproduction in Camacolaimus sp. In our study, addition of fertilizer increased the abundance of dominant and opportunistic species. Fertiliser additions also increased oil decomposition rate of microorganisms by stimulating bio-degrading bacterial activity, which in turn elevates N and P concentrations in the interstitial water (Xu et al. 2005).
Juveniles of the genera, Rhabditis and Rotylenchus were absent in the O but present in the O+F treatment, suggesting that reproduction was stimulated by fertiliser addition. In the O-F treatment, Camacolaimus sp. exhibited the highest juvenile abundance which suggests opportunistic behaviour. In the O+F treatment, there were no differences in juvenile abundance of five species. Similar results were reported for juvenile abundance of nematodes in fertilised, oiled treatments in field mesocosms (Schratzberger et al. 2003). Lubricating oil decreased the abundance of dominant nematodes in oiled treatments resulting in decreased competition (Beyrem et al. 2010). In the O+F treatment, the decrease in juvenile abundance of Ethmolaimus sp. contributed to the increase in oil-sensitive species through reduced competition.
The food sources of nematodes, which include bacteria and microalgae, are negatively affected by oil contamination. The addition of fertiliser to oiled sediment increases resilient microalgae and bacteria, which provide a food source for oil-resistant nematodes (Sundbäck et al. 2010). In this study, most nematode taxa were bacterivores, but plant parasites and one predator (food consists of algae, diatoms, and small animal such as ciliates and rotifers) were also encountered. Other studies demonstrated that bacterivorous nematodes proliferated in soils contaminated with PAHs probably due to increased microbial activity and availability of food (Chen et al. 2009). Long-term studies showed that burrowing and bioturbating amphipods increased the availability of microalgae which in turn increased densities of nematodes, copepods and juvenile polychaetes (Fleeger et al. 2021). Desmodora sp. was present in the O+F but absent in the O and C treatments, suggesting that this species is tolerant to oiling if fertiliser is present. Although microcosms of natural nematode assemblages do not mimic natural conditions, the observed responses provide insight into the complex effects of oil contamination on natural meiofaunal communities. Moreover, toxicity of PAHs depends on their partitioning between the sediment, pore water, overlying water and sediment carbon.