Tilapia occur in more than 100 countries outside of their native range after tilapia has been introduced with joy for more than 60 years (Esselman et al. 2013). In 2014, tilapia was officially listed as one of the world's top 100 invasive species in the list of non–native invasive species in China (the third batch). In the present study, we found that tilapia invasion decreased the mean estimated trophic position of native top fish predators. Our analysis clearly demonstrated that this decrease in trophic position was solely due to the decline in prey fish biomass associated with tilapia invasion.
Tilapia have a preference for the same type of habitat as native fish and so the presence of tilapia displaced native fish from their preferred habitats. Tilapia invasion can reduce local biodiversity and result in the extinction of native fish species due to competitive replacement (Starling et al. 2002; Figueredo & Giani 2005). Therefore, the establishment of tilapia has detrimental effects on aquatic food web structure in native habitats (Martin et al. 2010; Attayde et al. 2011; Russell et al. 2012). Fishes which are adapted to consume a diversity of foods often change their diets to overcome increased competition for food following species invasions (McMeans et al 2016; Wainright et al. 2021). These diet changes, such as switching from a specialist to a generalist diet or eating insects instead of fish, are reflected in the trophic structure of food webs.
This is the first study to clarify how the invasion of tilapia affects the feeding habits and trophic position of native species. There was strong evidence of a shift in diet composition and a decline in the trophic position of top fish predators in the invaded Dongjiang River related to changes in prey availability. The trophic position of culter fish, mandarin fish, and catfish in the invaded Dongjiang River, was significantly lower than in the reference Beijiang River. The diet of culter fish shifted from small fish (32.7% small fish, 17% zooplankton) to zooplankton (36.3% zooplankton, 25.5% small fish) in the invaded river. The diet of mandarin fish shifted from small fish (46.7% small fish, 10.4% aquatic insects) to aquatic insects (20.3% aquatic insects, 29.9% small fish) in the invaded river. The diet of catfish changed from fish eggs (25.1% fish eggs, 24.8% aquatic insects) to aquatic insects (43.5% aquatic insects, 4.8% fish eggs) in the invaded river.
This dietary shift was accompanied by a prolonged reduction in the abundance of native fish species. The sampling data showed that the relative densities of native prey fish decreased significantly over time in the invaded Dongjiang River. There has been a great deal of evidence to show that the increase of tilapia in rivers affects the CPUE of the fish community and native fish species (Gu et al. 2015), including the most abundant native species mud carp (Cirrhinus molitorella), black amur bream (Megalobrama terminalis), barbel chub (Squaliobarbus curriculus) and common sawbelly (Hemiculter leucisculus) (Shuai et al. 2019). The larvae of these fish are an important food source for top predators. A significant reduction in the CPUE of other commercially important species was also observed after the introduction of Nile tilapia in the North–eastern Brazil reservoir (Attayde et al. 2011). There is substantial overlap in diet between tilapia and native fishes in most tropical and subtropical habitats (Henson et al. 2016). In the current study, which spanned 9 years in the Pearl River, native fish densities decreased with increasing tilapia density. In particular, a progressive decrease in body size, such as fish plumpness, body length, and body weight, of native fishes coincided with the increasing prevalence of Nile tilapia (Shuai et al. 2019), and increased competition from Nile tilapia with local native species for food resources.
Trophic position stability is considered to be an important variable in the structural stability of food webs (Rennie et al. 2011; Thomsen et al. 2014). Analyzing trophic position variation can be helpful in detecting the effects of invasive fish species on the structure of food webs and understanding subsequent impacts on ecosystem functioning (Cardinale 2012; Thompson et al. 2012). Stable trophic positions of predators and prey are one component of stable food webs (Johnson et al. 2014), while trophic dispersion implicitly involves variability in trophic position. Tilapia invasion induced significant trophic dispersion, thereby disrupting trophic positions and destabilizing food webs in the Pearl River. We found that native top fish predators increasingly relied on zooplankton and aquatic insects as invasion progressed, which may have destabilized food webs and promoted their transition to tilapia dominance. Indeed, food web instability is a precursor to ecological state change (Rooney and McCann 2012), and biological invasions are known to yield alternative ecological states (Scheffer and Carpenter 2003), it is likely that these food web changes ultimately produced a new ecological regime (Wainright et al. 2021).
We found that invasive tilapia forced other fishes to increasingly rely on zooplankton and aquatic insect resources in the tropical river. These results demonstrated how invasive tilapia initiated disruption of native food webs via trophic displacement, and the study provided clear evidence that invasive predators can influence the dominant energy pathways of native predators, ultimately destroying ecosystem stability. The results of this study provided a basis for understanding and predicting the directional effects of invasive species on recipient food webs. Trophic changes due to fish invasion can also exhibit biotic homogenization with trophic downgrading (Singh 2021). For example, the invasion of lake trout (Salvelinus namaycush) increased fish diet variability, disrupted food webs by reorganizing macroinvertebrate communities, and displaced native fishes from their reference diets in the northern Rocky Mountains, USA (Wainright et al. 2021). The invasion of Dreissenid mussels, including the zebra mussel (Dreissena polymorpha) and quagga (Dreissena rostiformus bugensis) in the Great Lakes, caused commercially harvested native whitefish (Coregonus clupeaformis) to become more reliant on nearshore benthic production, changing the fundamental energy pathways in the lakes (Fear et al. 2017).
Therefore, the invasion of tilapia is bound to have a serious impact on the trophic position of native fish populations, and the negative impact of tilapia on native fisheries and ecosystems in southern China should not be underestimated. Protecting native fish populations often involves stopping the intentional introduction of non–native fish. The potential damage associated with invasive species has prompted recent efforts to predict the vulnerability of ecosystems to species invasions and prioritize them for management (Strassburg et al. 2020; McDonald–Madden et al. 2016). Ultimately, protecting entire landscapes from biological invasions may be required to sustain native biodiversity and ecosystems. This strategy may require stopping the introduction of invasive species, including non–native fish–stocking programs, and using innovative bio–surveillance monitoring techniques, such as environmental DNA (Evans et al. 2017), for early detection of potential invaders.
However, tilapia plays a very important role in the international market, ranking second in the global freshwater fish trade, second only to salmon and trout. Tilapia is one of the most internationally competitive aquaculture varieties in China, and it is also the species with the most potential for industrial development (Yao and ye 2014). In 2020, the global culture output of tilapia reached about 6.93 million tons. The huge demand for tilapia in the international market has further expanded the breeding scale of tilapia in China. The production of tilapia in aquaculture in China reached 1.66 million tons in 2020 (Fisheries and Fishery Administration Bureau of Ministry of Agriculture 2021). For many years, China has been the world's largest tilapia producer and leading tilapia exporter (more than 60% of global tilapia exports), exporting to 80 countries or regions every year (Liao et al. 2020).
In spite of available regulatory approaches and guidelines to manage aquatic invasive species, fish invasions are increasing. The importance of the tilapia breeding industry, makes it difficult to control tilapia invasion, and it is neither realistic nor desirable to completely eradicate tilapia. To date, at least 10 tilapia species have been recorded in China, including New tilapia zillii, tilapia zillii, Mossambica tilapia (Oreochromis mossambicus), Nile tilapia (Oreochromis niloticus), Fushou tilapia (Mossambica tilapia × Nile tilapia), aureus tilapia (Oreochromis aureus), O'nei tilapia (aureus tilapia × Nile tilapia), blackchin tilapia (Sarotherodon melanotheron), Sarotherodon galilaeus and Tilapia rendalli (Yao and Ye 2014). As a result, feral tilapia have hybridized and introgressed in aquaculture settings before escaping to the wild. Reproductively viable hybrids have resulted, facilitating tilapia invasion. In order to better develop the aquaculture industry, germplasm improvement of tilapia is progressing rapidly. It is fairly well understood that hybrids, mixed hybrids and breeding, will lead to a general invasion success for most tilapia species. Therefore, after the serious ecological consequences caused by tilapia, the prevention and control of tilapia invasion is still a difficult problem.
In recent years, local governments have invested a lot of human and financial resources to protect and repair of the decline of fishery resources in rivers, such as annual proliferation and release activities, but these attempts have not been particularly successful. This was largely due to a lack of understanding regarding the mechanisms driving the decline in fishery resources. The results of the current study provided an initial insight into the decline of fishery resources in the Pearl River following tilapia invasion. At present, the most effective way to prevent invasion impacting fishery resources in the Dongjiang River is to be stringent regarding environmental isolation in pond culture, avoiding tilapia for release activities, and strictly controlling the growth range of this species. More stringent regulation of aquaculture activities and proactive fisheries management are required to avoid additional releases and further spread of tilapia in the region.
Understanding the consequences of invasive species on ecosystem functioning through changes in trophic interactions among species has received considerable interest over the past decade (Thébault 2003). Most of these studies have used stable isotopes to quantify changes in the trophic structure of communities (Cucherousset et al. 2012), as carbon (δ13C) and nitrogen (δ15N) can provide an accurate quantitative method for the study of the changes of nutritional structure in aquatic ecosystems (Bearhop et al. 2004). Recent methodological developments have facilitated the quantification of multiple facets of the trophic structure of communities, such as isotopic diversity metrics, i.e. trophic niche width (TA), isotopic richness (IRic), isotopic evenness (IEve), isotopic divergence (IDiv), isotopic dispersion (IDis), and isotopic uniqueness (IUni) (Jackson et al. 2011; Cucherousset and Villéger 2015). These metrics were widely used to assess the effects of biological invasions on a multitude facets of food webs and ecosystem functioning at both local and global scales (Zambrano et al. 2010; Walsworth et al. 2013; Spurgeon et al. 2014; Sagouis et al. 2015).
While theoretical and methodological approaches have been recently developed, empirical studies are still needed to assess the effects of biological invasions on the trophic structure of recipient communities. The changes in food webs described in the current study have serious implications for native fish populations and food resources. An increased understanding of the interactions between tilapia and native fish is necessary for fishery management in many regions. Our findings emphasized the need to implement proactive control efforts to restore invaded ecosystems, particularly during colonization and early stages of establishment, to avoid food web disruptions that may be difficult to reverse. As tilapia is a commercially important species, its introduction cannot be banned, and so the strictest supervision of this species is required.