The Ner River has been for decades the major route of disposing sewage and storm water from the Łódź City, a million people municipality located on the upper course of the river24. The improvement in water quality, and resulting fish recovery in the Ner, which are described in this study, was a consequence of two major processes that began in the early 1990s. Both these processes were management measures undertaken as part of the preparation for Poland’s accession to the European Community (now European Union), which took place in 2004. One of the processes was the liquidation of textile industry in the Łódź City, once one of the greatest textile production centers in the world24. The other of the processes was the modernization of agriculture and construction of numerous sewage purification stations in the Ner catchment, which took place over the 1990s and 2000s. The most important of the stations was the huge Łódź City Sewage Treatment Plant (STP), whose first part was launched in 1994. By 1995 all sewage disposed to the Ner (which was 3–4 m3/s) had been mechanically treated, by 1998 half of it had also been biologically treated, and since 2001 all of it has been biologically treated24, although the STP was further modernized in the whole 2000s. As a result of the above processes, oxygen content or transparency of the Ner River water much increased, while the load of nutrients or heavy metals much decreased in the study period.
There were three things that were essential for obtaining the significant fish analysis results that are presented above. One of them was frequent fish monitoring, which consisted of seven surveys. If the number of surveys over the period of 2000–2012 had been lower, say two or three, the intimate relation between Prussian carp and ide, for example, would not have been noticed, because no useful regression model could either be constructed or be significant. Such frequent monitoring as ours was exceptional in the early 2000s in Poland, and this is probably why the relation between the two fish species had not been detected before our study.
The frequent sampling was also little biased. Electrofishing, which was used in the surveys, might be reliably applied owing to several factors. Firstly, the recovered course was of slow water current, which resulted from a 17 m difference in elevation (and thus a 0.43‰ slope) between the upstream and downstream ends of the course. Such slow current made drifting of stunned fish too fast to be captured impossible. Secondly, turbidity which obstructs discernment of stunned fish, was low. Thirdly, conductivity was very stable, only once slightly exceeding 1000 μS/cm, and being 700–960 μS/cm on other sampling occasions (Table 1); such range of conductivity does not create technical or assessment problems of sampling efficiency or sampling selectivity36.
Finally, fish biomass data were standardized in a way that enabled constructing significant regression models. This occurred owing to the Hellinger transformation of data. Transformation of the data was necessary because of high variation in raw fish biomass between some of the sampling occasions.
Prussian carp invasion, reversal of the invasion, recovery of the native fish species, and their drivers in the Ner
Results of the above analysis, in particular that of the RDA, indicate that the trait that enabled Prussian carp invasion of the recovered course in the phase of the initial environmental stress decrease was most probably the species’ ability to exist in worse oxygen conditions than other species. This is congruent with Prussian carp’s capacity for anaerobic metabolism, which is absent or weaker in other fish species15,37. Owing to this metabolism, Prussian carp can survive weeks of hypoxia, and even several hours of anoxia. Perhaps, other traits additionally enabling the invasion were Prussian carp’s tolerance of high phosphorus and nitrogen levels16, which were also noticed in the Ner in the late 1990s and early 2000s, and phenotypical plasticity of reproduction12,38.
The RDA results also indicate that additional factors favouring Prussian carp might have been high calcium and total phosphorus contents. In contrast, weatherfish were able to thrive and avoid competition with Prussian carp in the recovered course till 2000 owing to their ability to breath atmospheric air, detritus-oriented feeding tactics, and preference for vegetated zones of extremely shallow water depths39,40.
Yet, when the next phase of environmental stress decrease (over the course of the fish sampling period) made the recovered course of the Ner good enough to become colonisable by other fish species, the situation of Prussian carp changed dramatically. As the amount of dissolved oxygen further considerably increased in that period, the ability of anaerobic metabolism was no longer an asset, while the new colonizers became its competitors. Of these competitors ide may have been the most important species for Prussian carp decline (the causes of which are explained in the next subchapter). This is indicated by results of regression analysis presented in Tables 6 and 7 and Fig. 6 (see “Results”).
An open question is whether slower decrease in environmental stress than that presently observed in the recovered course would enable Prussian carp to develop defence mechanisms that would reduce their replacement by ide. This might be possible owing to Prussian carp’s phenotypical plasticity. This plasticity might produce modifications of the niche occupied by Prussian carp, and in this way lessened the interference competition between the two species. Unfortunately, there is no MA (or any other) model II regression that may be used with multiple predictors (and hence no such multispecies models are presented here), by analogy to multiple regression31. Multispecies model II regression might be useful because a probable long term interaction of Prussian carp with roach, for example, was observed by Paulovits et al.41, although it occurred in a shallow reservoir instead of a river.
Why was ide the replacer of Prussian carp rather than other fishes?
The explanation why ide acted as the replacer of Prussian carp is difficult, but at least to some extent possible. Schiemer and Wieser42 defined food and feeding, ecomorphology, and energy assimilation and conversion as four groups of traits that decide about the success of given cyprinids, and used the traits to substantiate increasing roach dominance in Central European rivers. Although much less is known about these groups as regards ide (but see Rothla et al.43), yet ecomorphology seems to be most important also in its case. Large body depth of ide makes it similar to Prussian carp and thus its tough competitor. As the shape of ide is much less streamlined than that of most other large-bodied obligatorily riverine cyprinids, ide, like Prussian carp, avoids water current zone44 in order to reduce energy loss resulting from water resistance during movement. This increases the risk of occupying similar ecological niches by these two species. However, ide grow to bigger body sizes than Prussian carp, which gives the former a big advantage over the latter while searching for food (interference competition) and while avoiding predation.
Moreover, while Prussian carp is one of the most resistant fish species in general, ide belongs to the most resistant obligatory riverine (i.e. fluvial specialist) cyprinids, although its occurrence may sometimes even resemble that of limnophilic fishes45,46. The capacity of ide to be successful in more than averagely polluted river courses is manifest in the Warta, the parent river of the Ner. Przybylski47 and Kruk46, who distinguished contrasting reaches in the Warta, noticed a significantly higher biomass of ide in the middle, most polluted reach (to which the Ner empties), as early as in 1986–87 and 1996–1998, respectively. Ide usually dominated poor, several-species rich assemblages there. The situation was much similar in the Warta much later, in 2011–2012, when ide was significantly associated with the middle course, in which fish assemblages were in the poorest condition as compared to the upper and lower courses48.
Kruk46 attributes the high abundance of ide in the most polluted middle Warta River to weak competition from other rheophils, which were absent there because river degradation was too severe for them. In contrast, in the other sections of the Warta, ide were much less abundant owing to improved water quality and thus higher abundance of other rheophils, competitors of ide. If this presumption is correct, i.e. if the consequences of a spatial degradation gradient may become reflected in a temporal degradation gradient, then further decrease in environmental stress in forthcoming years may result in the replacement of ide by other rheophilic species in the Ner, too. This prognosis is supported by Eklöv et al.’s45 observation of ide decline coinciding with trout increase after a long-term improvement in water quality in streams of southern Sweden.
All fish species that colonized the recovered course of the Ner were species recorded for several dozen years in the Warta catchment46,49,50,51,52,53,54, and the fish species list of the catchment is about 20–40% longer than the list of species determined in the Ner. The list of the Warta is also similar to those of other nearby catchments of central Poland55,56. This indicates that all species that colonized the Ner in recent decades may have originated from the regional species pool57,58 rather than from stocking, aquaculture or unintentional introductions. Nevertheless, ide are frequently used in stocking, which increases their chance to become an instrument of controlling non-native fish species, while the present study contributes to the purposefull exploitation of the fish species.
A quite different perspective of an invasion was presented by Bøhn et al.59. While monitoring the invasion of vendace (Coregonus albula L.) into upstream and downstream lakes 50 km apart located on the Norwegian sub-arctic Pasvik watercourse they observed great life history variability of the non-native fish entering a new environment. This consisted in decrease in the mean length in all age-classes, in fecundity, in the mean weight and size of individuals at first maturation, and increase in growth rate. Unfortunately, in the Ner we could only check the mean weight of individuals (results not shown): it varied in both Prussian carp and ide, but no clear decreasing or increasing trends were observed over the study period.
Ide as the suppressor of Prussian carp, and other methods of extirpating the latter species
If the presumption that ide contributes as a biotic extirpator to Prussian carp decline is true then a comparison of ide with other suppression drivers is worth considering. One thing that may limit ide importance in other environments, for example, may be the above mentioned Prussian carp’s phenotypical plasticity: consequently, further research in this respect is necessary. Although the herpesviral hematopoietic necrosis virus (Cyprinid herpesvirus 2, CyHV-2) operates much faster than ide it cannot practically be used because it is uncontrollable in natural environments. This is the case because the virus, which is believed to have global occurrence, causes epizootics only when triggered by a specific range of water temperatures60, which of course can hardly be manipulated.
Besides, the virus suffers from the problem of selectivity. In the Czech Republic, the virus caused an epizootic that killed probably most individuals of numerous Prussian carp populations within weeks, but the fish were all triploid females18. It is not known why other ploidy forms38 were not affected, which is important because there is a natural tendency of invasive triploid female populations (with a few percent of males) to quickly transform themselves into diploid bisexual populations12. Moreover, first information about the virus indicated mass mortality of cultured goldfish [Carassius auratus (auratus)] in many countries, and it is not certain that it will not affect other fish species in the future20. Finally, the virus-assisted extirpation would be a very drastic form of animal control.
Reduction in frequency of desiccation events is an environmental measure of Prussian carp suppression that was discovered in Hungary21. It was observed there that in reservoirs, lakes and canals in which few or no desiccation events occurred, the relative abundance of Prussian carp constituted between one fifth and half of that recorded in fish ponds, for example, where desiccation was frequent. Moreover, the method is probably selective, affecting no other, native species. However, it cannot be applied to all freshwater bodies, for technical or financial reasons, and the elimination of Prussian carp is far from total. Interestingly, desiccation, and its relation to small water body sizes, was determined as one of factors favouring Prussian carp occurrence by Górski et al.61 in the Volga floodplain areas, where large water body size was also assessed as a factor favouring ide occurrence.
Theoretical perspective
Generally, both the invasion by Prussian carp and its reversal comply with major theoretical predictions: the invasion with community ecology as a framework for biological invasions62,63 and the reversal with both the framework and the concept of biotic (ecological) resistance27,28,64,65. In the case of the invasion, because mostly the amount of resource (in this case: increase in dissolved oxygen, accompanied by decrease in BOD5, decrease in total phosphorus, etc.; in short—water quality) increased to a level that allowed the invader to exploit the environment, but was too low for other, native fishes, and thus Prussian carp (and weatherfish) colonized the river instead of the others. This also agrees with scenario 2 of the theoretical framework for invasions defined by Facon et al.66, in which environmental change is the main factor of invasion.
In the case of the reversal of the invasion, compliance with the theories occurs because the resource (mainly water quality) increased/improved high enough to be exploited by other, native species, and also because the native species became then competitors of the invader and thus biotic resistance drivers23,28. These drivers are defined in the biotic resistance hypothesis64, which describes the chances of an invasive species to be successful in a new environment. According to the hypothesis native-species-diverse environments are more resistant to invasive species than native-species-poor environments through a combination of predation, competition, parasitism, disease, and aggression. In this context, ide may resist Prussian carp, for example, owing to occupying similar spawning grounds as both species are open substratum spawners [ide being a phyto-lithophil (A.1.4), and Prussian carp a phytophil (A.1.5)]67. In the case of these two species, the resistance may be extended to ide predation on Prussian carp’ eggs, larvae or juveniles. Besides, ide grows to bigger body sizes than Prussian carp, which may result in aggressive behaviour in the form of scaring Prussian carp away from feeding grounds or hiding places.
In contrast, both the invasion and its reversal do not support the concept of invasional meltdown68, according to which in the initial phase an invasive species causes rapid changes in an ecosystem (by altering the trophic chain, for example), in this way paving the way for the invasion of subsequent non-native species66. In a next phase, when two or more alien species have invaded the ecosystem, synergistic interactions among them accelerate the invasion process68.
Yet, it is possible that the occurrence of biotic resistance rather than invasional meltdown has been an effect of insufficient biomass or abundance of other invasive species in the regional species pool57,58, of other aspects of the biotic context or small spatial and/or temporal scales of the processes26, or of environmental filters that might have prevented the invasion of other non-native species in the Ner69. Consequently, a number of quite different possible scenarios for the Ner are imaginable, for example no reversal of Prussian carp invasion if ide had not been abundant in the parent Warta River, or if species composition there had been quite different in other respects. This problem requires further research to reach reliable conclusions.
Source: Ecology - nature.com
