Variations in the migratory history of the tropical catadromous eels Anguilla bicolor bicolor and A. bicolor pacifica in south-east Asian waters

Fish movements between aquatic habitats of different salinity ranges (fresh, estuarine, marine) by the tropical catadromous eels Anguilla bicolor bicolor and A. bicolor pacifica were examined by analysing the otolith strontium and calcium concentrations of yellow (immature) and silver (mature) stage eels collected in south-east Asian (Indonesia, Malaysia and Vietnam) waters. The ratios suggest that all migratory-type eels, including freshwater, brackish water and marine residents, pass the river mouth. However, the habitat preference was different among the sites (countries). In Indonesia and Vietnam, most A. bicolor bicolor and A. bicolor pacifica were either marine or brackish water residents in this study. Alternatively, most A. bicolor bicolor were freshwater residents in Malaysia; such a typical catadromous migration pattern in these eels has not been found in previous studies. The wide range of otolith Sr:Ca in both subspecies indicates that the habitat use of these tropical eels was opportunistic among fresh, brackish and marine waters during their growth phases following recruitment to coastal areas. The geographical variability of migratory histories suggests that habitat use might be determined by the inter and intraspecific competition and environmental conditions at each site.     

Evaluation of downward movements of Japanese eel Anguilla japonica inhabiting brackish water areas

This study evaluated the size and age distributions and otolith microchemistry of the Japanese eel Anguilla japonica in freshwater and brackish water areas in the Aki and Tsuchikawa rivers for 1 year, and in brackish water areas in the Asahi River for 3 years to understand the movements of Japanese eels between continental habitats of different salinity after recruitment (n = 759). For all three rivers, the total length (L_T) and age distributions were consistent; yellow eels captured in the upper brackish water (Aki River: 353.5 ± 77.4 mm and 3.0 ± 0.8 years; Tsuchikawa River: 287.7 ± 87.3 mm and 3.7 ± 1.3 years; Asahi River: 418.2 ± 112.1 mm and 4.2 ± 1.7 years) were smaller and younger than not only those in the fresh water of the two rivers but also those in the lowest brackish water sampling areas (Aki River: 436.0 ± 71.6 mm and 3.8 ± 1.1 years; Tsuchikawa River: 370.9 ± 121.7 mm and 4.9 ± 2.3 years; Asahi River: 558.5 ± 85.9 mm and 5.7 ± 1.7 years). In the Asahi River, these tendencies were found throughout the 3 years. Otolith analysis indicated that the majority of the eels captured in the lowest brackish water areas had moved down from upstream. These results suggest that Japanese eels inhabiting saline water generally move from the upper estuary as they grow. The upper estuary can be an important area for the management of this species because these eels spend their early continental growth life there.     

Dispersal of yellow phase Japanese eels <Emphasis Type="Italic">Anguilla japonica</Emphasis> after recruitment in the Kojima Bay-Asahi River system,Japan

The density, size and age distribution were investigated for 233 eels, Anguilla japonica, sampled in fresh and brackish water areas of the Kojima Bay-Asahi River system, Okayama, Japan, to evaluate the possible patterns of dispersal of eels that recruit to this area. Migratory histories of 183 eels were categorized into 5 types depending on the Sr and Ca concentrations in their otoliths: (1) brackish water residents (74 fish, 40.4%), which settled in saline water and remained until capture; (2) freshwater residents (46 fish, 25.1%), which settled in freshwater and remained until capture; (3) upstream shifters (3 fish, 1.6%), which settled in saline water and moved upstream into freshwater; (4) downstream shifters (53 fish, 29.0%), which settled in freshwater and moved downstream into saline water; (5) multiple habitat shifters (7 fish, 3.8%), which shifted their habitats between freshwater and saline water more than twice. For eels captured in the brackish water area, fish density decreased with distance in the downstream direction, while the size and age of eels increased. For eels captured in the freshwater area, size and age were greater than those in the upper-most brackish site. These observations suggest that eels in this system initially accumulate in the lower reaches of the river and then disperse in both upstream and downstream directions following their growth.     

Head‐shape polymorphism in Japanese eels Anguilla japonica in relation to differences of somatic growth in freshwater and brackish habitats

The age, total length (L_T), head shape and skull shape were investigated for 379 Japanese eels Anguilla japonica sampled in freshwater and brackish areas of the Kojima Bay–Asahi River system, Okayama, Japan, to learn about the differentiation process of head‐shape polymorphism. The relative mouth width (ratio of mouth width to L_T) of A. japonica > 400 mm L_T collected in fresh water was significantly greater than that of fish collected in brackish water. Growth rates of mouth width and the distance from the snout to the midpoint of the eyes (the ratio of width and distance to age, respectively) were not significantly different between freshwater and brackish‐water samples, whereas the somatic growth rate (the ratio of L_T to age) of freshwater samples was significantly lower than that of brackish‐water eel samples. These results suggest that the factors affecting head and somatic growth of A. japonica are not identical. According to these results and feeding patterns in each habitat reported by another study, it is suggested that somatic growth appears to play a significant role in the differentiation process of the head‐shape polymorphism in A. japonica, with the slow‐growing fish in fresh water becoming broad‐headed and the fast‐growing fish in brackish water becoming narrow‐headed.     

Migration and habitat use of the tropical eels Anguilla marmorata and A. bicolor pacifica in Vietnam

The patterns of use of marine and freshwater habitats by the tropical anguillid eels Anguilla marmorata and A. bicolor pacifica were examined by analysing the otolith strontium (Sr) and calcium (Ca) concentrations of yellow (immature) and silver (mature) stage eels collected in Vietnamese waters. In A. marmorata, the change in the Sr:Ca ratios outside the high Sr:Ca core was generally divided into three patterns: (1) typical catadromous life history pattern; (2) constant residence in brackish water; and (3) habitat shifting between sea and brackish waters with no freshwater life. In A. bicolor pacifica, no eels had a general life history as freshwater residents. The eels were also divided into three patterns: (1) constant residence in sea water; (2) constantly living in brackish water; and (3) habitat shifting from brackish to sea water with no freshwater residence. The mean Sr:Ca ratio value after recruitment to coastal waters ranged from 1.73 to 5.67 × 10^?3 (mean 3.2 × 10^?3) in A. marmorata and from 2.53 to 6.32 × 10^?3 (mean 4.3 × 10^?3) in A. bicolor pacifica. The wide range of otolith Sr:Ca ratios in both species indicated that the habitat use of these tropical eels was facultative among fresh, brackish, and marine waters during their growth phases after recruitment to coastal areas. Tropical eel species may have the same behavioural plasticity as temperate anguillid species regarding whether to enter freshwater or to remain in estuarine and marine environments.     

Unravelling the life-history patterns and habitat preferences of the Japanese eel (Anguilla japonica) in the Pearl River,China

Eels have fascinated biologists for centuries due to their amazing long-distance migrations between freshwater habitats and very distant ocean spawning areas. The migratory life histories of the Japanese eel, Anguilla japonica, in the waters of south China are not very clear despite its ecological importance, and the need for fishery regulation and management. In this study, strontium (Sr) and calcium (Ca) microchemical profiles of the otoliths of silver eels were measured by X-ray electron probe microanalysis based on data collected from different habitats (including freshwater and brackish habitats), in the large subtropical Pearl River. The corresponding habitat preference characteristics were further analysed using redundancy analysis (RDA). A total of 195 Japanese eels were collected over 6 years. The collected individuals ranged from 180 to 771 mm in total length and from 8 to 612 g in body weight. Two-dimensional pictures of the Sr:Ca concentrations in otoliths revealed that the A. japonica in the Pearl River are almost entirely river eels, spending the majority of their lives in fresh water without exposure to salt water, while the catadromous migration time has delayed about 1 month in the Pearl River estuary in the past 20 years. RDA analysis further indicated that juveniles and adults preferred water with high salinity and high tide levels. Youth preferred habitats with high river fractals. Our findings contribute to a growing body of evidence showing that the eels are extremely scarce currently and conservation measures against them are imminent, including the protection of brackish and freshwater areas where they live in south China.     

Stable isotope analyses provide new insights into ecological plasticity in a mixohaline population of European eel

Recent studies have shown that anguillid eel populations in habitats spanning the marine–freshwater ecotone can display extreme plasticity in the range of catadromy expressed by individual fishes. Carbon and nitrogen stable isotope analysis was used to differentiate between European eels (Anguilla anguilla) collected along a short (2 km) salinity gradient ranging from <1‰ to ~30‰ in Lough Ahalia, a tidal Atlantic lake system. Significant differences were recorded in mean δ¹³C, δ¹⁵N and C:N values from eels collected from fresh, brackish and marine-dominated basins. A discriminant analysis using these predictor variables correctly classified ca. 85% of eels to salinity zone, allowing eels to be classified as freshwater (FW), brackish (BW) or marine (MW) residents. The results of the discriminant analysis also suggested that a significant proportion of eels moved between habitats (especially between FW and BW). Comparisons of several key population parameters showed significant variation between eels resident in different salinity zones. Mean condition and estimated age was significantly lower in MW eels, whilst observed length at age (a correlate of growth) was significantly higher in MW eels, intermediate in BW and lowest in FW eels. This study has demonstrated that the ecology of eels found along a short salinity gradient can be extremely plastic and that stable isotope analysis has considerable utility in demonstrating intra-population variation in diadromous fishes.     

How does salinity influence habitat selection and growth in juvenile American eels Anguilla rostrata?

The influence of salinity on habitat selection and growth in juvenile American eels Anguilla rostrata captured in four rivers across eastern Canada was assessed in controlled experiments in 2011 and 2012. Glass eels were first categorized according to their salinity preferences towards fresh (FW), salt (SW) or brackish water (BW) and the growth rate of each group of elvers was subsequently monitored in controlled FW and BW environments for 7 months. Most glass eels (78–89%) did not make a choice, i.e. they remained in BW. Salinity preferences were not influenced by body condition, although a possible role of pigmentation could not be ruled out. Glass eels that did make a choice displayed a similar preference for FW (60–75%) regardless of their geographic origin but glass eels from the St Lawrence Estuary displayed a significantly higher locomotor activity than those from other regions. Neither the salinity preferences showed by glass eels in the first experiment nor the rearing salinities appeared to have much influence on growth during the experiments. Elvers from Nova Scotia, however, reached a significantly higher mass than those from the St Lawrence Estuary thus supporting the hypothesis of genetically (or epigenetically) based differences for growth between A. rostrata from different origins. These results provide important ecological knowledge for the sustained exploitation and conservation of this threatened species.     

Migration,residency and habitat utilisation by wild and cultured Japanese eels (Anguilla japonica) in a shallow brackish lagoon and inflowing rivers using acoustic telemetry

This study monitored post-release movements of 20 wild Japanese eels (Anguilla japonica) [mean ± S.D. 520.8 ± 92.3 mm total length (TL), 217.9 ± 146.3 g body mass (BM)] in a brackish water lagoon in northeastern Japan using acoustic telemetry to elucidate how wild Japanese eels use different river, estuary and marine environments. In addition, 12 cultured Japanese eels (TL = 578.9 ± 18.0 mm, BM = 344.9 ± 25.5 g) were released to understand the comparative behaviours of wild and cultured eels. Both types of eels were simultaneously released in the southern inner part of the lagoon in September 2016 where there are freshwater influences from a river. Following release, eight of the wild eels (40%) were largely sedentary near the released point (river mouth) and stayed at the site for overwinter. Nonetheless, several individuals showed behavioural plasticity of habitat use: three wild eels moved towards the northern part of the lagoon with stronger influence from the sea during May–July 2017. Two wild eels showed clear repeated movements from the lagoon to a river at night and returned to the lagoon by dawn for more than a week every day, and one wild eel migrated upstream for overwintering. Signals from 55% of the wild eels could be detected for more than 6 months, whereas those from all of the cultured eels were lost by December 2016, indicating a short resident time of large cultured eels (BM > 200 g) released in a brackish water area. One wild silver eel migrated to the outer sea during the ebb tide at night in November 2016, probably triggered by the decrease in water temperature (from c. 20°C to c. 13°C), and seven cultured eels similarly moved to the outer sea during October–November 2016. The results revealed the similarities (e.g., nocturnal movements) and differences (e.g., stay period and seasonal movements) in the behavioural characteristics of wild and cultured eels and indicated that habitat connectivity among river, estuary and coastal waters is crucial for enabling eels to efficiently utilise these productive habitats through their behavioural plasticity.     

Trichinella spiralis: the influence of short chain fatty acids on the proliferation of lymphocytes, the goblet cell count and apoptosis in the mouse intestine

This study was carried out to determine the influence of short chain fatty acids (SCFA) on spleen and mesenteric lymph node lymphocyte proliferation, goblet cells and apoptosis in the mouse small intestine during invasion by Trichinella spiralis. BALB/c mice were infected with 250 larvae of T. spiralis. An SCFA water solution containing acetic, propionic and butyric acids (30:15:20 mM) was administered orally starting 5 days before infection and ending 20 days post infection (dpi). Fragments of the jejunum were collected by dissection 7 and 10 dpi, and were examined for apoptotic cells in the lamina propria of the intestinal mucosa, and for goblet cells. The proliferation index of the cultured spleen and mesenteric lymph node lymphocytes with MTT test was also determined. The orally administered SCFA solution decreased the proliferation of mesenteric lymph node lymphocytes in the mice infected with T. spiralis at both examination times, but did not influence the proliferative activity of the spleen cells. Seven dpi, both in the spleen and mesenteric lymph nodes, the highest proliferation index of concanavalin A (Con A)-stimulated lymphocytes was found in the group of uninfected animals receiving SCFA animals. This tendency could still be seen 10 dpi in the mesenteric lymph nodes but not in the spleen, where the proliferation index in this group had significantly decreased. In vitro studies revealed, that butyric and propionic acids added to the cell cultures suppressed the proliferation of Con A-stimulated mesenteric lymph nodes and spleen lymphocytes taken from uninfected and T. spiralis-infected mice. Acetic acid stimulated proliferation of splenocytes taken from uninfected mice but did not affect lymphocyte proliferation in mesenteric lymph nodes from uninfected or infected mice. Orally administered SCFA increased the number of goblet cells found in the epithelium of the jejunum 7 dpi, but this number had decreased 10 dpi. The number of apoptotic cells in the lamina propria of the intestinal mucosa of animals infected with the T. spiralis and receiving SCFA was also lower, particularly 10 dpi. The above results show that SCFA can participate in the immune response during the course of trichinellosis in mice.     

Head morphology and piscivory of European eels,Anguilla anguilla,predict their probability of infection by the invasive parasitic nematode Anguillicoloides crassus

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Salinity-linked growth in anguillid eels and the paradox of temperate-zone catadromy

Temperate-zone anguillid eels use both saline (marine or brackish) and fresh waters during their continental phase, but use of fresh waters is paradoxical because on average these fishes grow more rapidly in saline than in fresh waters. Based on data from anguillid eels whose habitat-residency histories had been determined by Sr:Ca otolithometry, superiority of growth rates in saline water is much greater in American eels Anguilla rostrata in north-eastern North America (mean saline:fresh growth rate ratio 2·07) than in European Anguilla anguilla , Japanese Anguilla japonica and shortfinned Anguilla australis eels (range of mean ratios 1·12–1·14). Data from A. rostrata in the Hudson Estuary, U.S.A., and Prince Edward Island, Canada, were used to test adaptive explanations of catadromous migrations. The hypothesis that lower mortality in fresh water offsets faster growth in saline water was not supported because loss (mortality + emigration ) rates did not vary between saline and fresh zones of the Hudson Estuary. Hypotheses that anguillid eels move to fresh water to escape from larger anguillid eels in saline water or to evaluate habitat quality were not supported by size and age distributions. Catadromy in temperate-zone anguillid eels increases the diversity of occupied habitats and therefore lowers fitness variance caused by environmental fluctuations. Catadromy in temperate-zone anguillid eels could be due to natural selection for maximum geometric mean fitness which is sensitive to fitness variance. Temperate-zone catadromy might also be maladaptive, at least in local areas, due to shifts over time in selective pressures or to inability of panmictic genetic systems to adapt to local conditions.     

A comprehensive hypothesis on the migration of European glass eels (Anguilla anguilla)

The European eel (Anguilla anguilla) is a catadromous fish that spawns in the Sargasso Sea. As larvae, eels cross the Atlantic Ocean and reach the continental slope of Europe, where they metamorphose into post‐larval glass eels. These reach the continent, where some enter fresh water, some remain in marine waters, and others move between fresh and marine waters. After 5–25 years, as adult silver eels, they migrate back from fresh water to the Sargasso Sea to spawn and die. The glass eel stage is a critical step during which the eels cross the continental shelf and recruit to estuaries, where they facultatively transition to fresh water. Extensive research has been conducted to understand the behavioural mechanisms and environmental cues that aid and guide glass eels' migration. Glass eels follow odours and salinity gradients, they avoid light, and they change orientation and depth according to the tides. Recent work revealed that European glass eels also use Earth's magnetic field and lunar cues to orient. However, while we understand many aspects of their orientation behaviour, a unifying theory describing how glass eels migrate from the continental slope to fresh water is lacking. The goal of this review is to develop a comprehensive hypothesis on the migration of European glass eels, integrating previous knowledge on their orientation behaviour with recent findings on magnetic and celestial orientation. This review follows the journey of a hypothetical glass eel, describing the nature and the role of orientation cues involved at each step. I propose that, although glass eels have the sensory capacity to use multiple cues at any given time, their migration is based on a hierarchical succession of orientation mechanisms dictated by the physical properties of the environments that they occupy: (i) lunar and magnetic cues in pelagic water; (ii) chemical and magnetic cues in coastal areas; and (iii) odours, salinity, water current and magnetic cues in estuaries.     

Chemical marking of European glass eels Anguilla anguilla with alizarin red S and in combination with strontium: in situ evaluation of short‐term salinity effects on survival and efficient mass‐marking

This study presents a new chemical double‐marking technique for European glass eels Anguilla anguilla by combing alizarin red S (ARS) and strontium chloride hexahydrate (Sr). Marked eels (double marked with ARS and Sr, but also single marked with ARS) were exposed in situ to brackish water (15 g l^?1 artificial sea salt) for 14 days and did not exhibit increased mortalities compared with unmarked eels. Indeed, no mortality occurred in a marked group during the experiments. Moreover, an efficient mass‐marking approach with low handling effort for both single ARS and double ARS‐Sr techniques is described and was proven to be practicable for large‐scale stocking programmes.     

Biological Differences between Brackish and Fresh Water-Derived Aedes aegypti from Two Locations in the Jaffna Peninsula of Sri Lanka and the Implications for Arboviral Disease Transmission

The mainly fresh water arboviral vector Aedes aegypti L. (Diptera: Culicidae) can also undergo pre-imaginal development in brackish water of up to 15 ppt (parts per thousand) salt in coastal areas. We investigated differences in salinity tolerance, egg laying preference, egg hatching and larval development times and resistance to common insecticides in Ae. aegypti collected from brackish and fresh water habitats in Jaffna, Sri Lanka. Brackish water-derived Ae. aegypti were more tolerant of salinity than fresh water-derived Ae. aegypti and this difference was only partly reduced after their transfer to fresh water for up to five generations. Brackish water-derived Ae. aegypti did not significantly discriminate between 10 ppt salt brackish water and fresh water for oviposition, while fresh water-derived Ae. aegypti preferred fresh water. The hatching of eggs from both brackish and fresh water-derived Ae. aegypti was less efficient and the time taken for larvae to develop into pupae was prolonged in 10 ppt salt brackish water. Ae. aegypti isolated from coastal brackish water were less resistant to the organophosphate insecticide malathion than inland fresh water Ae. aegypti. Brackish and fresh water-derived Ae. aegypti however were able to mate and produce viable offspring in the laboratory. The results suggest that development in brackish water is characterised by pertinent biological changes, and that there is restricted genetic exchange between coastal brackish and inland fresh water Ae. aegypti isolates from sites 5 km apart. The findings highlight the need for monitoring Ae. aegypti developing in coastal brackish waters and extending vector control measures to their habitats.     

Colonization, larval survival and epidemiology of the nematode Anguillicola crassus, parasitic in the eel, Anguilla anguilla, in Britain

In late 1987, immature Anguillicola crassus were reported for the first time in Britain from eels from two river systems. By late 1988, gravid adults were present in a number of rivers in the east of England in two discrete centres of distribution: one in East Anglia correlated with the route taken by lorries exporting eels to the continent, and one in the R. Thames correlated with the import of eels to London. The parasite was firmly established in the R. Trent, where prevalence levels reached 100% in some places. Laboratory investigations showed that adult parasites and their eggs remained viable even after infected eels had been maintained for 4 weeks in 100% sea water. Hatching of eggs declined with increasing salinity, but was not totally inhibited by sea water. Survival and infectivity of freeliving second stage larvae were maximal in natural fresh water (95% survival for 4 months, and 50% still infective to copepod intermediate hosts after 70 days), but declined in alkaline water and with increased salinity. Nevertheless, in 100% sea water, 50% of larvae were still infective after 8 days. Specificity to the intermediate host was low, and eels of all sizes could be infected. These characteristics, plus a high reproductive potential, give the parasite exceptional colonization potential and ability, enabling it to survive natural movements of eels from catchment to catchment and to increase rapidly within a new locality. The ability of free-living larvae to adhere to the substratum and survive in sea water enables them to survive in eel-transport lorries from which they will not readily be removed by flushing, the normal cleansing procedure. It is concluded that there were two separate introductions of the parasite to Britain; via the eel import trade through London, and, totally unexpectedly, via the eel export trade in lorries traversing East Anglia. The parasite is now firmly established in Britain and will continue to spread by natural movements of eels but especially by human-assisted movements of infected eels for stocking and market. This latter practice is recognized as a major factor in introducing and disseminating fish parasites.     

Effect of salinity on hatching, survival and infectivity of Anguillicola crassus (Nematoda: Dracunculoidea) larvae

The effect of salinity on hatching, larval survival and infectivity of Anguillicola crassus was studied under experimental conditions using eggs obtained from naturally infected eels. Egg hatching rate, second-stage larval survival and larval infectivity were maximal in fresh water and declined with increase in salinity. Larvae survived up to 100 d in fresh water, 70 d in 50 % sea water and 40 d in 100% sea water. Infectivity experiments demonstrated that salinity influenced transmission success throughout the life cycle by decreasing total infectivity of the larval population in utero within female A. crassus and when larvae were free-living in the aquatic environment. Infectivity was age-dependent in relation to salinity. Larvae were infective to intermediate and paratenic hosts for up to 80 d in fresh water, 21 d in 50% sea water and up to 8 d in 100% sea water. The data confirm field observations that infection levels decrease with an increase in salinity. The study contributes to experimental verification of the colonization abilities of A. crassus and supports the hypothesis that A. crassus can be disseminated and transmitted in brackish water. The importance of regular monitoring and stringent hygiene practices in the transportation of eels is emphasized.     

Chloridzellen der Larven von Caenis diminuta WALKER (Ephemeroptera,Caenidae) bei unterschiedlicher Salinität

The larvae of Caenis diminuta WALKER (Ephemeroptera, Caenidae) have coniform chloride cells which are involved in osmoregulation. The number of chloride cells varies according to salinity conditions of the surrounding waters. The larvae from brackish water have less chloride cells than the larvae from fresh water.     

Nutritional condition of Anguilla anguilla starved at various salinities during the elver phase

The effects of food deprivation and environmental salinity (<1, 10 and 20) on survival, fish morphology, organization of the digestive system and body lipid reserves in European eel Anguilla anguilla during the transition from glass eel to elver, were evaluated. Fasted elvers kept in fresh water were able to withstand starvation for >60 days, while those in brackish environments (salinity 10 and 20) reached the level of irreversible starvation at 37 and 35 days, respectively. The high level of lipid reserves contained in liver inclusions and the abdominal cavity (perivisceral deposits) in elvers might explain their long resistance to starvation and differences in fasting tolerance under different salinities. Fasting resulted in a significant reduction of the elvers' condition factor and body depth. There were severe histopathological changes in the digestive system and musculature, such as the alteration of the liver organization, and hepatic glycogen and lipid content, shrinkage of enterocytes and reduction of their height, pancreas degeneration, autolysis of the oesophageal and intestinal mucosa and disarrangement of myofibrils and degeneration of trunk musculature. Degeneration of the oesophageal and intestinal mucosa as a consequence of fasting might have impaired digestive and osmoregulatory functions in feed‐deprived fish, directly affecting the tolerance to starvation and survival. Length of food deprivation was associated with a significant increase in mortality, coefficient of variation, cannibalism and point of no return at high salinities. Mortality was dependent on food deprivation and salinity concentrations. Environmental salinity directly influenced the ability of elvers to withstand starvation; once glass eels metamorphosed into elvers, they tolerated starvation better in fresh water than in brackish environments.