Abstract
Freshwater eels are of tropical marine origin and have spread worldwide. Of the 19 recognised species or subspecies, all 6 temperate species are listed within IUCN Threatened Species categories, together with 7 tropical species. Many reasons have been advanced to explain the significant declines of eels including habitat fragmentation and loss, spread of parasites and diseases, pollution, impacts of hydro dams, overfishing and oceanic changes. The present paper reviews some of the unique life history characteristics of Anguillids—fecundity and semelparous spawning, adaptability, resilience, and being energetically conservative—but despite such remarkable adaptations, according to the IUCN the genus is facing possible extinction. It is suggested that Anguillid life history strategies rely on two additional components—environmental determination of sex, and the need for surplus production (the Surplus Production Hypothesis, SPH). Surplus production is required to counteract the many hazards that eels face throughout an often long and complex life history. Recruitment of temperate species has fallen by over 90%, and resulting lower densities of juvenile eels in tidal and lower river reaches provides less incentive for upstream migration and dispersal. Female eels are generally found further inland than males, with development of sex associated with lower densities. With fewer juveniles migrating to inland areas, the numbers of females will become reduced, and further compound the reduced spawner biomass and consequent reduced recruitment of glass eels. The SPH hypothesis emphasises the importance of conservative harvest of glass eels, habitat connectivity, the need to ensure maximum female escapement, and the importance of stocking inland waterways with juvenile eels.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
Freshwater eels (Anguillidae) are a highly successful group of diadromous fish. The genus comprises 19 recognised species or sub-species (Kaifu et al. 2019), of which 13 are tropical and 6 are temperate. The marbled eel, A. marmorata has the greatest geographic range of any anguillid species, being found from the east coast of Africa to the Galapagos islands (McCosker et al. 2003), while A. anguilla occupies over 10,000 km2 (Dekker 2008). The American eel, (Anguilla rostrata) is found along more than 10,000 km of the western Atlantic coastline, leading to the claim by Helfman et al. (1987) that it probably occupies the broadest diversity of habitats of any fish species in the world. As well as being widespread, eels have colonized an extensive range of inshore marine and freshwater habitats worldwide, including estuaries and coastal embayments, mainstem rivers, swamps and wetlands, lowland and inland lakes, ranging from oligotrophic to eutrophic (Dekker 2008). Thus, anguillids will have the widest distribution of any naturally occurring freshwater genus.
Origins and Life history
The genus originated in tropical marine areas but has since colonised freshwater habitats (Tseng 2016; Arai 2020). Thirteen species live in the Indo-Pacific region (Tseng 2016), considered to be the ancestral home of the genus (Minegishi et al. 2005). The ancestor of Anguilla probably originated in the Tethys Sea 50–100 Mya, but closure of this sea separated the Atlantic eels from Indo-Pacific eels, leading to the vicariant speciation of other Anguillid species (Tseng 2016). With the exception of the New Zealand longfin (A. dieffenbachii), all anguillids today range at least partially in tropical and subtropical areas (Nijman and Siriwat 2020).
Being of marine origin, the genus retains marine spawning, with dispersal of larvae (leptocephali) being largely passive on favourable ocean currents that convey larvae to island and continental waters. For temperate species, distances from spawning areas to freshwater habitats are measured in 1000’s of km—the greatest distance traversed is by A. anguilla, the European eel, where migrations range from 5000–10,000 km (Righton et al. 2016). In contrast, the spawning ground for A. celebesensis, a tropical species, is probably less than 100 km from adult habitat (Aoyama et al. 2003; Arai 2016). However, the scale of spawning migrations of tropical species varies considerably with some species undertaking migrations between 1000–3000 km (Arai 2020). While dependence upon larval dispersal by oceanic currents has been an effective one for colonisation of widespread regions, it is also a constraint as lack of suitable currents means freshwater eels are absent from significant areas of the world, notably western coasts of Africa and North America, and South America.
When they arrive over continental shelves, the larvae metamorphose from the leaf-shaped leptocephalus to a miniature version of the elongate and slender adult, the transparent glass eel. This is the stage of entry to fresh water, and while a proportion of glass eels may choose to reside in estuarine and brackish water, most will continue their inland penetration the following summer as pigmented juveniles, elvers (Jellyman 1977; Naismith and Knights 1988; Jellyman and Arai 2016). While there are ontogenetic differences in preferred habitats occupied (Laffaille et al 2003; Jellyman et al 2003), eels will often inhabit the same general area for several years. While freshwater eels are catadromous, this behaviour is facultative as both yellow and silver eels of temperate and tropical species are capable of living their entire lives in coastal marine habitats (e.g. Tsukamoto and Arai 2001; Daverat et al. 2006; Jessop et al. 2008; Arai 2020). Eventually adult eels undergo a second metamorphosis and become silver eels, the stage of emigration to the spawning grounds. This is a fasting stage. It is assumed that eels die after spawning due to the huge energetic demands of both oceanic migration and spawning, and the severe weight loss and organ degeneration of post-spawned eels (Kurogi et al. 2011).
Importance and status of species
Ecologically, eels are very important opportunistic predators and scavengers, and serve as indicator, umbrella and flagship species for conservation of freshwater biodiversity (Itakura et al. 2020). Eels can often dominate fish biomass (Rowe et al. 1999), and, at least at historic high levels of recruitment, constrained populations of other species (Burnet 1968; Dorner and Berg 2016). Eels are also important in the diet of a range of predators including larger eels (Jellyman 1989), birds (Leukona 2002) and otters (Lutra lutra; Jenkins and Harper 1980; Kruuk 2014). Additionally, freshwater eels are commercially important, providing an international trade of almost 270,000 t in 2014, of which 98% was cultured (Monticini 2014). Unlike most commercially important fish species that are usually harvested as adults, eels are exploited at all continental life stages i.e. glass eels, elvers, yellow eels, silver eels. The demand for glass eels for culture in Asia has led to the prohibition of export of A. anguilla glass eels beyond EU borders, but unfortunately a lucrative illegal market has developed, trafficking an estimated 100 t (~ 350 million fish) annually (Kaifu et al. 2019). Eels are of great importance to native peoples, both as a foodstuff but also as a species of cultural significance (Tsukamoto and Kuroki 2014)—for example, there are many legends of the interactions of eels and human ancestry in the South Pacific (e.g. Downes 1918; Jellyman 2014).
Historically, eels were much more prolific than at present. In medieval England they were once so plentiful that they were used as currency (https://www.historyextra.com/period/medieval/eels-medieval-life-eel-rent-economy). Ribbons of glass eels migrating upstream could be seen in many European rivers (Tesch 2003), and have been described in the United Kingdom as “dense ribbons of fish, hundreds deep and tens of miles long” (Righton and Roberts 2014) and providing a black margin to either bank of the River Thames (Cornish 1902). A shoal in the Waikato River, New Zealand (4.5 m wide and 2.5 m deep) took over 8 h to pass a stationary point (Cairns 1941), while reports of continuous migrations lasting several days were not uncommon (Jellyman 1979). Glass eels were so abundant and widely available they were an important traditional food source in many European countries (Hunt 2007; McCarthy 2014). Numbers are staggering—for instance, the peak European glass eel catch in 1976 of 2700 t would equate to approximately 6.7 billion glass eels (Jellyman and Briand 2016). However, since 1980, recruitment of A. anguilla glass eels has fallen to 1–10% of former levels and in recent decades the yield of A. anguilla from eel fisheries has gradually declined to ∼10% of the quantity caught just half a century ago (Dekker and Beulaton 2016).
Overall, the genus is in a parlous state. Of the recognised 19 species and sub-species, 4 of the tropical species are listed by IUCN (2017) as Data Deficient so cannot be assessed but 7 of the remaining 9 tropical species are within Threatened Species categories (Near Threatened, Vulnerable, Endangered, Critically Endangered), while all 6 temperate species are within this Threatened Species classification (Table 1). The three species most important to world economy, are either critically endangered (A. anguilla) or endangered (A. rostrata, A. japonica).
There is a huge assemblage of scientific studies on Anguillid eels. For instance, Table 2 shows the genus Anguilla has 179,000 references in Google Scholar (Table 2), and while that is exceeded by other “freshwater” species, it exceeds references for common marine genera. Despite such scientific endeavour, many of the life history aspects of Anguilla remain elusive or controversial and key events like spawning behaviour have only been observed in the laboratory (Dou et al. 2007). Age and growth studies dominate the literature from the 1970’s to 2010 for the European eel (14%), followed by aquaculture (13%), diseases (10%), migration (10%), abundance (10%), and fisheries (8%), but studies on the impacts of climate change and resource management were low but increasing (Nikolic et al 2011).
Purpose of this paper
Much has been written about possible causes of the alarming decline of northern hemisphere eels (e.g. Dekker 2003, 2008; Haro et al. 2000; Feunteun 2002; Miller et al. 2009; Kettle et al. 2011; ICES 2014; Jacoby et al. 2015; Castonguay and Durif 2016; Drouineau et al. 2018). Possible reasons include reduction and loss of freshwater habitats, spread of parasites and diseases, pollution, impacts of hydro dams, overfishing of all freshwater stages, and oceanic changes, but most authors concede that it is very likely a combination of factors are involved (e.g. Dekker 2009). Drouineau et al. (2018) suggest that although eels are highly adaptable, the rate of anthropogenic change has exceeded their adaptive capacity, with resultant drastic declines in northern hemisphere species. Most reviews have concentrated on the potential impacts of physical changes to the eel’s environment and have been less focused on how unique Anguilla life history strategies might be involved. The present paper examines aspects of eel life history to explore why such an apparently successful genus is now almost universally threatened. Firstly, the paper highlights some of the unique adaptations of freshwater eels that have led to their widespread distribution and success in colonising an extensive range of habitats. Secondly, the paper discusses why such strategies that have been successful over geological time scales, appear less successful in the Anthropocene era.
Life history features that make major contributions to the success of Anguillid eels
Eels are amazing creatures and endowed with a unique set of morphological and behavioural features that collectively have enabled them to become such a successful and widespread genus. Five of these features are foundational to this success i.e. semelparous spawning, high fecundity, adaptability, resilience, and being energetic conservative (note that because semelparous spawning and fecundity are highly inter-related, they are combined in the following discussion).
Semelparous spawning and fecundity
Freshwater eels, like Pacific salmon, are semelparous species, and invest heavily in a single reproductive effort, after which the parents die. Much has been written about the evolution and relative advantages of semelparity versus iteroparity (e.g. Cole 1954), and for eels it is characterised by the production of numerous small eggs rather than fewer larger eggs, presumably as success of pelagic spawning is more strongly associated with egg numbers than egg size (Duarte and Alcaraz 1989). While iteroparity might be sustainable for tropical eels with shorter marine migrations, it would not be suitable for temperate species that undergo extensive migrations unless it were accompanied by feeding en route; however, given that eels are principally benthic ambush carnivores, this would not be a successful strategy in the open ocean.
Many fish species use a form of “bet-hedging” (e.g. partial spawning, parental care) to provide some buffer against such adverse effects as high predation or significant environmental change. Being complete spawners, eels do not exhibit bet-hedging at spawning; however, as sexual maturity is not dependent upon achieving a specific size or age, the spawning population will be comprised of many age cohorts—for example, ages of silver A. dieffenbachii females can range between 25 and 60 years (Todd 1980). Such a mixed age cohort spawning strategy reduces the risk of overall spawning failure by diluting the impacts of both poorly and well represented cohorts.
Semelparity is an “all eggs in one basket” strategy, as eels risk spawning failure due to such factors as insufficient energy reserves to swim to the spawning grounds (van den Thillart et al. 2009), high loadings of the swim bladder parasite, Anguillicola, that can impair swimming performance (Székely et al. 2009), predation en route (Béguer-Pon et al. 2012; Wahlberg et al. 2014), failure to navigate to the spawning ground, and failure to find a mate. In addition, the conveying of larvae back to parental habitats requires stability in the strength and direction of ocean currents. To compensate for such uncertainties and risks, eels, like other broadcast spawning fish (e.g., tuna, Farley et al. 2013) are highly fecund. Fecundity in eels is positively related to fish size (Todd 1981; MacNamara and McCarthy 2012), and females adopt a size-maximising strategy (Helfman et al. 1987). Actual fecundity varies with species and size, but recorded values range between 0.3–192.9 m eggs per female (Table 3).
Adaptability
Anguillids display remarkable adaptability during their freshwater residence. Most will enter fresh water, but many have extended or permanent residence in marine or estuarine environments (Tsukamoto and Arai 2001). The habitats they occupy change with growth—small individuals often prefer areas of shallow water and fine substrates (Jellyman et al. 2003; Johnson and Nack 2013), but with increasing size, eels prefer greater depth. At all freshwater stages, eels are closely associated with the availability of daytime cover, which can range from riparian shade and tree roots, debris clusters, undercut banks, macrophytes, and anthropogenic material like bridge piles, pipes and other debris. The climbing ability of juvenile eels (Skead 1959; Jellyman 1977) allows them to negotiate waterfalls, dams and weirs, and they can also travel through subterranean aquifers and enter coral atolls via subsurface outfalls (Castle 1968; Jellyman 1991).
Despite being primarily nocturnally active (Tesch 2003; Glova and Jellyman 2000), eels will actively feed during the day if food is available. Their diet changes with size (Jellyman 1989; Tesch 2003; Dörner and Berg 2016), and while they display ontogenetic feeding preferences (e.g. Sagar et al. 2005; Jellyman 1989), they are opportunist scavengers and eat a wide range of prey species. This opportunist behaviour is perhaps best demonstrated during periods of increased flow, when eels will enter newly inundated areas and forage widely on terrestrial food like insects and earthworms (Jellyman 1989). Although their maintenance ration is < 1% of body weight (Burnet 1952; Graynoth and Taylor 2000), their stomach is extensible, and they can consume ~ 10% of body weight/day (Gousset 1992).
Eels have different feeding mechanisms ranging from suctorial feeding via rapid buccal suction to grasping and tearing using rotational spinning (Helfman and Clark 1986). Typically, eels do not feed every day (Jellyman 1989), and can survive extended periods of fasting—for instance, the silver eel migration of several months is a non-feeding stage, and eels kept in captivity and not fed have survived for up to 5 years (Olivereau and Olivereau 1997). Growth rates are highly variable, ranging from achieving 200 g in 6 months in culture (Gousset 1992), to growing at < 1 cm/year and reaching > 100 years old (Jellyman 1995).
The determination of sex in eels is labile, and predominantly a response to growth rates and population density (Davey and Jellyman 2005), with high density favouring development of males, and lower density favouring females. Hence sex ratios typically change along the length of a waterway, with males predominating in lower reaches where densities tend to be higher but the proportion of females increasing with increasing distance inland (Tesch 2003; Oliveira and McCleave 2000; Walsh et al. 2004).
Phenotypic plasticity in eels is demonstrated by their use of diverse growth habitats (Daverat et al. 2006; Edeline 2007), variable growth rates (Geffroy and Bardonnet 2012) and length at silvering (Vollestad 1992). The seaward migration of silver eels can be delayed for a year or more should environmental conditions be unfavourable (Piper et al 2013; Jellyman and Unwin 2017). Collectively, such physical and behavioural plasticity results in considerable risk spreading and is suggested as one of the main reasons contributing to eel’s widespread distribution and colonisation of a wide range of marine and freshwater habitats. In colloquial terms, eels “go with the flow”, and their adaptive abilities enable them to utilise a wider range of environments and habitats that any other freshwater genus.
Resilience
Eels are hardy. They can tolerate water quality conditions that few other species can and survive droughts and extended periods of fasting. Tropical species are adapted to warm temperatures, hence the conclusion of Luo et al. (2013) that A. marmorata and A. bicolor pacifica survive and grow better at water temperature of 28–33 °C than at temperatures of ≤ 23 °C. However, even temperate species display remarkable tolerance of warm water, and Richardson et al. (1994) found the upper lethal temperatures for A. australis were 35.7 °C for juveniles and 39.7 °C for adults, with equivalent data for A. dieffenbachii being 34.8 °C and 37.3 °C respectively, similar to the upper limit of 38 °C for A. anguilla (Sadler 1979).
They also survive low temperatures, and between 1 –3 °C, A. anguilla enter a state of torpor (Sadler 1979). While A. rostrata survived at ≤ 5 °C for more than five weeks, the fish ceased feeding and displayed a dramatic decrease in oxygen consumption rates (Walsh et al. 1983). A. rostrata can survive under ice-covered water, where the temperature is below the freezing point of fish tissue, probably by using mud substrate as a thermal refuge (Tomie et al. 2016). Silver eels are known to use low temperatures during winter to enter a state of dormancy prior to emigration (Westerberg and Sjoberg 2014; Jellyman and Unwin 2019).
Eels subject to drought conditions do not aestivate but are able to lower their metabolic demands by up to 70% during periods of anoxia (van Ginneken et al. 2001), a practice that will enhance survival during such adverse conditions. In New Zealand, A. australis often survive loss of surface water by burrowing into moist mud (Eldon 1968; https://www.stuff.co.nz/the-press/news/north-canterbury/89068402/mata-kopae-lagoon-vanishes).
Eels can survive in oxygen-depleted waters (Wood and Johansen 1973) where more active species cannot. This survival in hypoxic conditions is due to such features as their blood having a high affinity for oxygen, and periodic apnoea (Forster 1981). Eels also have an exceptional tolerance to elevated CO2 levels in the blood (hypercapnia; McKenzie et al. 2002), conditions associated with hypoxic conditions resulting from warm temperatures and/or eutrophication. Further, they can augment gill respiration with cutaneous respiration (Forster 1981), and when dissolved oxygen levels fall below 10%, they will frequently come to the water surface and gulp air, or leave the water altogether (Itazawa 1960). The tenacity for life shown by eels is legendary, and they can even survive severing of the nerve cord (Flight and Verheijen 1993), so that humane killing requires destruction of the brain itself. Under adverse environmental conditions like low flows, eels tolerate living in close proximity. Crowding reaches extremes in culture where eels can be reared in high densities (e.g. 15 kg/m3 Gousset 1992); agonistic interactions do occur but can be reduced by size grading (Knights 1987).
So, Anguillids are hardy and resilient fishes, and frequently survive in conditions that other species cannot tolerate. This resilience is apparent at all life stages, but particularly during the yellow eel stage in coastal or freshwaters where physiological robustness aided by the eel’s sinuous shape, enables penetration of aquifers, and even climbing near-vertical surfaces. Eels rapidly colonise newly available habitats (Briand et al. 2005) or even temporary habitats like water storage ponds (author. unpubl. data), and in many ways exemplify the colloquialism “when the going gets tough, the tough get going”.
Energetically conservative
Many of the features listed in the above sections on adaptability and resilience result in reduced energy expenditure by eels—for example, being relatively inactive during daylight, and able to feed sporadically and endure prolonged fasts. Their acute olfactory sensitivity enables them to locate prey with precision, thus avoiding extensive searching behaviour; for larger individuals, adoption of piscivory means utilising larger prey species with high energy content, often captured from ambush using macrophyte beds for concealment (Burnet 1952), again reducing energy expenditure. Their use of cover and crevices for concealment avoids the need to maintain station in flowing water conditions, and this is even more evident in juvenile eels that spend most of their time within substrates (Burnet 1952; Glova and Jellyman 2000).
Eels employ a buccal pump system whereby the opercular chamber functions as a pump, enabling eels to respire while being immobile. Thus they can remain motionless for extended periods, whether diel (Baras et al. 1998; Jellyman and Sykes 2003) or seasonal (Westerberg and Sjoberg 2014). Their sinuous swimming action is energetically conservative and efficient for long distance travel (van Ginneken et al. 2005b). In swimming tube trials to study the effect of continuous swimming for 5500 km (equivalent to swimming from Europe to the Sargasso Sea), van Ginneken et al. (2005b) found that eels could accomplish this with expenditure of only 40% of their stored fat reserve (van Ginneken and van den Thillart 2000), and their swimming action was 4–6 times more efficient than non-eel-like fish. To use a human metaphor, eels are built for a marathon not a sprint.
Eels take advantage of passive transport from oceanic, tidal and river currents. Thus, leptocephali are largely carried along by favourable ocean currents, while glass eels use selective tidal transport to enter rivers and migrate upstream (Creutzberg 1961; Jellyman 1979). Silver eels usually emigrate downstream during periods of increased flow (e.g. Bruijs and Durif 2009) and mainly use the centre of main river channels to ensure they derive maximum benefit from currents (Euston et al. 1998; Jansen et al. 2007; Behrmann-Godel and Eckmann 2003) and avoid bankside obstacles. Even at sea, silver eels are known to use selective tidal stream transport (McCleave and Arnold 1999), and it is speculated that they may use directional tidal streams to cross the continental shelf (van Ginneken and Maes 2005).
Overall then, eels largely sedentary mode of life in freshwater, combined with an efficient swimming action and their widespread use of currents, means they are energetically conservative species, yet able to draw upon considerable reserves of stored energy when required for long distance migration. In many ways they epitomise Aesop's fable of the hare and tortoise that “slow and steady wins the race”.
Exploring the enigma
So, anguillids are a very successful genus, inhabiting many countries and a wide range of habitats, largely due to their extraordinary life history features of semelparous spawning and high fecundity, adaptability, resilience, and being energetically conservative. Given such physical and physiological versatility, it seems incongruous that the genus is in a parlous state worldwide. What has changed over the past few decades that has led to such a dramatic decline in the fortunes of these highly successful species?
The drastic reductions seen in stocks of many eel species may be largely a consequence of the reduced effectiveness of two fundamental life-history drivers, i.e. environmental determination of sex (EDS), and the need for surplus production (the Surplus Production Hypothesis, SPH). While the former process has been long known and extensively discussed (e.g. Beullens et al. 1997; Krueger and Oliveira 1999; Davey and Jellyman 2005; Melia et al. 2006), SPH is a new hypothesis and suggests that the risks associated with semelparous marine spawning are offset by surplus production of juveniles—a type of insurance against adversity.
In general, EDS is an advantageous mechanism and can ameliorate the effects of reduced stock levels. Limiting factors for successful spawning and subsequent recruitment to landmasses will be more associated with abundance of spawning females than males—theoretically, a few males could inseminate the total female spawner biomass (although in practice, spawning behaviour and disparate spawning locations will inevitably require the presence of many males). There is little reproductive advantage to males in achieving large size, and their strategy is one of growing as rapidly as possible to a size where they have the ability and enough stored energy to sustain a long-distance spawning migration (Helfman et al. 1987; Vollestad 1992). As eel stocks diminish, reduced densities will favour production of females, a feature of EDS that should provide some buffer against overall reduced numbers of fish. Thus, with reduced recruitment, populations have been found to change from male-dominated to female-dominated (Laffaille et al. 2006; Bark et al. 2007).
Surplus Production in Anguilla life history
Surplus production is suggested as an essential and allied component to EDS in eel life histories. Further, success of the Anguilla life history strategy is dependent upon a surplus in overall recruitment, and recruitment failure in turn has led to negative cascades in eel population size and reduced numbers of female silver eels.
SPH is demonstrable at spawning and recruitment of anguillids. High fecundity and mass spawning events should result in vast numbers of larvae. Essentially, semelparous spawning at distant locations is a “numbers game”, such that large number of offspring are required to ensure successful recruitment. Spawning over widespread areas (a 2000 km wide region for A. anguilla, Miller et al. 2019) could provide some buffer against localised spawning failure or development of unfavourable currents to transport larvae. Little is known about the behaviour and mortality of leptocephali—they can be found over vast areas (Miller et al. 2019) and their transparency presumably reduces the likelihood of predation (Miller 2009). Although they are capable swimmers and undergo diel vertical migrations (Miller 2009), there is no evidence that they form shoals, a feature that should enhance survival as shoals attract predators whereas it can be less energetically efficient for predators to pursue individual fish.
To arrive at continental destinations, leptocephali must become entrained in favourable currents. This process can be problematic. For instance, for A. japonica, the North Equatorial Current is the main vector transporting larvae westwards, but whether larvae then get transported north in the Kuroshio Current or south in the Mindanao Current depends on where the larvae are located in relation to the current bifurcation and the location of the salinity front (e.g. Kim et al. 2007). For A. rostrata, arrival at continental North America requires detrainment from the Gulf Stream, and failure to do so would result in continued transport towards Europe. Recent drift model simulations of larval A. anguilla and A. rostrata have indicated that the majority of leptocephali may become trapped in unfavourable areas of the Sargasso Sea and die, with only a small proportion becoming entrained in the Gulf Stream (Westerberg et al. 2018).Thus, high fecundity is required to compensate for the collective risks of larval mortality.
Importance of SPH
SPH would benefit eels in several ways:
-
Overall survival Eels are subject to mortality at all phases of their lives, whether in the open ocean or in fresh water. To be successful, semelparity requires a sufficient number of yellow eels to survive to silvering. Historically it is suggested that SPH provided an adequate safeguard against survival uncertainty, but of particular concern at present is the overlay of anthropogenic mortality upon an already risk-prone life history.
-
Predator satiation The synchronised shoaling behaviour of large numbers of glass eels and juvenile pigmented eels (elvers) migrating upstream will enhance their survival through predator satiation (e.g. Gill 2003). During such migrations, these juvenile eels are subject to a barrage of aquatic and avian predators (Leukona 2002; Jenkins and Harper 1980), but their sheer numbers will result in predators becoming satiated and confused (e.g. Ioannou et al. 2008) and enhance overall rates of survival.
-
Mass recruitment into estuarine areas is a trigger for subsequent upstream migration and dispersal of juveniles—the arrival of large numbers of new recruits into population-saturated areas results in density-dependent upstream migrations of previously-resident juveniles (Lobon-Cervia et al. 1995; Feunteun et al. 2003; Ibbotson et al. 2002; Briand et al. 2005; Edeline et al. 2007). Agonisitc behaviour and cannibalism will also reinforce such annual upstream migrations (Edeline et al. 2009). Annual upstream migrations will persist in individuals for several years (e.g. Naismith and Knights 1988; Jellyman and Ryan 1983). It is suggested that this process is an essential outcome of SPH as it results in colonisation of upstream parts of catchments where the reduced density of eels will result in a high proportion developing as females. The urge to migrate upstream will be reinforced by the odour of conspecifics (Galbraith et al. 2017)—reduced numbers of juvenile eels upstream would provide fewer olfactory cues and consequently fewer responses from downstream juveniles.
-
Reduced recruitment results in range contraction. As glass eel recruitment declines, it is most obvious at the extremes of the natural range—thus, recruitment to the Baltic Sea (both natural and by stocking) has declined by 95% between 1981 and 2012 (Westerberg and Wickström 2016). A number of studies of A. rostrata and A. anguilla have shown that the size of female silver eels increases and the proportion of males decreases with increasing latitude and distance from spawning areas (Helfman 1988; Oliveira 1999; Jessop 2010; Vøllestad 1992). As recruitment to such areas declines, the contribution of these large, fecund eels will be lost.
-
SPH ameliorates interannual variability in cohort strength. Unlike Pacific salmon (Oncorhynchus spp.) that spawn at pre-determined ages, female silver eels are comprised of multiple cohorts so the impact of periodic weak recruitment will not be discernible as a result of varying growth rates and ages at silvering.
A diagrammatic comparison of Anguilla historic (A) and present day (B) life history strategies (Fig. 1) shows the likely influence of EDS and SPH.
Vulnerability of SPH
A strategy like SPH is particularly vulnerable at two stages—a reduction in spawner biomass and variability in oceanic conditions that convey larvae back to inshore marine and freshwater habitats. Miller et al. (2016) proposed that a “perfect storm” of simultaneous oceanic changes and continental anthropogenic impacts could have led to recruitment reductions of northern hemisphere anguillids, with both sets of factors possibly acting synergistically. Variability in oceanic fronts (Miller et al. 2016), latitudes of bifurcation of currents (Zenimoto et al. 2009), and temperature and productivity changes associated with phase shifts in NAO (North Atlantic Oscillation) and ENSO (El Nino-Southern Oscillation) have all been associated with subsequent changes in juvenile eel recruitment (e.g. Knights 2003; Friedland et al. 2007; Bonhommeau et al. 2008a, b; Kettle et al. 2008; Durif et al. 2011; Arribas et al. 2012; Miller et al. 2016). The synchronous decline of northern hemisphere species over similar time scales points to widespread changes in oceanic conditions being a primary cause (Bonhommeau et al. 2008a; Drouineau et al. 2018). It is also possible that spawning over widespread areas means eels are subject to Allee effects whereby the chances of successful mating become drastically less as the number of available spawners declines (Poole et al. 2018), possibly as a result of failure to find mates or some behavioural aspects of social mating behaviour (Dekker 2008). Of course, all such marine life history lies beyond the sphere of immediate human influence, meaning that attempts at stock restoration must focus on the continental phase.
Maximising the production of female silver eels is proposed as the single most effective management tool for conservation of the genus, but to achieve this females have to survive a barrage of threats for many years. These threats include extensive habitat loss and fragmentation (e.g. Chen et al. 2014), accumulation of toxicants (Robinet and Feunteun 2002), transfers of parasites and diseases (Castonguay et al. 1994), barriers to movements (e.g. Laffaille et al. 2005; Piper et al. 2013), targeted fishing/overfishing by commercial and artisanal fishers (e.g. Jellyman 2014, 2016).
Upstream migrations of juvenile eels are often hindered by the lack of riverine connectivity due to weirs and dams; for example Busch et al. (1998) state that more than 15,000 dams have been built in North Atlantic coast drainages, blocking direct access to ∼87% of river and stream reaches flowing into the Atlantic, which has resulted in a greatly reduced inland range of the American eel (Miller and Casselman 2014). Restoration of connectivity via dam removal led Hitt et al. (2012) to conclude that restoring connectivity to headwater streams could increase eel population growth rates by increasing female eel numbers and fecundity.
Not only does reduced recruitment result in less upstream movement of juvenile eels and fewer females, but those females that do eventuate and become silver eels often have to run a gauntlet of dams, weirs, pumping station etc. before they are able to enter the sea. Again, much has been written about turbine mortality of female eels (e.g. McCleave 2001; Richkus and Dixon 2003; Verreault et al. 2004; Buysse et al. 2013; Heisey et al. 2019), and being relatively large with a tendency to follow paths of maximum flow (Euston et al. 1998; Jansen et al. 2007), female eels are very susceptible to entrainment and injury or death when they enter turbines. Eel size typically increases with distance inland (e.g. Smogor et al. 1995) so the largest and most fecund females travel the greatest distance and are consequently exposed the greatest risks. While many structural and behavioural systems have been trialled to prevent eels entering turbines (e.g. Richkus and Dixon 2003), unfortunately there is no “silver bullet” that can be universally applied. Consequently, injury rates and mortality can be up to 100% for larger eels (Haro et al. 2000; Carr and Whoriskey 2008; Boubée et al. 2008). Although there is currently no proven stock recruitment relationship (Feunteun 2002; Aström and Dekker 2007), insufficient spawning stock biomass has been suggested as a reason for recruitment collapse (Dekker 2003).
Over geological time scales, eel life histories have been very successful, enabling species divergence and colonisation of many landmasses. Presumably SPH played an important role in providing a numerical buffer against adverse conditions. However, today the impact of SPH is much diminished as eels face a variety of challenges to their survival within freshwater habitats. Superimposed on such challenges is variability in the marine environment, with the impacts of climate change uncertain but likely to be deleterious through lower primary productivity and changes in the strength of currents that provide larval transport (Knights 2003; Bonhommeau et al. 2008a, b; Miller et al. 2016). Irrespective of the causes, the net result has been widespread recruitment failure of several Anguilla spp. throughout much of the Anthropocene era.
In summary, it is proposed that the success of eels is largely due to a series of unique adaptations and life history features, of which adaptability, resilience, energetic conservatism, and environmental determination of sex are key features. It is suggested that these features have historically resulted in a significant over-production of juveniles, and that this SPH effectively drives the eel life history as the associated high densities of juvenile eels in freshwater provide the incentive for inland penetration and the development of females. Collectively these features have been sufficient to offset the considerable risks associated with eel life histories, whether that be arrival of silver eels at often distant spawning areas and finding suitable mates, survival by larvae of an extensive marine journey, accurate navigation to arrive at continental habitats (Jellyman and Bowen 2009), survival for many years in those habitats, and eventual egress to the sea (see summary, Table 4). The present declines in recruitment of many species reduces the incentive for such density-dependant upstream migrations, and most juveniles are expected to remain in the lower reaches of waterways where the propensity for rapid initial growth and high densities will result in a high proportion of eels developing as males (Holmgren 1996; Davey and Jellyman 2005). Should recruitment decline even further, it is possible that the resulting low densities could result in an increased proportion of eels developing as females in these lower reaches, a “last-ditch’ response that may partially offset the impact of reduced recruitment.
Proving the validity of SPH may be elusive. The hypothesis is intuitive and fits with observations of vast historical recruitment but drastically reduced recruitment of many species over recent decades, and also the longitudinal distribution of sexes within catchments. However, obtaining proof could require finding correlations between the strength of glass eel recruitment and subsequent upstream migration of juveniles. Additional support could come from examining a time series of otolith microchemistry of estuarine dwelling in yellow eels where a significant increase in the extent and duration of estuarine/lower river dwelling might indicate significant changes in life history patterns associated with levels of recruitment. Studying changes in the density and proportion of female eels following dam removal would also be informative.
The SPH hypothesis underscores the importance of conservative harvest of glass eels, habitat connectivity, and the need to ensure maximum female escapement. Where extensive stocking of juvenile eels is practiced, consideration should be given to stocking areas peripheral to the main geographic locations of eels, and stocking areas well upstream where eel densities are low; both techniques should result in increased development of females, an outcome critical to the ongoing survival of the genus Anguilla which is currently being driven towards extinction.
Change history
19 July 2021
A Correction to this paper has been published: https://doi.org/10.1007/s11160-021-09675-7
References
Abdul Kadir SR, Yamin L, Arai T (2017) Fecundity of the tropical catadromous eels Anguilla bicolor bicolor, A. bengalensis bengalensis and A. marmorata. Environ Biol Fish 100:1643–1648
Aoyama J, Wouthuyzen S, Miller MJ, Inagaki T, Tsukamoto K (2003) Short-distance spawning migration of tropical freshwater eels. Biol Bull 204:104–108
Arai T (2016) Spawning ground of tropical eels. In: Arai T (ed) Biology and ecology of anguillid eels. CRC Press, London, pp 89–107
Arai T (2020) Ecology and evolution of migration in the freshwater eels of the genus Anguilla Schrank, 1798. Heliyon 6(10):e05176
Arribas C, Fernández-Delgado C, Oliva-Paterna FJ, Drake P (2012) Oceanic and local environmental conditions as forcing mechanisms of the glass eel recruitment to the southernmost European estuary. Estuar Coast Shelf Sci 107:46–57
Astrőm M, Dekker W (2007) When will the eel recover? A full life-cycle model. ICES J Mar Sci 64:1491–1498
Baras E, Jeandrain D, Serouge B, Philippart JC (1998) Seasonal variations in time and space utilization by radio-tagged yellow eels Anguilla anguilla (L.) in a small stream. Hydrobiologia 371/372:187–198
Barbin GP, McCleave JD (1997) Fecundity of the American eel Anguilla rostrata at 45°N in Maine, U.S.A. J Fish Biol 51:840–847
Bark A, Williams B, Knights B (2007) Current status and temporal trends in stocks of European eel in England and Wales. ICES J Mar Sci 64:1368–1378
Béguer-Pon M, Benchetrit J, Castonguay M, Aarestrup K, Campana SE, Stokesbury MJW, Dodson JJ (2012) Shark predation on migrating adult American Eels (Anguilla rostrata) in the Gulf of St. Lawrence. PLoS ONE 7(10):e46830
Behrmann-Godel J, Eckmann R (2003) A preliminary telemetry study of the migration of silver European eel (Anguilla anguilla L.) in the River Mosel, Germany. Ecol Freshw Fish 12:196–202
Beullens K, Eding EH, Gilson P, Ollevier F, Komen J, Richter CJJ (1997) Gonadal differentiation, intersexuality and sex ratios of European eel (Anguilla anguilla L.) maintained in captivity. Aquaculture 153:135–150
Boetius I, Boetius J (1980) Experimental maturation of female silver eels, Anguilla anguilla. Estimates of fecundity and energy reserves for migration and spawning. Dana 1:1–28
Bonhommeau S, Chassot E, Rivot E (2008a) Fluctuations in European eel (Anguilla anguilla) recruitment resulting from environmental changes in the Sargasso Sea. Fish Oceanogr 17:32–44
Bonhommeau S, Chassot E, Planque B, Rivot E, Knap AH, Le Pape O (2008b) Impact of climate on eel populations of the Northern Hemisphere. Mar Ecol Prog Ser 373:71–80
Boubée J, Jellyman D, Sinclair C (2008) Eel protection measures within the Manapouri hydro-electric power scheme, South Island, New Zealand. Hydrobiologia 609:71–82
Briand C, Fatin D, Fontenelle G, Feunteun E (2005) Effect of re-opening of a migratory pathway for eel (Anguilla anguilla, L.) at a watershed scale. Bull Francais Peche Piscic 378(379):67–86
Bruijs MCM, Durif CMF (2009) Silver eel migration and behaviour. In: van den Thillart G, Dufour S, Rankin JC (eds) Spawning migration of the European eel. Springer, Dordrecht, pp 65–95
Burnet AMR (1952) Studies on the ecology of the New Zealand longfinned eel, Anguilla dieffenbachii Gray. Aust J Mar Freshw Res 3:32–63
Burnet AMR (1968) A study of the relationships between brown trout and eels in a New Zealand stream. NZ Mar Dep Fish Tech Rep 26:49
Busch WDN, Lary SJ, Castilione CM, McDonald RP (1998) Distribution and availability of Atlantic Coast freshwater habitats for American eel (Anguilla rostrata). Administrative Rep. No. 98–2, USFWS. Amherst, New York, 28 p
Buysse D, Mouton AM, Stevens M, Van den Neucker T, Coeck J (2013) Mortality of European eel after downstream migration through two types of pumping stations. Fish Manag Ecol 21:13–21
Cairns D (1941) Life-history of the two species of New Zealand freshwater eel. Part I. Taxonomy, age, growth, migration, and distribution. NZ J Sci 23:53–72
Carr JW, Whoriskey FG (2008) Migration of silver American eels past a hydroelectric dam and through a coastal zone. Fish Manag Ecol 15:393–400
Castle PHJ (1968) Anguilla obscura on Rennell Island. Nat Hist Rennell Island Br Solomon Islands 5:61–66
Castonguay M, Durif CMF (2016) Understanding the decline in anguillid eels. ICES J Mar Sci 73:1–4
Castonguay M, Hodson PV, Couillard CM, Eckersley MJ, Dutil J-D, Verreault G (1994) Why is recruitment of the American eel, Anguilla rostrata, declining in the St. Lawrence River and Gulf? Can J Fish Aquat Sci 51:479–488
Chen J-Z, Huang S-L, Han Y-S (2014) Impact of long-term habitat loss on the Japanese eel Anguilla japonica. Estuar Coast Shelf Sci 151:361–369
Cole LC (1954) The population consequences of life history phenomena. Quart Rev Biol 29:103–113
Cornish CJ (1902) The naturalist on the Thames. Seeley & Co., London
Creutzberg F (1961) On the orientation of migrating elvers (Anguilla vulgaris Turt.) in a tidal area. Neth J Sea Res 1:257–338
Daverat F, Limburg KE, Thibault I, Shiao JC, Dodson JJ, Caron FO, Tzeng W-N, Iizuka Y, Wickstrom H (2006) Phenotypic plasticity of habitat use by three temperate eel species, Anguilla anguilla, A. japonica and A. rostrata. Mar Ecol Prog Ser 308:231–241
Davey AJH, Jellyman DJ (2005) Sex determination in freshwater eels and management options for manipulation of sex. Rev Fish Biol Fish 15:37–52
Dekker W (2003) Did lack of spawners cause the collapse of the European eel, Anguilla anguilla? Fish Manag Ecol 10:365–376
Dekker W (2008) Coming to grips with the eel stock slip-sliding away. Am Fish Soc Symp 62:7–21
Dekker W (2009) A conceptual management framework for the restoration of the declining European eel stock. Am Fish Soc Symp 58:3–19
Dekker W, Beaulaton L (2016) Climbing back up what slippery slope? Dynamics of the European eel stock and its management in historical perspective. ICES J Mar Sci 73:5–13
Dörner H, Berg S (2016) Feeding ecology. In: Arai T (ed) Biology and ecology of anguillid eels. CRC Press, London, pp 171–191
Dou SZ, Yamada Y, Okamura A, Tanaka S, Shinoda A, Tsukamoto K (2007) Observations on the spawning behavior of artificially matured Japanese eels Anguilla japonica in captivity. Aquaculture 266:117–129
Downes TW (1918) Notes on eels and eel-weirs (tuna and pa-tuna). Trans Proc NZ Inst 50:296–316
Drouineau HD, Castonguay M, Mateo M, Rochard E, Verreault G, Yokouchi K, Lambert P (2018) Freshwater eels: a symbol of the effects of global change. Fish Fish 19:903–930
Duarte CM, Alcaraz M (1989) To produce many small or few large eggs: a size-independent reproductive tactic of fish. Oecologia 80:401–404
Durif CMF, Gjøsaeter J, Vøllestad LA (2011) Influence of oceanic factors on Anguilla anguilla (L.) over the twentieth century in coastal habitats of the Skagerrak, southern Norway. Proc R Soc B 278:464–473
Edeline E (2007) Adaptive phenotypic plasticity of eel diadromy. Mar Ecol Prog Ser 341:229–232
Edeline E, Beaulaton L, Le Barh R, Elie P (2007) Dispersal in metamorphosing juvenile eel Anguilla anguilla. Mar Ecol Prog Ser 344:213–218
Edeline E, DuFour S, Elie P (2009) Proximate and ultimate control of eel continental dispersal. In: van den Thillart G, Dufour S, Rankin JC (eds) Spawning migration of the European eel. Springer, Dordrecht, pp 433–461
Eldon GA (1968) Notes on the presence of the brown mudfish (Neochanna apoda Günther) on the west coast of the South Island of New Zealand. NZ J Mar Freshw Res 2:37–48
Euston ET, Royer DD, Simmons CL (1998) American eels and hydro plants: clues to eel passage. Hydrol Rev Aug 1998:94–103
Farley JH, Williams AJ, Hoyle SD, Davies CR, Nicol SJ (2013) Reproductive dynamics and potential annual fecundity of South Pacific albacore tuna (Thunnus alalunga). PLoS ONE 8(4):e60577
Feunteun E (2002) Management and restoration of European eel population (Anguilla anguilla): an impossible bargain. Ecol Eng 18:575–591
Feunteun E, Laffaille P, Robinet T, Briand C, Baisez A, Olivier J-M, Acou A (2003) A review of upstream migration and movements in inland waters by anguillid eels: toward a general theory. In: Aida K, Tsukamoto K, Yamauchi K (eds) Eel biology. Springer, Tokyo, pp 191–213
Flight WGF, Verheijen FJ (1993) The “neck-cut” (spinal transection): not a humane way to slaughter eel, Anguilla anguilla (L.). Aquacult Res 24:523–528
Forster ME (1981) Oxygen consumption and apnoea in the shortfin eel, Anguilla australis schmidtii. NZ J Mar Freshw Res 15:85–90
Friedland KD, Miller MJ, Knights B (2007) Oceanic changes in the Sargasso Sea and declines in recruitment of the European eel. ICES J Mar Sci 64:519–530
Galbraith HS, Blakeslee CJ, Schmucker AK, Johnson NS, Hansen MJ, Li W (2017) Donor life stage influences juvenile American eel Anguilla rostrata attraction to conspecific chemical cues. J Fish Biol 90:384–395
Geffroy B, Bardonnet A (2012) Differential effects of behaviour, propensity to migrate and recruitment season on glass eels and elvers’ growing performance. Ecol Freshw Fish 21:469–482
Gill AB (2003) The dynamics of prey choice in fish: the importance of prey size and satiation. J Fish Biol 63:105–116
Glova GJ, Jellyman DJ (2000) Size-related differences in diel activity of two species of juvenile eel (Anguilla) in a laboratory stream. Ecol Freshw Fish 9:210–218
Gousset B (1992) Eel culture in Japan. Spec Bull L’inst Oceanogr Monaco 10:1–128
Graynoth E, Taylor MJ (2000) Influence of different rations and water temperatures on the growth rates of shortfinned eels and longfinned eels. J Fish Biol 57:681–699
Haro A, Richkus W, Whalen K, Hoar A, Busch W-D, Lary S, Brush T, Dixon D (2000) Population decline of the American eel: implications for research and management. Fisheries 25:7–16
Heisey PG, Mathur D, Phipps JL, Avalos JC, Hoffman CE, Adams SW, De-Oliveira E (2019) Passage survival of European and American eels at Francis and propeller turbines. J Fish Biol 95:1172–1183
Helfman GS (1988) Patterns in the life history of anguillid eels. Verh Int Verein Theor Angew Limnol 23:1663–1669
Helfman GS, Clark JB (1986) Rotational feeding: overcoming gape-limited foraging in Anguillid eels. Copeia 3:679–685
Helfman GS, Facey DJ, Hales LS Jr, Bozeman EL Jr (1987) Reproductive ecology of the American eel. Am Fish Soc Symp 1:42–56
Hitt NP, Eyler S, Wofford JEB (2012) Dam removal increases American eel abundance in distant headwater streams. Trans Am Fish Soc 141:1171–1179
Holmgren K (1996) Effect of water temperature and growth variation on the sex ratio of experimentally reared eels. Ecol Freshw Fish 5:203–212
Hunt W (2007) The Victorian Elver wars. Reardon Publishing, Cheltenham
Ibbotson A, Smith J, Scarlett P, Aprahamian M (2002) Colonisation of freshwater habitats by the European eel Anguilla anguilla. Freshw Biol 47:1696–1706
ICES (2014) Report of the Joint EIFAAC/ICES/GFCM Working Group on Eel, 3–7 November (2014), Rome, Italy. ICES CM (2014)/ACOM: 18, 203 p
Ioannou CC, Tosh CR, Neville L, Krause J (2008) The confusion effect—from neural networks to reduced predation risk. Behav Ecol 19:126–130
Itakura H, Wakiya R, Gollock M, Kaifu K (2020) Anguillid eels as a surrogate species for conservation of freshwater biodiversity in Japan. Sci Rep 10:8790. https://doi.org/10.1038/s41598-020-65883-4
Itazawa Y (1960) Oxygen content of water in which eel suffers from surfacing or dyspnoea. Bull Jap Soc Sci Fish 26:960–965
IUCN (2017) The IUCN red list of threatened species. Version 2017-3. http://www.iucnredlist.org. Accessed July 2020
Jacoby DMP, Casselman JM, Crook V, DeLucia M-B, Ahn H, Kaifu K, Kurwi T, Sasa P, Silfvergrip AMC, Smith KG, Uchidal K, Walker AM, Gollock MJ (2015) Synergistic patterns of threat and the challenges facing global anguillid eel conservation. Global Ecol Cons 4:321–333
Jansen HM, Winter HV, Bruijs MCM, Polman HJG (2007) Just go with the flow? Route selection and mortality during downstream migration of silver eels in relation to river discharge. ICES J Mar Sci 64:1437–1443
Jellyman DJ (1977) Summer upstream migration of juvenile freshwater eels in New Zealand. NZ J Mar Freshw Res 11:61–71
Jellyman DJ (1979) Upstream migration of glass-eels (Anguilla spp.) in the Waikato River. NZ J Mar Freshw Res 13:13–22
Jellyman DJ (1989) Diet of two species of freshwater eel (Anguilla spp.) in Lake Pounui, New Zealand. NZ J Mar Freshw Res 23:1–10
Jellyman DJ (1991) Biology of the shortfinned eel Anguilla obscura in Lake Te Rotonui, Mitiaro, Cook Island. Pacific Sci 45:362–373
Jellyman DJ (1995) Longevity of longfinned eels Anguilla dieffenbachii in a New Zealand high country lake. Ecol Freshw Fish 4:106–112
Jellyman DJ (2014) Freshwater eels and people in New Zealand—a love/hate relationship. In: Tsukamoto K, Kuroki M (eds) Eels and humans. Spinger Verlag, Tokyo, pp 143–153
Jellyman DJ (2016) Management and fisheries of Australasian eels (Anguilla australis, Anguilla dieffenbachii, Anguilla reinhardtii). In: Arai T (ed) Biology and ecology of anguillid eels. CRC Press, London, pp 274–290
Jellyman DJ, Arai T (2016) Juvenile eels; upstream migration and habitat use. In: Arai T (ed) Biology and ecology of anguillid eels. CRC Press, London, pp 143–170
Jellyman DJ, Bowen M (2009) Modelling larval migration routes and spawning areas of Anguillid eels of New Zealand and Australia. Am Fish Soc Symp 69:255–274
Jellyman DJ, Briand C (2016) Glass eels. In: Arai T (ed) Biology and ecology of anguillid eels. CRC Press, London, pp 108–142
Jellyman DJ, Ryan CM (1983) Seasonal migration of elvers (Anguilla spp.) into Lake Pounui, New Zealand, 1974–1978. N Z J Mar Freshw Res 17:1–15
Jellyman DJ, Sykes JRE (2003) Diel and seasonal movements of radio-tagged freshwater eels, Anguilla spp., in two New Zealand streams. Environ Biol Fish 66:143–154
Jellyman DJ, Unwin MJ (2017) Diel and seasonal movements of silver eels, Anguilla dieffenbachii, emigrating from a lake subject to hydro-electric control. J Fish Biol 91:219–241
Jellyman DJ, Unwin MJ (2019) Fine- scale swimming movement and behaviour of female silver eels, Anguilla dieffenbachii, within a lake affected by hydro- power generation. Fish Manag Ecol 26:57–69
Jellyman DJ, Bonnett ML, Sykes JRE, Johnstone P (2003) Contrasting use of daytime habitat by two species of freshwater eel (Anguilla spp.) in New Zealand rivers. Am Fish Soc Symp 33:63–78
Jenkins D, Harper RJ (1980) Ecology of otters in Northern Scotland: II. Analyses of otter (Lutra lutra) and mink (Mustela vision) faeces from Deeside, N.E. Scotland in 1977–78. J Anim Ecol 49:737–754
Jessop BM (2010) Geographic effects on American eel (Anguilla rostrata) life history characteristics and strategies. Can J Fish Aquat Sci 67:326–346
Jessop BM (2018) American eel fecundity and ovary maturation in relation to body size and geographic distribution. Mar Coastal Fish 10:169–189
Jessop BM, Cairns DK, Thibault I, Tzeng W-N (2008) Life history of the American eel Anguilla rostrata: new insights from otolith micrchemsitry. Aquat Biol 1:205-216
Johnson JH, Nack CC (2013) Habitat use of American eel (Anguilla rostrata) in a tributary of the Hudson River, New York. J Appl Ichth 29:1073–1079
Kaifu K, Stein F, Dekker W, Walker N, Dolloff CA, Steele K, Aguirre AA, Nijman V, Siriwat P, Sasal P (2019) Global exploitation of freshwater eels (genus Anguilla): fisheries, stock status and illegal trade. In: Don A, Coulson P (eds) Eels. Biology, monitoring, management, culture and exploitation. Proceedings of the first international eel science symposium. 5m Publishing, Sheffield, pp 377–422
Kettle AJ, Bakker DCE, Haines K (2008) Impact of the North Atlantic Oscillation on the trans-Atlantic migrations of the European eel (Anguilla anguilla). J Geophys Res 113:G03004
Kettle AJ, Vollestad LA, Wibig J (2011) Where once the eel and the elephant were together: decline of the European eel because of changing hydrology in southwest Europe and northwest Africa? Fish Fish 12:380–411
Kim H, Kimura S, Shinoda A, Kitagawa T, Sasai Y, Sasaki H (2007) Effect of El Niño on migration and larval transport of the Japanese eel (Anguilla japonica). ICES J Mar Sci 64:1387–1395
Knights B (1987) Agonistic behaviour and growth in the European eel, Anguilla anguilla L., in relation to warm-water aquaculture. J Fish Biol 31:263–276
Knights B (2003) A review of the possible impacts of long-term oceanic and climate changes and fishing mortality on recruitment of anguillid eels of the Northern Hemisphere. Sci Total Environ 310:237–244
Krueger WH, Oliveira K (1999) Evidence for environmental sex determination in the American eel, Anguilla rostrata. Environ Biol Fish 55:381–389
Kruuk H (2014) Otters and eels: long-term observations on declines in Scotland. IUCN Otter Spec Group Bull 31:1–11
Kurogi H, Okazaki M, Mochioka N, Jinbo T, Hashimoto H, Takahashi M, Tawa A, Aoyama J, Shinoda A, Tsukamoto K, Tanaka H, Gen K, Kazeto Y, Chow S (2011) First capture of post-spawning female of the Japanese eel Anguilla japonica at the southern West Mariana Ridge. Fish Sci 77:199–205
Laffaille P, Feunteun E, Baisez A, Robinet T, Acou A, Legault A, Lek S (2003) Spatial organisation of European eel (Anguilla anguilla L.) in a small catchment. Ecol Freshw Fish 12:254–264
Laffaille P, Acou A, Guilloue J, Legault A (2005) Temporal changes in European eel, Anguilla anguilla, stocks in a small catchment after installation of fish passes. Fish Manag Ecol 12:123–129
Laffaille P, Acou A, Guioullet J, Mounaix B, Legault A (2006) Patterns of silver eel (Anguilla anguilla L.) sex ratio in a catchment. Ecol Freshw Fish 15:583–588
Lekuona JM (2002) Food intake, feeding behaviour and stock losses of cormorants, Phalacrocorax carbo, and grey herons, Ardea cinerea, at a fish farm in Arcachon Bay (Southwest France) during breeding and non-breeding season. Folia Zool 51:23–34
Lobon-Cervia J, Utrilla CG, Rincon PA (1995) Variations in the population dynamics of the European eel Anguilla anguilla (L.) along the course of a Cantabrian river. Ecol Freshw Fish 4:17–27
Luo M, Guan R, Li Z, Jin H (2013) The effects of water temperature on the survival, feeding, and growth of the juveniles of Anguilla marmorata and A. bicolor pacifica. Aquaculture 400:61–64
MacNamara R, McCarthy TK (2012) Size-related variation in fecundity of European eel (Anguilla anguilla). ICES J Mar Sci 69:1333–1337
MacNamara R, McCarthy TK, Wickström H, Clevestam PD (2016) Fecundity of silver-phase eels (Anguilla anguilla) from different habitat types and geographic locations. ICES J Mar Sci 73:135–141
McCarthy TK (2014) Eels and people in Ireland: from mythology to international eel stock conservation. In: Tsukamoto K, Kuroki M (eds) Eels and humans. Springer, Tokyo, pp 13–40
McCleave JD (2001) Simulation of the impact of dams and fishing weirs on reproductive potential of silver-phase American eels in the Kennebec River basin, Maine. N Am J Fish Manag 21:592–605
McCleave JD, Arnold GP (1999) Movement of yellow and silver-phase European eels (Anguilla anguilla L.) tracked in the western North Sea. ICES J Mar Sci 56:510–536
McCosker JE, Bustamante RH, Wellington GM (2003) The freshwater eel, Anguilla marmorata, discovered at Galápagos. Not De Galápagos 62:2–6
McKenzie DJ, Piccolella M, DallaValle AZ, Taylor EW, Bolis CL, Steffensen JF (2002) Tolerance of acute hypercapnic acidosis by the European eel (Anguilla anguilla). J Comp Physiol B 172:339–346
Matsui I (1952) Studies on the morphology, ecology and pond culture of the Japanese eel (Anguilla japonica Temminck and Schlegel). J Shimonoseki Coll Fish 2:1–245
Melia P, Bevacqua D, Crivelli AJ, Panfili J, De Leo GA, Gatto M (2006) Sex differentiation of the European eel in brackish and freshwater environments: a comparative analysis. J Fish Biol 69:1228–1235
Miller MJ (2009) Ecology of anguilliform leptocephali: remarkable transparent fish larvae of the ocean surface layer. Aqua-BioSci Mono 2:1–94
Miller MJ, Casselman J (2014) The American eel: a fish of mystery and sustenance for humans. In: Tsukamoto K, Kuroki M (eds) Eels and humans. Springer, Tokyo, pp 155–169
Miller MJ, Feunteun E, Tsukamoto K (2016) Did a “perfect storm” of oceanic changes and continental anthropogenic impacts cause northern hemisphere anguillid recruitment reductions? ICES J Mar Sci 73:43–56
Miller MJ, Kimura S, Friedland KD, Knights B, Kim H, Jellyman DJ, Tsukamoto K (2009) Review of ocean-atmospheric factors in the Atlantic and Pacific oceans influencing spawning and recruitment of anguillid eels. Am Fish Soc Symp 69:231–249
Miller MJ, Westerberg H, Sparholt H, Wysujack K, Sørensen SR, Marohn L, Jacobsen MW, Freese M, Ayala DJ, Pohlmann J-D, Svendsen JC, Watanabe S, Andersen L, Møller PR, Tsukamoto K, Munk P, Hanel R (2019) Spawning by the European eel across 2000 km of the Sargasso Sea. Biol Lett 15:20180835
Minegishi Y, Aoyama J, Inoue JG, Miya M, Nishida M, Tsukamoto K (2005) Molecular phylogeny and evolution of the freshwater eels genus Anguilla based on the whole mitochondrial genome sequences. Mol Phyl Evol 34:134–146
Monticini P (2014) Eel (Anguilla spp.): Production and trade according to Washington Convention Legislation. FAO Globefish Research Programme 114, 78 p
Naismith IA, Knights B (1988) Migrations of elvers and juvenile European eels, Anguilla anguilla L., in the River Thames. J Fish Biol 33:161–175
Nijman V, Siriwat P (2020) Distribution and conservation status of tropical eels. In: Don A, Coulson P (eds) Eels. Biology, monitoring, management, culture and exploitation. Proceedings of the first international eel science symposium. 5m Publishing, Sheffield, pp 24–32
Nikolic N, Bagliniere JL, Rigaud C, Gardes C, Masquilier ML, Taverny C (2011) Bibliometric analysis of diadromous fish research from 1970s to 2010: a case study of seven species. Scientometrics 88:929–947
Oliveira K (1999) Life history characteristics and strategies of the American eel, Anguilla rostrata. Can J Fish Aquat Sci 56:795–802
Oliveira K, McCleave JD (2000) Variation in population and life history traits of the American eel, Anguilla rostrata, in four rivers in Maine. Environ Biol Fish 59:141–151
Olivereau M, Olivereau JM (1997) Long-term starvation in the European eel: general effects and responses of pituitary growth hormone-(GH) and somatolactin-(SL) secreting cells. Fish Phys Biochem 17:261–269
Piper AT, Wright RM, Walker AM, Kemp PS (2013) Escapement, route choice, barrier passage and entrainment of seaward migrating European eel, Anguilla anguilla, within a highly regulated lowland river. Ecol Eng 57:88–96
Poole WR, Diserud OH, Thorstad EB, Durif CM, Dolan C, Sandlund OT, Bergesen K, Rogan G, Kelly S, Vøllestad LA (2018) Long-term variation in numbers and biomass of silver eels being produced in two European river systems. ICES J Mar Sci 75:1627–1637
Richardson J, Boubée JAT, West DW (1994) Thermal tolerance and preference of some native New Zealand freshwater fish. NZ J Mar Freshw Res 28:399–407
Richkus WA, Dixon DA (2003) Review of research and technologies on passage and protection of downstream migrating catadromous eels at hydroelectric facilities. Am Fish Soc Symp 33:377–388
Righton D, Roberts M (2014) Eels and people in the United Kingdom. In: Tsukamoto K, Kuroki M (eds) Eels and humans. Spinger, Tokyo, pp 1–12
Righton D, Westerberg H, Feunteun E, Økland F, Gargan P, Amilhat E, Metcalfe J, Lobon-Cervia J, Sjöberg N, Simon J, Acou A, Vedor M, Walker A, Trancart T, Brämick U (2016) Aarestrup K (2016) Empirical observations of the spawning migration of European eels: the long and dangerous road to the Sargasso Sea. Sci Adv 2:e1501694
Robinet TT, Feunteun EE (2002) Sublethal effects of exposure to chemical compounds: a cause for the decline in Atlantic eels? Ecotoxicol 11:265–277
Rowe DK, Chisnall BL, Dean TL, Richardson J (1999) Effects of land use on native fish communities in east coast streams of the North Island of New Zealand. NZ J Mar Freshw Res 33:141–151
Sadler K (1979) Effects of temperature on the growth and survival of the European eel, Anguilla anguilla L. J Fish Biol 15:499–507
Sagar PM, Graynoth E, Glova GJ (2005) Prey selection and dietary overlap of shortfinned (Anguilla australis) and longfinned (A. dieffenbachii) eels during summer in the Horokiwi Stream, New Zealand. NZ J Mar Freshw Res 39:931–939
Skead CJ (1959) The climbing of juvenile eels. Piscator 46:74–86
Smogor RA, Angermeier PL, Gaylord CK (1995) Distribution and abundance of American eels in Virginia streams: tests of null models across spatial scales. Trans Am Fish Soc 124:789–803
Sugeha HY, Aoyama J, Tsukamoto K (2001) First report on the silver eels of Anguilla marmorata (Quoy & Gaimard) from central Sulawesi Island, Indonesia. In: Aida K, Tsukamoto K, Yamauchi K (eds) Proceedings of the international symposium, advances in eel biology. University of Tokyo, pp 137–139
Székely C, Palstra A, Molnar K, van den Thillart G (2009) Impact of the swim-bladder parasite on the health and performance of European eels. In: van den Thillart G, Dufour S, Rankin JC (eds) Spawning migration of the European eel. Springer, Dordrecht, pp 201–226
Tesch F-W (2003) The eel. Blackwell Science Ltd, Oxford
Todd PR (1980) Size and age of migrating New Zealand freshwater eels (Anguilla spp.). NZ J Mar Freshw Res 14:283–293
Todd PR (1981) Morphometric changes, gonad histology, and fecundity estimates in migrating New Zealand freshwater eels (Anguilla spp.). NZ J Mar Freshw Res 15:155–170
Tomie JPN, Cairns DK, Hobbs RS, Desjardins M, Fletcher GL, Courtenay SC (2016) American eel (Anguilla rostrata) substrate selection for daytime refuge and winter thermal sanctuary. Mar Freshw Res 68:95–105
Tremblay V (2009) Reproductive strategy of female American eels among five subpopulations in the St. Lawrence River watershed. Am Fish Soc Symp 58:85–201
Tseng M-C (2016) Overview and current trends in studies on the evolution and phylogeny of Anguilla. In: Arai T (ed) Biology and ecology of anguillid eels. CRC Press, London, pp 21–35
Tsukamoto K, Arai T (2001) Facultative catadromy of the eel Anguilla japonica between freshwater and seawater habitats. Mar Ecol Prog Ser 220:265–276
Tsukamoto K, Kuroki M (eds) (2014) Eels and humans. Springer, Japan, p 177
van den Thillart G, Palstra A, van Ginneken V (2009) Energy requirements of European eel for trans Atlantic spawning migration. In: van den Thillart G, Dufour S, Rankin JC (eds) Spawning migration of the European eel. Springer, Dordrecht, pp 179–199
van Ginneken V, van den Thillart G (2000) Eel fat stores are enough to reach the Sargasso. Nature 403:156–157
van Ginneken VJT, Maes GE (2005) The European eel (Anguilla anguilla, Linnaeus), its lifecycle, evolution and reproduction: a literature review. Rev Fish Biol Fish 15:367–398
van Ginneken VJT, Onderwater M, Olivar OL, van den Thillart GEEJ (2001) Metabolic depression and investigation of glucose/ethanol conversion in the European eel (Anguilla anguilla Linnaeus 1758) during anaerobiosis. Thermochim Acta 373:23–30
van Ginneken V, Antonissen E, Muller UK, Booms R, Eding E, Verreth J, van den Thillart G (2005a) Eel migration to the Sargasso: remarkably high swimming efficiency and low energy costs. J Exp Biol 208:1329–1335
van Ginneken V, Vianen G, Muusze B, Palstra A, Verschoor L, Lugten O, Onderwater M, van Schie S, Niemantsverdriet P, van Heeswijk R, Eding E, van den Thillart G (2005b) Gonad development and spawning behaviour of artificially-matured European eel (Anguilla anguilla L.). Anim Biol 55:203–218
Verreault G, Dumont P, Mailhot Y (2004) Habitat losses and anthropogenic barriers as a cause of population decline for American eel (Anguilla rostrata) in the St. Lawrence watershed, Canada. ICES CM 2004/S:04
Vollestad LA (1992) Geographic variation in age and length at metamorphosis of maturing European eel: environmental effects and phenotypic plasticity. J An Ecol 61:41–48
Wahlberg M, Westerberg H, Aarestrup K, Feunteun E, Gargan P, Righton D (2014) Evidence of marine mammal predation of the European eel (Anguilla anguilla L.) on its marine migration. Deep-Sea Res Part I 86:32–38
Walsh PJ, Foster GD, Moon TW (1983) The effects of temperature on the metabolism of the American eel Anguilla rostrata (LeSueur): compensation in the summer and torpor in the winter. Phys Zool 56:532–540
Walsh CT, Pease BC, Booth DJ (2004) Variation in the sex ratio, size and age of longfinned eels within and among coastal catchments of south-eastern Australia. J Fish Biol 64:1297–1312
Wenner CA, Musick JA (1974) Fecundity and gonad observations of the American eel, Anguilla rostrata, migrating from Chesapeake Bay, Virginia. J Fish Res Board Can 31:1387–1391
Westerberg H, Sjoberg N (2014) Overwintering dormancy of the European eel (Anguilla anguilla L.) in a large lake. Ecol Freshw Fish 24:542–543
Westerberg H, Wickström H (2016) Stock assessment of eels in the Baltic: reconciling survey estimates to achieve quantitative analysis. ICES J Mar Sci 73:75–83
Westerberg H, Pacariz S, Marohn L, Fagerström V, Wysujack K, Miller MJ, Freese M, Pohlmann J-D, Hanel R (2018) Modeling the drift of European (Anguilla anguilla) and American (Anguilla rostrata) eel larvae during the year of spawning. Can J Fish Aquat Sci 75:224–234
Wood SC, Johansen K (1973) Blood oxygen transport and acid-base balance in eels during hypoxia. Am J Phys 225:849–851
Zenimoto K, Kitagawa T, Miyazaki S, Sasai Y, Sasak H, Kimura S (2009) The effects of seasonal and interannual variability of oceanic structure in the western Pacific North Equatorial Current on larval transport of the Japanese eel Anguilla japonica. J Fish Biol 74:1878–1890
Acknowledgements
I thank James McCleave, The University of Maine, for helpful comments on an earlier version of this manuscript.
Funding
Not applicable.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The author declares that there is no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Jellyman, D.J. An enigma: how can freshwater eels (Anguilla spp.) be such a successful genus yet be universally threatened?. Rev Fish Biol Fisheries 32, 701–718 (2022). https://doi.org/10.1007/s11160-021-09658-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11160-021-09658-8