Comparative lever analysis and ontogenetic scaling in esocid fishes: Functional demands and constraints in feeding biomechanics

When animals grow, the functional demands that they experience often change as a consequence of their increasing body size. In this study, we examined the feeding biomechanics in esocid species that represent different size classes (small, Esox americanus; intermediate, Esox niger; large, Esox lucius), and how their bite forces and associated functional variables change as they grow. In order to evaluate bite performance through ontogeny, we dissected and measured dimensions of the feeding apparatus and the adductor mandibulae muscle complex with its segmentum facialis subdivisions such as the ricto‐malaris, stegalis and endoricto‐malaris across a wide range of body sizes. The collected morphological data was used as input variables for a published anatomical model to simulate jaw function in these fish species. Maximum bite forces for both anterior bite and posterior bite increased in isometry in E. americanus and E. niger. The posterior bite of E. lucius also increases in isometry, however, the anterior bite increases in positive allometry. Intraspecific comparison within E. lucius indicated the increase of bite forces in more developed individuals accelerated after the fish grew out of fingerling stage. In addition, our analysis indicated functional differentiation between subdivisions of the adductor mandibulae segmentum facialis, as well as interspecific differences in the pattern of contribution to the bite performance by these subdivisions. Our study provides insights into not only the musculoskeletal basis of the jaw function of esocid species, but also the feeding capacity of this species in relation to the functional demands it faces as one of the top predators in lake and river systems. J. Morphol. 277:1447–1458, 2016. © 2016 Wiley Periodicals, Inc.     

Immunohistochemical localization of cyclic AMP and ultrastructural demonstration of adenylate cyclase activity in the testis of Esox lucius at time of spermiation

Summary In the testis of Esox lucius at the time of spermiation, activity of cyclic adenosine 3,5-monophosphate (cAMP) was immunocytochemically localized at the level of the Sertoli cells. In these cells adenylate cyclase activity was also ultracytochemically demonstrated by using adenylyl imidodiphosphate as a substrate. Reaction products of adenylate cyclase were primarily detectable on the basal and adluminal plasma membranes and on the surface of protrusions of the cell body into the lumen.     

Using accelerometry to quantify prey attack and handling behaviours in piscivorous pike Esox lucius

Accelerometer technology was used to evaluate behaviours in the teleost ambush predator pike Esox lucius foraging on crucian carp Carassius carassius. Automated rule‐based estimates of prey‐size determined handling time were obtained and are compared with video‐recorded behaviours. Solutions to tag attachment and the limitations imposed by battery‐time and data‐logging capacities are evaluated.     

Development of microsatellite markers for muskellunge (Esox masquinongy) and cross‐species amplification in two other esocids

We report the development of seven polymorphic microsatellite loci in muskellunge (Esox masquinongy) using an unenriched subgenomic library. Polymorphic loci exhibited 2–11 alleles with observed heterozygosities ranging from 0.190 to 0.917 (n = 24). All seven loci amplified by their respective primer pairs resulted in monomorphic products in northern pike (E. lucius) whereas three loci amplified monomorphic products in grass pickerel (E. americanus americanus); these results imply conservation of flanking sequence but loss of polymorphism between these closely related species. Only one of six microsatellite primers developed in a previous study in northern pike amplified polymorphic products in muskellunge.     

Prey selection by the larvae of three species of littoral fishes on natural zooplankton assemblages

The prey selection of larvae of three common littoral fish species (pike, Esox lucius; roach,Rutilus rutilus; and three-spined stickleback, Gasterosteus aculeatus) was studied experimentally in the laboratory by using natural zooplankton assemblages. Zooplankton prey was offered at four different concentrations to study the functional responses of the planktivores. The diets of pike and sticklebacks were formed mainly of copepod juveniles and adults, which dominated the prey communities, although sticklebacks ate also cladocerans. The diet of roach larvae consisted of rotifers, cladocerans and copepods, without prey selection, in equal proportions indicating a more omnivorous diet. All fish larvae were able to feed selectively although in sticklebacks prey selection was less pronounced. Pike and roach larvae preferred large prey to smaller prey types. Patterns of prey selection are discussed in the context of size-selection theory and apparent vs. true selection.     

Pike Esox lucius as an emerging model organism for studies in ecology and evolutionary biology: a review

The pike Esox lucius is a large, long‐lived, iteroparous, top‐ predator fish species with a circumpolar distribution that occupies a broad range of aquatic environments. This study reports on a literature search and demonstrates that the publication rate of E. lucius research increases both in absolute terms and relative to total scientific output, and that the focus of investigation has changed over time from being dominated by studies on physiology and disease to being gradually replaced by studies on ecology and evolution. Esox lucius can be exploited as a model in future research for identifying causes and consequences of phenotypic and genetic variation at the levels of individuals, populations and species as well as for investigating community processes.     

Food web manipulation in a small,eutrophic Lake Wirbel,Poland: effect of stocking with juvenile pike on planktivorous fish

In a four year experiment (1988–1991) carried out in a shallow, eutrophic lake, an increase in young-of-the-year pike (Esox lucius) density was used to control planktivorous fish assemblages consisting mainly of small-sized cyprinids: roach (Rutilus rutilus), Leucaspius delineatus, and white bream (Blicca bjoerkna). Stocking with pike fry of ca 30 mm in three successive springs resulted in large-scale mortality among prey of vulnerable sizes. Rotenone treatment at the end of the fourth year showed that roach and white bream populations contained few 0+ to 2+ fish, but very high numbers of 3+ to 6+ fish. By this time, short-lived, slow-growing L. delineatus, with no size refuge from predators, had been driven almost to extinction.     

Five new microsatellite markers for Northern pike (Esox lucius)

Five new microsatellite markers were isolated from Northern pike (Esox lucius), a freshwater fish widely distributed in both Northern Europe and Northern America. Characterization in 30 individuals from a population from France revealed four to seven alleles and an expected heterozygosity of 0.243–0.642. No departure from Hardy–Weinberg equilibrium nor linkage disequilibrium were found. The level of polymorphism was higher than previously reported in the literature for pike populations from Northern America and Northern Europe, but with different microsatellite loci.     

Molecular analysis of ependymins from the cerebrospinal fluid of the orders clupeiformes and salmoniformes: no indication for the existence of an euteleost infradivision

Summary Ependymins represent the predominant protein constituents in the cerebrospinal fluid of many teleost fish and they are synthesized in meningeal fibroblasts. Here, we present the ependymin sequences from the herring (Clupea harengus) and the pike (Esox lucius). A comparison of ependymin homologous sequences from three different orders of teleost fish (Salmoniformes, Cypriniformes, and Clupeiformes) revealed the highest similarity between Clupeiformes and Cypriniformes. This result is unexpected because it does not reflect current systematics, in which Clupeiformes belong to a separate infradivision (Clupeomorpha) than Salmoniformes and Cypriniformes (Euteleostei). Furthermore, in Salmoniformes the evolutionary rate of ependymins seems to be accelerated mainly on the protein level. However, considering these inconstant rates, neither neighbor joining trees nor DNA parsimony methods gave any indication that a separate euteleost infradivision exists.     

Non-lethal sampling for stable isotope analysis of pike Esox lucius: how mucus,scale and fin tissue compare to muscle

Stable isotope analysis (SIA) was used to examine the isotopic relationships between dorsal muscle and fin, scale and epidermal mucus in pike Esox lucius. δ¹³C and δ¹⁵N varied predictably within each tissue pairing, with conversion factors calculated for the surrogate tissues, enabling their application to the non-lethal sampling of E. lucius for SIA.     

Habitat utilisation by pike Esox lucius L. during winter floods in a southern English chalk river

Seven pike Esox lucius L., implanted with radio-transmitters, were tracked throughout autumn and winter in the River Frome, a southern English chalk river. During the first flood events of the year, pike remained within the main river channel but during subsequent flood events, pike could also be found in flooded fields, in drainage ditches or in a millstream. Eighty percent of the fixes over flooded land occurred within 10 m of the riverbank, although distances of up to 89 m from the bank were recorded. In ditches, pike could be found over 250 m from the main river. For pike in ditches and flooded fields, distance from the main river channel was positively correlated with discharge. There was individual variation amongst pike for the habitat types selected, with some pike utilising flooded field or ditch habitat more often than others. The proportion of time spent out of the main river channel does not appear to be related to the size of the pike. It is hypothesised that pike are leaving the main river channel to exploit feeding opportunities in the flooded fields and drainage ditches, rather than using these areas as refugia from high flow conditions.     

Short‐term evaluation of visible implant alpha tags in juveniles of three fish species under laboratory conditions

Visible implant alpha (VI alpha) tag‐induced changes in mortality and condition, as well as tag retention and readability, were examined during a 4‐week period for juveniles of three fish species: tiger muskellunge Esox masquinongy × Esox lucius (91 ± 7 mm total length, L_T, mean ± s.d.), Snake River cutthroat trout Oncorhynchus clarki behnkei (84 ± 8 mm) and rainbow trout Oncorhynchus mykiss (85 ± 5 mm). Mortality and condition did not differ between tagged fish and control fish for any species and overall tag retention rates were high (92% for E. masquinongy × E. lucius, 91% for O. c. behnkei and 100% for O. mykiss). Short‐term readability of VI alpha tags was low in juvenile E. masquinongy × E. lucius and juvenile O. c. behnkei. Therefore, it is not recommend to use VI alpha tags in juvenile E. masquinongy × E. lucius or juvenile O. c. behnkei for periods >2 weeks, but VI alpha tags seem to be suitable for juvenile O. mykiss for a period of at least 4 weeks.     

Behaviour in a standardized assay,but not metabolic or growth rate,predicts behavioural variation in an adult aquatic top predator Esox lucius in the wild

This study tested for links among behaviour, state and life‐history variables as predicted by the pace‐of‐life hypothesis in adult pike Esox lucius. First, a standardized open‐field behavioural assay was developed to assess individual behaviour of wild‐captured adult E. lucius. Behaviour within the standardized assay predicted swimming behaviour in the lake, providing an ecological validation of the assay. There was no relationship between standardized behaviour and any of the life‐history and state variables, including metabolism, body condition, juvenile growth rate and adult growth rate in contrast to predictions from the pace‐of‐life hypothesis. This study demonstrates that it is possible to assess ecologically relevant behavioural variation in a large‐bodied top predator using a standard open‐field assay, but it is noteworthy that this standardized behaviour is not systematically related to standard metabolism or growth.     

Initial mortality of radio-tagged Atlantic salmon (Salmo salar L.) smolts following release downstream of a hydropower station

The fate of radio-tagged hatchery-reared salmon smolts (Salmo salar L.) was investigated in the tailrace of a hydropower station in the Danish River Gudenaa during 2 years. Seventeen and 27 smolts were tagged and released in late May 1996 and during April 1999, respectively. Out of the total of 44 smolts, only two were recorded to leave the river and enter the estuary. In both years of study, electrofishing was used to sample tagged smolts. In 1996, these attempts were unsuccessful, while in 1999, 19 (70% of total) transmitters were retrieved in the stomachs of pikeperch (Stizostedion lucioperca (L.)) and pike (Esox lucius L.), and in grey heron (Ardea cinerea L.) nests. The present study demonstrates that the physical condition of the watershed, with respect to spawning and rearing, may not be the only crucial determining factors of the success of reintroduction of Atlantic salmon. Hydropower plants not only block the free movement of migratory fish, hence preventing the utilisation of spawning and rearing areas, but also form the basis of areas with increased mortality.     

Photoreceptors and eyes of pikeperch Sander lucioperca,pike Esox lucius,perch Perca fluviatilis and roach Rutilus rutilus from a clear and a brown lake

The photoreceptors and eyes of four fish species commonly cohabiting Fennoscandian lakes with different light transmission properties were compared: pikeperch Sander lucioperca, pike Esox lucius, perch Perca fluviatilis and roach Rutilus rutilus. Each species was represented by individuals from a clear (greenish) and a humic (dark brown) lake in southern Finland: Lake Vesijärvi (LV; peak transmission around 570 nm) and Lake Tuusulanjärvi (LT; peak transmission around 630 nm). In the autumn, all species had almost purely A2-based visual pigments. Rod absorption spectra peaked at c.526 nm (S. lucioperca), c. 533 nm (E. lucius) and c. 540 nm (P. fluviatilis and R. rutilus), with no differences between the lakes. Esox lucius rods had remarkably long outer segments, 1.5–2.8-fold longer than those of the other species. All species possessed middle-wavelength-sensitive (MWS) and long-wavelength-sensitive (LWS) cone pigments in single, twin or double cones. Rutilus rutilus also had two types of short-wavelength sensitive (SWS) cones: UV-sensitive [SWS1] and blue-sensitive (SWS2) cones, although in the samples from LT no UV cones were found. No other within-species differences in photoreceptor cell complements, absorption spectra or morphologies were found between the lakes. However, E. lucius eyes had a significantly lower focal ratio in LT compared with LV, enhancing sensitivity at the expense of acuity in the dark-brown lake. Comparing species, S. lucioperca was estimated to have the highest visual sensitivity, at least two times higher than similar-sized E. lucius, thanks to the large relative size of the eye (pupil) and the presence of a reflecting tapetum behind the retina. High absolute sensitivity will give a competitive edge also in terms of short reaction times and long visual range.     

Mercury accumulation in five species of freshwater fish in Lake Tyrifjorden,south-east Norway,with emphasis on their suitability as test organisms

Synopsis Mercury concentration in axial muscle of brown trout, Salmo trutta, whitefish, Coregonus lavaretus, Arctic charr, Salvelinus alpinus, smelt, Osmerus eperlanus and pike, Esox lucius, were studied in Lake Tyrifjorden during 1978–1982. Our data demonstrate that older and bigger fish on an average have higher mercury concentration than smaller and younger. Further, complex life histories as in brown trout influence the pattern of mercury accumulation. During young stages accumulation in brown trout is moderate, while accumulation in older stages is highly correlated to lake residency time. Based on our data we suggest the following requirements for a test organism and the collecting procedure; (1) life history should be simple with small sexual differences, (2) ageing should be easy and reliable, and (3) large representative samples should be easily obtained during (4) a fixed biological period i.e. the spawning period. We consider smelt as an appropriate test organism based on these criteria.     

Myoid cells in the peritubular tissue (lamina propria) of the reptilian testis

The arrangement and fine structure of peritubular myoid cells was studied in the testes of three species of reptiles (Lacerta dugesi, Testudo graeca and Natrix natrix) during two short periods of the seasonal cycle (European spring and autumn) and correlated with some ultrastructural properties of Leydig cells. The lamina propria consists of myoid cells, fibroblasts and non-cellular components comprising collageneous and non-striated microfibrils. Both components are arranged in alternating layers surrounding seminiferous tubules. In spring the lamina propria of lacertilian testis shows 1-5 layers of myoid cells which are rich in 50-70 A filaments and exhibit plasmalemmal and intracellular dense patches, smooth vesicles along the cell membrane and a concentration of organelles in a juxtanuclear position. Leydig cells are rich in smooth ER profiles and have few lipid droplets. In atumumn most myoid cells are replaced by fibroblast-like elements. Leydig cells display large numbers of lipid droplets and dense bodies, but only small amounts of agranular ER. Similar changes are noted in Leydig cells of Testudo and Natrix. However, in these species the boundary tissue of seminiferous tubules fails to show significant alterations comparing spring and autumn animals. In both species the lamina propria exhibits a few fibroblast-like cells interspersed among myoid cells.     

Environmental factors regulate the effects of roach Rutilus rutilus and pike Esox lucius on perch Perca fluviatilis populations in small boreal forest lakes

In this study of 18 small boreal forest lakes, the effects of abiotic and biotic factors (roach Rutilus rutilus and pike Esox lucius) on various population variables of perch Perca fluviatilis were examined. As a single variable, the gillnet catch per unit effort (CPUE) of R. rutilus was negatively related to the mean mass of small (< 200 mm) and the growth rate of young (1–2 years) P. fluviatilis. The mean mass of large (≥ 200 mm) P. fluviatilis was the highest at intermediate CPUE of R. rutilus. Redundancy analysis including environmental factors and P. fluviatilis population variables suggested that ‘predation–productivity–humus' gradient affected P. fluviatilis populations by decreasing the CPUE and mean mass of small individuals but increasing these variables of large individuals. The CPUE of R. rutilus and lake area had a negative effect on small and a positive effect on large P. fluviatilis growth rate. In small boreal forest lakes, P. fluviatilis populations are affected by the partially opposite forces of competition by R. rutilus and predation by E. lucius, and the intensity of these interactions is regulated by several environmental factors.     

Predicting the contributions of novel marine prey resources from angling and anadromy to the diet of a freshwater apex predator

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General morphology and axonal ultrastructure of the olfactory nerve of the pike,Esox lucius

Summary The olfactory nerve of the European pike (Esox lucius) contains 5.1 × 10⁶ axons with an average diameter of 0.20 ± 0,04 m and a length of 5.5 cm in 1 meter long pike. Each axon contains an average of 4 microtubules as well as neurofilaments, smooth endoplasmic reticulum and about 500 mitochondria per centimeter. The number of neurofilaments ranges from zero in 15% of the cross sections to over 10 in 6%. Neurofilaments generally occur in clusters located opposite to microtubule regions. Smooth ER can not be identified in 14% of the cross sections suggesting that this structure may not be continuous. Microtubules often display annular regions (halos) of low electron density ranging in size from 800 to 1300 Å. Halos from adjacent tubules usually merge into regional halos. The ratio of axoplasm to glial cytoplasm is 4.4:1, while the ratio of axonal plasma membrane to glial plasma membrane exceeds 7:1. A 4 cm nerve contains 1280 cm² of axolemma. This nerve represents an extreme in high density axonal packing and is therefore exceptionally well suited for biochemical, biophysical and physiological investigations.