A multivariate morphometric and meristic description of a population of freshwater-feeding river lampreys, Lampetra fluviatilis (L.), from Loch Lomond, Scotland

Adults of a freshwater-feeding population of Lampetra fluviatilis (L.) in Loch Lomond, Scotland, were trapped on their upstream (spawning) migration in the main inflow to the loch, the Endrick Water. These animals could be distinguished from the more typical anadromous upstream migrant L. fluviatilis , from the Endrick Water and the nearby catchment of the River Forth, principally by their smaller total length, greater disc, snout and eye size and much darker pigmentation. These, and other morphometric and meristic characteristics have been compared for populations of L. fluviatilis and Lampetra planeri (Bloch) from the Lomond and Forth catchments using univariate and multivariate statistics. The Endrick Water 'dwarf' L. fluviatilis was found to differ significantly from the other Lampetra studied, in a number of body proportions in addition to those traits mentioned above, and also in mean numbers of trunk myomeres and teeth. These differences are likely to be due to a combination of the effects of genetic isolation, and the short (freshwater) feeding phase of the 'dwarf' L. fluviatilis , which may, therefore, represent the intermediate stage between parasitic and non-parasitic forms in the L. fluviatilis/L. planeri species pair.     

A comparison of the metamorphosing and macrophthalmia stages of the lampreys Lampetra fluviatilis and L. planeri

Comparisons of metamorphosing and macrophthalmia stages of the closely related species, L. fluviatilis (L.) and L. Planeri (Bloch), have shown that these can be distinguished within a few weeks of the onset of metamorphosis by characteristic differences in colouration and body form. Measurements of several body intervals have disclosed differences between the macrophthalmia stages of the two species. A sharp distinction between the blunt teeth of L. planeri and the supposedly sharp teeth of L. fluviatilis has not been confirmed in these early stages, but significant differences have been found in the numbers of teeth in the anterior field of the oral disk and in the lateral and posterior marginal series. For material from several rivers, the range of length of metamorphosing and macrophthalmia stages of L. fluviatilis is83–119 mm (mean 99.3 mm). Weights varied from 0.71-2.5 g (mean 1.51 g). Regression coefficients for weight on length are much lower in the macrophthalmia of L. fluviatilis than in comparable stages of L. planeri. Total oocyte counts on macrophthalmia of L. fluviatilis gave values from8000–20,000 which are in general agreement with egg counts for adults of this species in the river Severn. Observations on the earliest metamorphosing forms have shown that it is not possible at this stage to distinguish the males of the two species by the structure of the testes. The development of the lumen in the adult foregut of L. fluviatilis has been shown to be variable and in some instances the gut does not become patent until early Spring. The possibility has also been raised that, in exceptional cases, a temporary lumen may also be present for a short period in L. planeri. Observations on the foregut and dentition, together with field data, suggest that the climax of downstream migration and the onset of parastic feeding takes place in late March or April.     

Larval growth in the river lamprey, Lampetra fluviatilis

A series of 987 ammocoetes from the rivers Towy, Teme, and Taw have been identified as mainly L. fluviatilis (L.) on the basis of oocyte counts on female ammocoetes. The length frequency distributions for this material differs from either L. planeri or P. marinus in showing only three modes in addition to the young of the year and the length distribution of the final mode coincides with the length range for 119 metamorphosing and macrophthalmia stages of L. fluviatilis that have been found at the same sites. These animals measured from 80–117 mm in length and weights varied from 0.76–2.28 g. Metamorphosis is believed to take place in late summer and early autumn when in the majority of cases, the ammocoetes are four and a half years old. The evidence that the non-parasitic L. planeri has a longer larval life than the closely related parasitic L. fluviatilis is thought to have some significance in relation to the evolution of the brook lamprey species.     

Metamorphosis in the paried species of lampreys, Lampetra fluviatilis (L.) and Lampetra Planeri (Bloch): I. A description of the timing and stages

A large number of larval, metamorphosing and adult nonarasitic lampreys, lampetra planeri, were collected from three different rivers and placed in a morphological series. The characteristic changes were then described and used to propose a sequence of Stages (1–9). The first signs of metamorphosis (Stages 1–2), which could occasionaly be found as early as late June, are characterized by the eruption and enlargement of the eyes. This is followed by rapid transformation of the the oral hood into an oral disc, and changes in the shape of the pharyngeal region (Stages 2–5). Pronounced alterations in body pigmentation, enlargement of the fins and the development of teeth occur during Stages 4 to 6. The vast modifications involved in Stages 2 to 6 take place relatively repidly in the period between approximately mid-July and mid-September. The subsequent changes which occur more slowly, eventually lead to the production of immature (Stage 7) and sexually mature adults (Stage 8). Mature males are characterized by the presence of a urinogenital papilla, while the females posses a post-cloacal fin-like fold and greatly distended trunk. Spawning took place between late March and late April with the spent animals (Stage 9) dying soon afterwards. The above sequence of Stages was then compared with those found in a smaller sample of the parasitic and ancestral species L. fluviatilis. The early metamorphosing stages in both species are apparently indistinguishable but clear differences atart to appear at Stage 5 when the body surface of L. fluviatilis is assuming a distinct silvery sheen. This trend becomes more marked in Stages 6 and 7, at wich time the river lamprey also has a more pronounced eye and disc and a slimmer trunk. Stage 7 in L. fluviatilis represents animals migrating to the sea in either the autumn or spring to commence their trophic phase. On the other hand this Stage in L. planeri may be regarded as representing a massive contraction of adult Stages and is in many ways similar to the early upstream migrants of parasitic species.     

Changes in haemopoietic sites during the metamorphosis of the lampreys Lampetra fluviatilis and Lampetra planeri

An investigation has been made in both the parasitic lamprey Lampetra fluviatilis and in its non-parasitic derivative Lampetra planeri of the rate at which the fat column replaces the typhlosole and nephric fold as the principal site of haemopoiesis. In the typhlosole, blood cell formation started to decline prior to the onset of external metamorphosis and had ceased within four weeks of the commencement of transformation. In the nephric fold haemopoiesis continued for several weeks in the region where the larval opisthonephros persisted but was never observed in the newly developing adult kidney. Soon after the onset of external metamorphosis the fat column started to become haemopoietic and later became the main site of blood cell formation. The rate at which the haemopoietic function was transferred from the nephric fold and typhlosole to the fat column was greater in L. fluviatilis than in L. planeri. Since a similar more rapid change in L. fluviatilis has also been found in the switch from larval to adult haemoglobin, the former type of haemoglobins may be produced only in erythrocytes originating in the nephric fold and typhlosole, whereas the latter type may be restricted to cells developed in the fat column. It is also suggested that the functional significance of the alteration in haemopoietic sites is related to changes at metamorphosis in the three regions where blood cell formation occurs.     

Population genetics of a cyclostome species pair, river lamprey (Lampetra fluviatilis L.) and brook lamprey (Lampetra planeri Bloch)

Horizontal agarose gel electrophoresis of 24 allozyme loci in four species of Central European lampreys (321 Lampetra planeri , 83 L. fluviatilis , 11 Eudontomyzon mariae and nine Petromyzon marinus ) was used to study the 'paired species' L. fluviatilis and L. planeri . The genetic differentiation of the anadromous river lamprey ( L. fluviatilis ) from the stationary brook lamprey ( L. planeri ) was within the range of ingroup differentiation of the latter, but L. fluviatilis exhibited much greater population cohesion over a more extended geographic range: G _ST = 0.0537 versus G _ST = 0.3398, N _em = 4.402 versus N _em = 0.4856, mean genetic among-stock distances D = 0.0047 versus D = 0.0257. L. planeri populations coexisting geographically with L. fluviatilis in the Rhine and Elbe river systems were genetically more cohesive than L. planeri stocks from the Danubian basin where L. fluviatilis is absent. Danubian L. planeri populations exhibit a lower degree of heterozygosity than brook lampreys from the Rhine river system, but comprise deeper genetic lineages ( G _ST = 0.4629 versus G _ST = 0.2434), despite being sampled from a much more restricted area. Isolation-by-distance is observed for L. planeri from the Danubian but not from the Atlantic drainage basins. Transspecific gene flow between L. planeri from Atlantic drainage basins and the long-distant migrating L. fluviatilis is inferred, raising doubt on the validity of two separate biospecies. E. mariae and P. marinus are clearly differentiated from Lampetra spp. at several allozyme loci.     

The relationship of gonadal development to the life cycles of the paired species of lamprey, Lampetra fluviatilis (L.) and Lampetru planeri (Bloch)

Gonadal developnient has been studied throughout the larval period of Lumpetru fluviatitis and comparisons have been made with conditions in the larvae of the closely relatcd non-parasitic species, L. planeri . The two forms differ in the time of onset or mitotic division in germ cells and in the period when oogenesis is initiated. These phases begin in L. pluneri when the ammocoetes are one year old and in L. fluviatilis at the end of the second year. The course of sex differentiation appears to be sinlilar in both forms. While in the early stages, the oocytes of L. planeri are larger than those of L. fluviatilis. at comparable ages, by the end of the third year they are sinlifar in size in both spccics. It is suggested that in L. planeri , during the extension of the larval period, gonad growth is retarded and during this phase the ammocoete accumulates body reserves which are used to meet the metabolic requirements of the rapidly developing gonads after metamorphosis. The differences observed in early gonadogenesis are believed to account for the reduced fecundity of the L. planeri ammococtc and their adaptive significance is discussed.     

Gill Morphometrics of the Lampreys Lampetra fluviatilis (L.) and Lampetra planeri (Bloch)

Morphometric measurements have been made on various gill components of different stages in the life cycle of the anadromous parasitic lamprey, Lampetra fluviatilis, and its nonparasitic derivative Lampetra planeri. The total gill area, expressed in terms of body weight, of both larval (1462–2717 mm² g^–1) and adult (1402–2337 mm² g^–1) L. fluviatilis are greater than those previously recorded in the rather meagre literature on lamprey gill measurements and are comparable with those found in the most active teleosts. The gills of the two Lampetra species are apparently identical in the larval stages and those of metamorphosing and adult L. planeri are similar to those of metamorphosing L. fluviatilis. Although the pharyngeal arrangement of lampreys differs greatly from that of teleosts, there are many features of the gills indicative of convergence between the two groups. Thus, in a given stage in the life cycle of lampreys, the secondary lamellae on either side of the filaments also alternate, become more widely spaced as the filament length increases and increase in area as the body weight becomes greater. Furthermore, the fractional cumulative increase in secondary lamellae area along a line following the presumed direction of water flow is also represented by a sigmoid curve. While at metamorphosis the pharynx becomes considerably modified to accommodate the change from a unidirectional to a tidal respiratory water flow, the total gill areas of the ammocoete are similar to those of metamorphosing stages which have attained adult characteristics. However, there are clearly differences in some of the components that influence and contribute towards the total gill area. Thus, in terms of body weight, the number and total length of the filaments and the total number of secondary lamellae, together with the number of secondary lamellae found on a given distance of filament, are greater in late metamorphosing stages, while the reverse is true for the average bilateral area of the secondary lamellae which is considerably greater in ammocoetes.     

Evolutionary history of lamprey paired species Lampetra fluviatilis (L.) and Lampetra planeri (Bloch) as inferred from mitochondrial DNA variation

A remarkable trend in the evolution of lampreys is the occurrence in most genera of 'paired species', in which the parasitic anadromous lampreys are believed to have given rise to nonparasitic freshwater resident populations. The present work examines the phylogeography of the European paired species Lampetra fluviatilis and Lampetra planeri, in an attempt to elucidate species pair evolutionary history. We studied sequence variation in cytochrome b and ATPase 6, 8 mitochondrial genes in 63 individuals from 21 localities of the paired species throughout their distribution range. Results from the phylogenetic and nested clade analyses were largely consistent, suggesting the existence of three major evolutionary lineages: lineage I and possibly lineage II are widespread throughout Europe, while the most ancestral lineage III is apparently restricted to the Iberian Peninsula. The high genetic diversity observed in the Iberian Peninsula is probably the result of refugial persistence and subsequent accumulation of variation over several ice ages, whereas the low levels of genetic diversity observed in central and northern Europe should reflect a rapid postglacial colonization. Results suggest that L. planeri originated within at least two distinct evolutionary lineages, rejecting the single origin hypothesis. The observed lack of taxa monophyly within lineage I may be the result of ongoing gene flow if the two taxa are alternate life-history forms of a single species. However, structure within lineage I is also consistent with the hypothesis of divergence of taxa after postglacial dispersion (around 2000 generations ago) with incomplete lineage sorting. Further testing of the alternative hypotheses is warranted.     

Brown trout Salmo trutta redd superimposition by spawning Lampetra species in a lowland stream

Reproductive interaction between sympatric lampreys and salmonids was studied. The superimposition of brown trout Salmo trutta redds by spring-spawning river lamprey Lampetra fluviatilis and brook lamprey Lampetra planeri was examined in a small lowland stream of western Lithuania. A high superimposition rate of S. trutta redds by both L. fluviatilis (up to 83%) and L. planeri (up to 48%) was found, when the spawning intensity of Lampetra spp. was high. The occurrence of this phenomenon is the result of the overlap in the spawning habitat preferences at the reach-scale and at the microhabitat scale for the three species. One of the main requirements for Lampetra spp. spawning site selection was the negative streambed slope, an essential trait of the pool-riffle transitional zone. The structure of the salmonid redd created a considerable negative microhabitat slope suitable for Lampetra spp. spawning, which put the redds under a higher susceptibility to be superimposed. The timing of Lampetra spp. spawning overlapped closely with the emergence of S. trutta fry, suggesting a probable ecological effect of superimposition on S. trutta in the pre-emergent and emerging stages.     

The systematics of British larval lampreys

Several taxonomic characters, including the number of trunk myomeres, proportional body measurements and patterns of external and internal pigmentation, have been investigated in populations of ammocoetes belonging to the three species of lampreys found in British rivers. Petromyzon marinus can be readily distinguished by the pigmentary pattern in the tail and on the oral hood, and by the much higher number of trunk myomeres. Although no character can be used to separate with certainty the larvae of Lampetra fluviatilis and Lampetra planeri , significant differences were found between the mean number of trunk myomeres in the two species. Moreover, the values for ammocoetes were virtually identical to those of the respective post-larval stages, at which phase in the life cycle the two Lampetra species are clearly distinguishable. The incidence of pigmentation on the tongue precursor was much higher in larval populations of L. fluviatilis than in those of L. planeri and there was also a difference in the rate of change in the relative length of the trunk and tail. Where comparisons can be made, the results in this paper are in agreement with those of most other European and North American workers. The data differ markedly, however, from that contained in the only other previous detailed systematic study on British larval lampreys, which was subsequently used as the basis for taxonomic keys.     

Morphological development and allometric growth patterns in hatchery-reared California halibut larvae

Morphological development, allometric growth and behaviour of hatchery-reared California halibut Paralichthys californicus were studied from hatching to metamorphosis (42 days post hatch, dph) at 187° C. Mean standard length ( L _S) of larvae and juveniles increased from 2.1 mm at hatching to 10.5 mm at metamorphosis with the increase in length being approximately linear. Stages of morphological development were described using the alphabetic staging (A–I) used for other flatfish species. Organogenesis and differentiation were more rapid and complex in yolk-sac (hatching, stage A–3 dph, stage B), preflexion (3–19 dph, stages B–C), and flexion larvae (from 20 to 23 dph, stages D–E), as larvae developed most of their sensory, feeding, respiratory and swimming systems. After notochord flexion at 24–25 dph (stage F), most morphological changes were related to the progressive transformation from a bilateral symmetrical larva to an asymmetrical benthic juvenile (42 dph, stages G–I).     

Allozyme Polymorphisms and Biochemical-Genetic Taxon Markers in Lampreys (Lampetra, Eudontomyzon, Petromyzon)

Variation at 23 putative enzyme-coding loci was scored in 424 lampreys, including 321 European brook lampreys (Lampetra planeri), 83 European river lampreys (L. fluviatilis), 11 Ukrainian brook lampreys (Eudontomyzon mariae), and nine sea lampreys (Petromyzon marinus). Twelve polymorphisms are described for Lampetra species (LDH*, SOD-2*, PNP*, AAT-1*, AK-1*, ES-2*, LGL*, MPI*, GPI-1*, GPI-2*, PGM*, IDHP-2*), and two each for E. mariae (GPI-1*, ME-2*) and P. marinus (MDH-1*, ME-2*). Diagnostic allozymes are presented for the discrimination of lamprey taxa, some of which are difficult to recognize from the morphology of ammocoetes larvae, the life stage usually encountered when collecting cyclostomes. The allelic markers described permit the clear allocation to a genus, except for the species L. fluviatilis and L. planeri, which are not differentiated by qualitative allozyme analysis.     

Quantitative studies on the skin of the paired species of lampreys,Lampetra fluviatilis (L.) and Lampetra planeri (BLOCH)

The number of mucous, club, and granular cells in the epidermis, and the number of rows of subcutaneous adipose cells, as well as the thickness of the epidermis and the dermal collagen layer, have been recorded for the larval and metamorphosing stages of the anadromous parasitic lamprey, Lampetra fluviatilis, and for the larval, metamorphosing, and adult stages of the nonparasitic lamprey, Lampetra planeri. In L. fluviatilis, the mucous cells predominated in all stages but were more abundant in fully metamorphosed individuals than in larvae. During metamorphosis, the number of granular cells increased continuously, whereas the club cells showed little change. Although lampreys do not feed during metamorphosis, there was an increase in the thickness of the epidermis and in the dermal collagen sheath; the latter increase probably foreshadows the increase in activity by the adults. Simultaneously, there is a reduction in the subcutaneous fat layer, which can be attributed to mobilization of lipid as an energy source. Changes similar to those just described for L. fluviatilis were also found in metamorphosing L. planeri. However, the pattern altered markedly during adult stages in this nonparasitic species. There were marked declines in the number of cells, in the thickness of the epidermis, in the width of the collagen sheath, and in the quantity of subcutaneous fat.     

Heart Ratios at Different Stages in the Life Cycle of Lampreys

Heart ratios (heart weight/body weight. ×100) have been obtained for freshly killed and preserved (10% formalin) specimens of the lampreys Petromyzon marinus, Lampetra fluviatilis and L. planeri. Values for comparable stages were significantly higher in the preserved material, probably as a result of retention and fixation of blood in the heart chambers. The regression slope for the logarithmic relationship between heart and body weights was close to one in all stages of the three species investigated. A marked increase was observed in the heart ratio during metamorphosis, apparently attributable to an increase in the number and density of myocardial fibres. Heart ratios in the lamprey were generally higher than for most other fishes, with values of 0.1 and 0.3 being obtained for example in the case of freshly killed ammocoete and sexually mature adult stages of L. fluviatilis.     

The effects of temperature and meal size on the rate of gastric evacuation in perch (Perca fluviatilis) fed on fish larvae

SUMMARY. The rate of gastric evacuation in perch (Perca fluviatilis) (89–170 mm length) fed on fish larvae was studied at temperatures between 12.0 and 21.7°C. Gastric evacuation rates were usually described by an exponential function. The instantaneous rate of gastric evacuation ( R ) was constant for a large number of different meal sizes. At higher food rations, a lag phase in digestion was found during the first part of digestion, and this ration size was smaller for smaller perch (89–110 mm) than for bigger perch (120–170 mm). Below these larger meal sizes, gastric evacuation was similar for the different size classes studied. The relation between R and temperature was described by an exponential function. The effects of meal size, number of food items, fish size and temperature on the rate of gastric evacuation are discussed.     

Early events in adult eye development of the moth, Manduca sexta

The eye imaginal disc of Manduca sexta is created early in the final larval instar from the adult eye primordium, which is composed of fully differentiated cells of the larval head capsule epidermis. Concomitant with the down-regulation of the larval epidermal program, expression of broad, a marker of pupal commitment, is activated in the primordium. The cells then detach from the cuticle, fold inward, and begin to proliferate at high levels to produce the inverted, eye imaginal disc. These and other events that begin on the first day of the final larval instar appear to mark the initiation of metamorphosis. Little is known about the endocrine control of the initiation of metamorphosis in any insect. The hemolymph titer of juvenile hormone (JH) declines to low levels during this period and the presence of JH is sufficient to repress development in cultured eye primordia. However, maintenance of JH at high levels in vivo by treatment with long-lasting JH mimics has no apparent effect on early steps in eye imaginal disc development. We discuss our findings in the context of the endocrine control of metamorphosis. The initiation of metamorphosis in Manduca, and perhaps a wide range of insect species, appears to involve the overcoming of JH repression by an unidentified, nutrient-dependent, hormonal factor.     

Thyroglobulin biosynthesis in a larval (ammocoete) and adult freshwater lamprey (Lampetra planeri Bl.).

1. The biosynthesis of 18-19S thyroglobulin has been studied in a larval and adult freshwater lamprey (Lampetra planeri Bl.). 2. In vivo and in vitro experiments have been performed by injecting into the coelomic cavity or by incubating branchial region labeled constituents of Tg of higher vertebrates (125I, [3H]leucine and various [3H]carbohydrates). 3. Larvae (ammocoetes) and adults incorporate all labels into thyroglobulin (18-19S Tg), containing a small proportion of labeled T3 and T4, as identified by paper chromatography, and very minute amounts of stable iodine. 4. In adults, the biosynthesis of 18-19S Tg proceeds much more rapidly and the labels are incorporated in higher percentage than in larvae. 5. The demonstration of the biosynthesis of the specific thyroid protein, 18-19S Tg, in larvae indicates that the biochemical mechanism of hormonogenesis is present in larval endostyle before the morphological differentiation of thyroid cells and follicles occurring during metamorphosis. 6. Some 18-19S Tg is apparently stored in the endostyle.     

Description and ontogeny of young Stolephorus baganensis and Thryssa kammalensis, two Engraulididae from Peninsular Malaysia

The morphology of the digestive system was useful to distinguish the larvae of Stolephorus baganensis and Thryssa kammalensis before the full development of their dorsal and anal fins. The relative positions of these fins, the length of the anal fin, and body depth, were good criteria for identifying individuals >10·0 mm L _S. For both species, the relative growth of the ten morphometric characters studied was best explained by linear piecewise regressions indicating inflection in allometry at specific standard lengths. Most of these sudden changes in growth rate occurred between 6·9 and 10·0 mm L S for S. baganensis and between 5·8 and 8·9 mm L S for T. kammalensis . Double-centred principal component analysis (PCA) confirmed important changes in the external morphology of both species during this transition period. Prior to this period, the main parameters characterizing the global morphological changes of both species were the length and position of dorsal and anal fins whereas they were body depth and eye diameter (only in S. baganensis ) for larger specimens. Complete development of scales did not appear as a suitable criterion to define the end of the larval period, which, instead, was set at the size at which larvae presented an adult-like pigmentation (respectively 35·0 mm L S and 55·0 mm L S in S. baganensis and T. kammalensis ).