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.     

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.     

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.     

Metamorphosis in the paired species of lampreys, Lampetra fluviatilis (L.) and Lampetra planeri (Bloch): 2. Quantitative data for body proportions, weights, lengths and sex ratios

Representatives of the various Stages (1–9) in the metamorphosis and short adult life of the brook lamprey, Lampetra planeri , were used to provide quantitative data to describe the pattern of changes that take place during this period of the life cycle. During the transformation of the oral hood into an oral disc, this ventral region of the snout first declines in length before increasing markedly. The branchial region declines in length and remains relatively smaller than in the ammocoete, a feature probably correlated with the concomitant internal changes in the pharynx which permit a change from a unidirectional to a tidal respiratory flow. The eye increases in size only through the initial Stages (1–5). The main period of fin enlargement occurs rather later in metamorphosis than the above changes.
During maturation the two initially separate dorsal fins increase further in height and eventually become separated only by a notch. Differences between the two sexes are found in the relative size of the disc and fins, the larger structures of the male probably being related to their greater activity in spawning behaviour. Measurements on metamorphosed L. fluviatilis confirm that in this species the eye and disc are relatively larger than in L. planeri. Data are presented which illustrate that in collections taken during the metamorphosis of both species the males are smaller and slightly more numerous than the females and that transformation is initiated at a longer length in L. planeri than in L. fluviatilis .     

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.     

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.     

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.     

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.     

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.     

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 structure of Mordacia mordax insulin supports the monophyly of the Petromyzontiformes and an ancient divergence of Mordaciidae and Geotriidae

The phylogenetic relationships between the two southern hemisphere lamprey families (Geotriidae and Mordaciidae) and their northern hemisphere counterparts (Petromyzontidae) are unresolved. Insulin was isolated from an extract of islet-containing intestinal tissue from ammocoetes of the Australian lamprey, Mordacia mordax. Its primary structure was established as A-chain: GIVEQCCHRK10CSIYDMENYC20N and B-chain: SALMGTGGTH10LCGSHLVEAL20YVVCGQRGFF30 YTP[SKG]. Although the residues in parentheses are only tentatively assigned, mass spectrometry supports the proposed sequence and demonstrates that Mordacia proinsulin, unlike proinsulin from Geotria australis, is fully processed to mature insulin. Insulins from M. mordax and G. australis and from the northern hemisphere lampreys Petromyzon marinus and Lampetra fluviatilis share a pentapeptide extension to N-terminus of the B-chain (Ser-Ala-Leu-Xaa-Gly) that has never been found in the insulins of any other vertebrate class. This observation provides support for the claim that the Petromyzontiformes constitute a monophyletic group. M. mordax insulin differs from that of G. australis by 18 amino acid residues but by only four residues from the common sequence of P. marinus and L. fluviatilis insulin. These data are consistent with the view that Geotriidae and Mordaciidae have been separated for a long period and suggest that G. australis insulin has undergone an accelerated rate of molecular evolution.     

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.     

Stunted growth of pikeperch Sander lucioperca in Lake Sahajärvi, Finland

Growth of pikeperch Sander lucioperca in the eutrophic and clay-turbid Lake Sahajärvi, Southern Finland, was extremely slow in comparison with other lakes at similar latitudes. The most important food item in July was phantom midge larvae Chaoborus flavicans for all sizes of S. lucioperca (239–423 mm total length L _T), while later, in August and September, the diet of S. lucioperca (149–407 mm L _T) consisted of small (30–100 mm L _T) perch Perca fluviatilis , ruffe Gymnocephalus cernuus and roach Rutilus rutilus .     

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.     

Heated competition: how climate change will affect non-native pumpkinseed Lepomis gibbosus and native perch Perca fluviatilis interactions in the U.K

Heated and ambient temperature experimental ponds were used to examine competition between introduced pumpkinseed Lepomis gibbosus and native perch Perca fluviatilis in England, U.K., and how these interactions are likely to change under climate warming conditions. Results from three sets of two-week experiments indicated that in both species and in all sets, growth was faster in heated than in ambient temperature ponds. Growth of both P. fluviatilis and L. gibbosus in sympatry did not differ significantly from that observed in allopatric ponds. Diet analysis indicated that increased resource partitioning occurred when P. fluviatilis and L. gibbosus were reared in sympatry, with P. fluviatilis shifting to a diet higher in microcrustaceans. The results do not support the previous claims of adverse effects of L. gibbosus on P. fluviatilis populations. Under conditions of climate change, however, which have been demonstrated experimentally to enhance L. gibbosus recruitment, this species is expected to become invasive in England, resulting in higher densities that may exert a stronger competitive effect than examined in this study.     

Information on the growth of the ammocoete larva of the anadromous Sea lamprey, Petromyzon marinus in British rivers

An examination has been made of the length frequency distribution of ammocoetes of the Sea lamprey, Petromyzon marinus L. collected during April, July, August and October. A comparison of the frequency distributions for the individual collections and a study of gonadal development within certain length ranges suggests that the duration of the larval period cannot be less than five years.     

Gut length plasticity in perch: into the bowels of resource polymorphisms

Resource polymorphisms, intraspecific variation in morphology due to differential resource use, are common across a wide range of animal taxa. The focus in studies of such polymorphisms has been on external morphology, but the differential use of food resources could also influence other phenotypic traits such as the digestive performance. In the present study, we experimentally demonstrate that Eurasian perch ( Perca fluviatilis L.) display adaptive plasticity in gut length when exposed to different food types. Perch fed a less digestible food type developed relatively longer guts compared to fish fed a more easily digested food type. This divergence in gut length was also apparent under natural conditions because perch inhabiting the littoral and pelagic habitats of a lake differed in resource use and relative gut length. Despite that the digestive system in perch is plastic, we found that individuals switching to a novel food type might experience an initial fitness cost of the diet switch in the form of a temporary reduction in body condition. These results show the importance of gut length plasticity for an ontogenetic omnivore but also a cost that might prevent diet switching in polymorphic populations.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 517–523.     

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.     

Changes in the proximate body composition of the landlocked sea lamprey Petromyzon marinus (L.) during larval life and metamorphosis

Estimates were made of the growth rates and proximate body composition of larval and metamorphosing P. marinus (L.) collected at various times of the year from Shelter Valley Creek, Lake Ontario. Analysis of length-frequency data indicates that the average duration of larval life was 6 years, with metamorphosis occurring predominantly in the length range above 13 cm. Increases in length were almost entirely restricted to the warmest months and did not take place during the final year of larval life. Three categories were thus recognized for the proximate analysis: ammocoetes <13 cm, ammocoetes > 13 cm and metamorphosing individuals. In ammocoetes <13 cm, seasonal differences were observed in the regression coefficients in the logarithmic relationships between wet weight and length and between each of water, lipid and ash and the wet weight. No such difference was found for the regressions between protein and wet weight. For a fixed length (9 cm), the wet weight varied only slightly during the year, although a small peak was seen in May. When considered on the basis of fixed weight (1 g), the relative amount of lipid deposited was greatest in May/July, coincident with a high diatom density. The water content followed an inverse pattern to that of lipid, while the protein and ash contents showed little seasonal variation and exhibited values lower than those normally found in teleosts. Throughout the last year of larval life, the animal stored a greater proportion of lipid, presumably to facilitate the energy demands of metamorphosis during which this food store underwent a marked reduction.     

Maximum daily ration of juvenile fish fed on living natural zooplankton

Juveniles of five species of cyprinids of body length 15–90 mm as well as juvenile perch, Perca fluviatilis L., were fed on living natural zooplankton over periods of 2 or 3 days. For all species the correlation of the daily ration (% body weight) with body weight showed a maximum curve. The maximum was reached at a body weight (wet weight) of 0.6 g for Leuciscus leuciscus (L.) and 0.1 g for a group consisting of varying numbers of Rutilus rutilus (L.), Abramis brama (L.) and Alburnus alburnus (L.). For L. leuciscus , the maximum was 220% body weight (wet weight), corresponding to 40% on a dry weight basis. For the mixed species group the maximum was about 500% (wet weight) and about 140% on a dry weight basis. The highest daily ration coincided with the occurrence of the spring bloom of zooplankton.