%oulogcalJournalojtheLinnean Society, 65: 127-143. With 4 ligures
bc")I.Udl.\.
1Y79
Metamorphosis in the paired species of lampreys,
LampetraJuaiatilis (L.) and Larnpetra planeri ( Bloch)
1. A description of the timing and stages
D. J. BIRD"
AND
I. C. POTTER, F.L.S."
School o f Biological Sciences, University $Bath, Claverton Down, Bath B A 2 7AY, Auon
Arcepted for publicationJune I977
A large number of lawal, metamorphosing and adult nonparasitic 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 Krst signs of
nietainorphosi, (Stages 1-2). which could occasionally be found as early as late June, are
characterized by the eruption and enlargement of the eyes. This is followed by the rapid transformation of the the oral hood into an oral disc, and changes in the shape of the pharyngeal region (Stages
5-5). Pronounced alterations in body pigmentation, enlargement of the fins and the development of
tccth occur during Stages 4 to 6. The vast modifications involved in Stages 2 to 6 take place
relatively rapidly 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 possess a post-cloaca1 fin-like fold and greatly distended
trunk. Spawning t o o k place between late March and late April with the spent animals (Stage 9) dying
won attcrwards.
The above sequence of Stages was then compared with those found in a smaller sample of' the
parasitic and ancestral species L. j u u i a t i h . The early metamorphosing stages in both species are
apparently indistinguishable but clear differences start to appear at Stage 5 when the body surface of
L.Juuiatdis is assuming a distinct silvery sheen. This trend becomes more marked in Stages 6 and 7,
at which time the river lamprey also has a more pronounced eye and disc and a slimmer trunk. Stage
7 in L. /fnuiatihr 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.
KEY WORDS: - parasitic and nonparasitic lampreys - stages in metamorphosis
characters - sexual maturity -evolution in lampreys - morphological abnormalities.
-
key
-'Present address: School of Environmental & Life Sciences, Murdoch University, Murdoch, Western Australia
6153.
127
0044-4082/79/020127-17/$02.00/0
6
0 I979 The Linnean Society of London
D . J . MIRD AND I . C. POTTER
I28
CONTENTS
Iiiti-oductioti
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M.itci-i.tl\ a i i d inrth~rda . . . . . . . . . . . . . . . . . . . .
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Descr.iption ol larval, inetainorphosing and adult Larnp~traplanert
Lai-gcaininocoete
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Stage 7 (iininature adult)
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piarm
Coiiiparisc)n 01 the 5tagcs in irretarnoi-ptlosls o f Larnp~/rapur/in/ilisand Larr~pdrc~
Titiiiiig ol’inetaiiiorphosis in Lanipelraplaneri and LampetraJuviafilis
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Morphological almormalities
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Discussion
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ALki~owledgeinent . . . . . . . . . . . . . . . . . . . . .
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IS:!
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142
INTRODUCTION
~ l lampreys
l
undergo a protracted and relatively sedentary larval phase during
which they live in the silt deposits of streams and rivers from which they filter
their food (Hardisty & Potter, 197 la). At this stage they are blind, toothless and
have poorly developed fins. After a radical metamorphosis, the parasitic species
migrate downstream to either marine or large freshwater environments where
they feed on teleost fishes (Hardisty 8c Potter, 1971b). Many of the changes
undergone in the transition from larva to adult are thus related to the alteration
in feeding habit. For example, the oral hood of the ammocoete becomes
converted into a tooth-bearing disc which can be utilised for attachment to host
fishes. The actual rasping away of host tissues is carried out, however, by the
newly-developed tongue-like piston on which are borne two longitudinal and
one transverse lingual laminae. During metamorphosis, the eyes also erupt above
the body surface and the fins become much enlarged, features presumably
associated with the development of a more active and predatory mode of life. After
the completion of the parasitic 1hase, the lamprey embarks on an upstream
migration to its spawning grounds in the shallow faster flowing regions of the river
(Hardisty&Potter,197 lb).
In contrast to the lampreys with a parasitic phase in their life cycle are the
nonparasitic o r brook lampreys which do not feed as adults and reach maturity
some six to ten months after the initiation of metamorphosis (Weissenberg, 1925,
1926, 1927; Zanandrea, 1959 a,b,c, 1961; Hardisty 8c Potter, 197 lc). O n the basis
of the marked similarity in the morphology of certain species with divergent life
cycles, Hubbs ( 1925) suggested that each nonparasitic lamprey had evolved from
one in which there was a parasitic phase. That these so-called “paired species”
(Zanandrea, 1959a) are widespread in the lamprey fauna is borne out by their
discovery in the genera Zchthyomyzon, Eudontomyton, Tetrapleurodon, Lampetra and
Mordacia (Hubbs 8c Potter, 197 1).
LAMPREY METAMORPHOSIS. 1
I2Y
The only paired species found in British rivers is that comprising the
anadromous parasitic river lamprey, LampetraJuviatilis (L.1, and its nonparasitic
derivative, Lampetra planeri (Bloch). Although features, such as the incidence of
pigmentation on the tongue precursor and the number of trunk myomeres,
differ significantly between larval populations of these two species, there is
always a considerable degree of overlap in these and other morphological
characters (Potter & Osborne, 1975). A significant difference between the
ammocoetes of the two species is also found in the number of oocytes they
possess, but here again the range in values overlaps (Hardisty, 197 1 ) .
The difticulties in obtaining pure samples of the larvae of either of the
representatives of paired species is compounded by the fact that they often occur
together in the same silt beds. Extensive sampling in many rivers has shown,
however, that L. planeri occurs alone in several small rivers and streams. This
feature is apparently correlated with differences between the migratory and
spawning requirements of the two species, L.Juviatilis tending to enter rivers that
are relatively wide and deep. Although L. planeri almost invariably occurs in those
regions where L. Juuiatilis is also found, there are a few exceptions to this
generalization. One such sampling site is located at Bransford Bridge on the
River Teme near a region where breeding populations of L. Juviatilis have often
been observed (Hardisty & Huggins, 1970; P. N . Claridge, pers. comm.).
The problem in distinguishing with certainty between the ammocoetes of L.
Juviatilis and L. planeri using morphological criteria is perpetuated in the period
immediately after the commencement of transformation. After metamorphosis
has been under way for several weeks, however, the marked silver coloration and
relatively larger eye developed by L. Juviatilis facilitate the separation of this
species from L. planeri (Hardisty, Potter & Sturge, 1970).
Attempts to provide a description of a series of stages in the metamorphosis of
lampreys have been restricted to investigations of the nonparasitic lampreys,
Eudontomyzon mariae and Lampetra planeri, by Balabai ( 1948) and Dines ( 1973)
respectively, and to the landlocked parasitic sea lamprey, Petromyzon marinus, by
Manion & Stauffer (1970). Since the completion of the study of L. planeri, the
collection and examination of a very much larger number of brook lampreys has
demonstrated that Dines’ stages were not comprehensive. This study provides
both a qualitative description of the sequence of stages that occur during the
metamorphosis and short adult life of L. planeri, together with a record of when
they were found in the rivers. Comparisons are then made with the
metamorphosing stages of the ancestral species, L.Juviatilis, for which rather less
material was available for certain stages.
MATERIALS AND METHODS
Ammocoetes and metamorphosing stages of L. Juuiatilis and L. planeri were
collected with an electric fish shocker. The representatives of L. Juviatilis were
caught in the Rivers Towy (Powys),Teme (Worcestershire)and Tawe (Devon)and
those of L. planeri in the Rivers Honddu (Powys) and Wylye (Somerset) and in
Highland Water (Hampshire). The downstream migrants of L. Juviatilis were
collected from the intake screens of the Oldbury Power Station (Avon) in the
Severn Estuary while spawning L. planeri were taken with scoop nets from their
redds in Highland Water.
Figurc I . T he anterior region of Lampetra plaiirri in large ammocoetes ( A , Bi a nd metamorphosing Stage\ 1 (C, Dl, 2 ( E , Fi, 3 ( G , HI a i d 4 ( I , J). In this
and Fig. 2, each ofthe I,ctei-.tl vie\\.\ 'ire d l i v i n g aniiiials while the ventral views are of specimens pw w r\e d in 10'h loriiialiii,
Figui.v 2. TJic diiicrior region ol'larnpt-frupluntnin Stages5 (A. B), 6 (C, D).7 I t ,
iiiature leitiale and Stage 9 a spent kinale.
F), I
IC;. 14) aiitl 9
( I . J). Stage 7 is an irn~nriurc~
adult. Stay;? 8 a
I
3
1.3:'
D . J . B I R D A N D I. C. POTTER
After transportation back to the laboratory, the animals were anaesthetized in
MS 222 (Sandoz) prior to morphological examination and photography. After
removal of surface water, a representative sample was measured and weighed to
the nearest 0.1 min and 10 mg respectively. The lampreys were preserved in 10%
f'ormalin and then stored in separate 200 mm tubes so as to retain the animal's
longitudinal shape.
Although the separation of metamorphosing animals into various Stages was
based on formalin-preserved material, it was assisted by observations of living
animals in the case of those characters, such as pigmentation, which were more
clearly detectable before preservation. During the course of several years
sampling a total of 504 L. planeri and 225 L._fEuviatilis were caught in various
stages of metamorphosis and used for the production of the staging criteria.
Each animal was sexed by examining the gonad, microscopically where
necessary, through a small incision made in the anterior region of the trunk. The
state of the teeth was ascertained by examination of preserved and living
specimens with a dissecting microscope and from photographs of the disc of the
more advanced animals once they had reached a stage when they could attach to
the inside wall of glass aquaria.
RESULTS
Description $larval, metamorphosing and adult Lampetra planeri
Large ammocoete
At the anterior end of the body is the oral hood through which the nutritive
and respiratory water current is channelled into the pharynx. The hood consists
of a semicircular dome whose free lateral edges are not continuous with the
transverse lip of tissue which marks the posterior boundary of the hood (Fig. 1
A,B). The prominent projection of the transverse lip produces a depression
immediately behind the hood (Fig. 1A), a characteristic which disappears during
the first two stages of metamor hosis (Fig. lC, El. The branched network of cirrhi
at the hind end of the inside o the hood are arranged in such a manner that they
prevent the entry of large particles into the pharynx. A slight crescent-shaped
bulge of tissue can be seen in front of the first gill aperture. The seven gill
apertures are large and surrounded by an abundant blood supply which gives
this region a very dark red coloration. In living animals, blood vessels are also
conspicuous in other regions of the branchial chamber, particularly in the
myotomal septa. The mottled and rather dark appearance of the dorsal surface
of the body, related to the presence of numerous melanophores, contrasts
with the light brown coloration of the ventral region. The two dorsal fins are very
small and rise only just above the body surface (Fig. 3A).
Key characters. Eyes below surface. Prominent depression immediately posterior
to transverse lip of oral hood.
P
Stage I
The first signs of external transformation are those associated with the initial
stages in the eruption and development of the eyes and the modification of the
oral hood into a disc (Fig. 1C, D). Thus, the eyes, which were previously only just
visible below the surface, each now form a small dark elliptical to oval patch in a
LAMPREY METAMORPHOSIS. 1
133
furrow which has itself become less prominent than in large ammocoetes. The
oral hood has become “stubbier” and the lateral edges have started to fuse with
the transverse lip which has become reduced in width. The depression, behind
the transverse lip, has become less conspicuous than in the ammocoete.
Key character. Eyes visible as small dark elliptical to oval patches.
Stage 2
The eye has erupted further and is now clearly visible as a prominent dark oval
patch (Fig. 1E). The surface of the snout at the base of the eye is beginning to
fbrrn a fold. Reduction of the transverse lip of the oral hood has progressed to
the extent where it no longer forms a depression posteriorly. The branchial
region has increased in prominence and the snout has become narrower,
resulting in the crescent-shaped bulge of tissue in front of the first gill aperture
becoming prominent. The lips of the oral hood have thickened (Fig. 1F)and the
oral cirrhi have become reduced in size.
Key character. Eyes conspicuous as dark oval patches.
Stage 3
The eyes now appear more circular and, in live animals, the iris for the first
time is visible as an anterior and a posterior light-grey crescent (Fig. lG). That
the iris and part of the pupil are obscured ventrally is due to further development
of the small wedge of tissue that lies below the eyes. The prebranchial region has
become more triangular, particularly when viewed from the ventral surface (Fig.
lH), and the crescent-shaped bulge in front of the first gill aperture is less
conspicuous. Although the lips of the oral hood have become thicker, thus
reducing the size of the oral aperture, the lateral edges of the hood have not yet
become fully fused with its transverse lip. The transverse lip has undergone,
however, a very marked thickening and reduction in width. Within the
presumptive oral disc of the adult can now clearly be observed for the first time
the early stages in the development of the tongue-like piston. The oral cirrhi,
whose previously transverse orientation resulted in their being hidden in direct
ventral view, have now become visible through the differential forward growth of
the dorsal region of the snout. These cirrhi are clearly very reduced in size
compared with the condition found in the ammocoete. During this stage the
branchial region attains its maximum relative depth.
Key characters. Iris present as anterior and posterior light-grey crescents.
Prominent bulge immediately ventral to eye. Tongue-like piston evident.
Stage 4
The eye is now larger and the iris, although still greyish, forms a continuous
region around the pupil which in live animals exhibits the three equidistantly
arranged blood vessels characteristic of this and later stages (Fig. 11). The lateral
edges and transverse lip of the oral hood have become completely fused to form
a thickened and small oval oral disc (Fig. 1J). The oral cirrhi have become further
reduced to just a few short tufts. The dorsal surface of the snout has grown
further forwards and the tongue-like piston can be very clearly observed. The
prebranchial region has become much more slender, a feature which, with the
increased development of the eyes, means that the latter can for the first time be
observed when the animal is viewed from the ventral surface (Fig. 1J).
Key character. Tissue continuous around a very small oral disc.
134
L). J.
BIRD AND I . C . P O T T E R
Stage 5
In living animals, the iris has become a bright silver and the three V-shaped
blood vessels are now conspicuous (Fig. 2A). Although the oral disc is still small,
it has begun to differentiate and increase in size, producing a small triangular
depression behind its posterior edge (Fig. 2B). The oral cirrhi are no longer
present. For the first time, the presumptive lateral circumoral teeth and the
supra- and infra-oral teeth laminae can be readily discerned. The branchial
region is slimmer and the gill apertures are reduced in size and slightly more oval
in shape, their outline becoming better defined through the presence of
increased pigmentation which is starting to obscure any underlying blood
vessels. A similar marked change in pigmentation is also found in other regions
of’ the body leading to a slight silvering of the ventral surface. The myotomal
septa have become more conspicuous.
Key characters. A large silver iris characteristic of the later stages is combined with
an alnmocoete-like appearance to the gill region. Presumptive tooth structures
evident around oral apertures.
Stage 6 (macrophthalmia)
This Stage, which corresponds to the macrophthalmia of Hardisty & Potter
(197 1 b), superficially resembles an immature adult. The most noticeable feature
is the further change that has taken place in the pigmentation, resulting in the
animals developing a more pronounced silvery body surface (Fig. 2C). These
changes have also led to the underlying blood vessels of the branchial region
becoming totally obscured so that the gill apertures now appear as clearly
defined oval structures. There has been considerable growth of the snout
forwards and an enlargement and differentiation of the disc (Fig. 2D). It is at this
Stage that the oral fimbriae can first be readily observed, these being formed
initially at the posterior end of the disc behind which a well defined indentation
has now developed. The teeth are now clearly differentiated and recognizable as
white or yellow structures, depending on whether they are in live or in
formalin-preserved specimens respectively. The pits of the lateral line system are
conspicuous just behind the disc and ventral to the eye (Fig. 2C) and the region
around the aperture leading to the naso-hypophyseal apparatus has become
transformed into a tube. In the trunk region, the myotomal septa are well
defined and the fins have now clearly increased in height (Fig. 3B).
This Stage, which is generally reached in September or October (Table l ) , can
be regarded as representing the end of a very rapid series of modifications
from the ammocoete condition. During the following winter months the rate of
change in external structures is much slower.
Key character. Disc enlarged and becoming differentiated with clearly defined but
small fimbriae around the perimeter.
Stage 7 (immature adult)
Compared with the macrophthalmia, the disc has increased in size, is much
more oval than round and now bears prominent fimbriae along its edges (Fig.
2F). In ventral view, the indentation immediately behind the disc has become a
well-marked semicircular depression. The dorsal surface of the body has lost
some of its silvery sheen, becoming duller and more brownish, especially in the
tail region. In live specimens particularly, the pits of the lateral line system on the
D. J . BIRD AND I. C. POTTER
136
Table 1. The number of representatives of each of the stages caught monthly
during the post-larval life ofL. planeri in 197 1/72 and 1975176
197 111972
Stage
I
2
3
4
5
6
197511976
7
8
9
July
2
August
4
October
2
3
12
6
4
5
6
11
3
6
5
9
3
6
4
2
6
7
8
54
Decembrr
6
6
January
Febi-uaiy
April
8
9
80
November
Mad1
7
10
Jurie
Septciiiber
1
3
4
1 4
5
9
34
4
8
4
12
14
dorsal and lateral surfaces of the snout have become prominent (Fig. 2E).
Although the two dorsal fins are still separate, the gap between them has closed
appreciably and for the first time their trailing edges have developed a fine
fringe.
Key character. Two enlarged but separated dorsal fins with fringed edges.
Stage 8 (mature adult)
The sexually mature adult can be distinguished from the previous Stages both
by its coloration and by the presence of well developed secondary sexual
characters. Thus, the body surface has now lost its metallic silver appearance and
become a dark brownish-grey. The female is clearly distinguished by an upward
curling of the tail, a distended trunk and a transparent ventral body wall through
which can be seen the mature eggs (Fig. 3D). The latter have become released into
the body cavity from the mesovarium and can be extruded through the cloaca by
applying pressure on the ventral part of the trunk. By contrast, the males are
slimmer, have a prominent urinogenital papilla projecting from the cloaca, and
the fluid constituting the milt can occasionally be detected through the body wall
(Fig. 3C). In both sexes, the gap between the two dorsal fins has disappeared and
the second may even encroach on the region occupied by the first. The female
also possesses a prominent heavily pigmented oedematous swelling at the base
of the second dorsal fin and, just behind the cloaca, a fin-like fold which is
separated from the most anterior part of the caudal fin (Fig. 3D). The teeth have
degenerated and are much shorter and blunter than previously and in preserved
specimens tend to be white rather than yellow. The nasopore is very conspicuous
LAMPREY METAMORPHOSIS. I
137
as a small elevated tube-like structure (Fig. 2G) and the regions immediately
surrounding the pits of the lateral line are raised. The oral fimbriae have
increased in size and, in preserved specimens, the disc tends to remain open
(Fig. 2H).
Key characters. N o gap between the two dorsal fins. I n the female, the eggs are
visible through the body wall, the tail is curved upwards and a post-cloaca1 (anal)
tin-like fold is present. In the male, a urinogenital papilla is present.
Stage 9 (spent adult)
The most noticeable difference between spent and sexually mature animals
(Stage 8 ) is that, particularly in the case of the female, the animal is more slender
(Fig. 3 E, F). By passing a finger along the ventral surface of the trunk the groove
remaining after the discharge of gonadal products during spawning can be
detected. The skin has now become very wrinkled, even in the branchial region,
and often shows signs of damage brought about during nest building and
spawning activity (Fig. 2 I, J).
Key characters. Similar to previous Stage but with loss of distension of body cavity
through emission of eggs and sperm.
Comparison ofthe stages in metamorphosis of Lampetra fluviatilis and
Lampetra planeri
The morphological changes in L. Jluuiatilis up to and including Stage 4, are
apparently indistinguishable (Fig. 4 A-E), from those already given for L. planeri
(Fig. 1 A,C,E,G,I). However, from Stage 5 onwards, the two species divergein the
pattern followed by the subsequent stages. Thus, although L. planeri has a silvery
sheen in Stages 5 and 6 (Fig. 4 F,G), it is never as marked as in these stages in L.
Jluuiatilis. Furthermore, whereas there is a subsequent decline in the silver
appearance in later stages of the brook lamprey, the end of metamorphosis and
the downstream migration in the river lamprey are periods marked by an
increase in the silvery sheen (Fig. 4 G,H). Other detectable differences between L.
fluviatilis and L. planeri in Stages 6 and 7 are the relatively much larger eye and
disc, the latter showing some inwards folding of the lateral edges to form a wide
slit, and the relatively slimmer branchial and trunk regions (ct: Figs 4 G,H and 2
C,E). The teeth are also much larger and sharper in the river lamprey than they
ever become in L. planeri.
Timing ofmetamorphosis in Lampetra planeri and Lampetra fluviatilis
From collections made in Highland Water during 1971172 and 1975176 an
estimate can be made of the time of initiation and rate of metamorphosis in
Lampetra planeri. It would appear from the records for these two years, and from
less comprehensive data for other years, that external metamorphosis cannot be
clearly observed to commence until between mid and late July, although in 1975
some Stage 1 animals were caught as early as the latter part of June. The data
presented in Table 1 show how rapidly animals pass through the initial stages of
metamorphosis, with the macrophthalmia (Stage 61, being attained in extreme
cases as early as the end of August. Generally, however, this Stage was not
reached until September, approximately eight weeks after the commencement of
LAMPREY METAMORPHOSIS. 1
I39
metamorphosis. The very earliest immature adults appeared in January and
mature individuals were first found in early March. Spawning generally took
place in April, the precise time depending on the attainment of critical water
temperatures (Hardisty 8c Potter, 197 1 b). Another feature of the data presented
in Table 1 is that it demonstrates that the initiation of metamorphosis occurred
later in 1971 than in 1975.
Data from Bransford Bridge on the River Teme indicate that the timing of
metamorphosis is similar in L. jluuiatilis with early metamorphosing stages also
being caught in mid to late July. I t is also clear that Stage 6 has been reached by
October and generally even earlier. Although the downstream migration may
reach a peak in the early spring (Potter 8c Huggins, 19731, it is clear from the
capture of downstream migrants in the estuary between late October and
February that metamorphosis can be completed by the early winter.
Morphological abnormalities
In a detailed examination of large samples of several species of lampreys from
the Lake Superior Basin, Manion (1967) found a number of morphological
abnormalities including most commonly the presence of additional caudal fins.
Although no such abnormalities were found in any of the 225 metamorphosing
L. juviatilis examined, one of the 504 metamorphosing L. planeri did possess an
additional caudal fin lying laterally and behind the cloaca. A similar situation
was also found in one of the numerous ammocoetes caught during this study.
Another abnormality was the failure of an eye to develop, one such case being
observed in L.jluuiatilis and two in L. planeri.
DISCUSSION
One of the main problems in any staging system is that it is attempting to
differentiate between characters that are part of a continual pattern of change.
However, the key characters, or combination of characters, that we have used for
the stages in Lampetra would appear to be of value in enabling estimates to be
made of how far an animal has progressed through metamorphosis. The validity
of the criteria employed is borne out by the consistency in the pattern of change
shown by measurements of certain regions of the body at different stages (Bird 8c
Potter, 1979).
Our scheme for metamorphosis in Lampetra differs from that for Petromyzon
marinus by Manion 8c Stauffer (1970) in its definition of the point at which
transformation can first be detected. For example, the figure illustrating Stage 1
in the landlocked sea lamprey corresponds very closely to that which we have
shown as Stage 3 in Lampetra. Thus a relatively well developed oval eye is present,
and the oral hood exhibits marked thickening of the lateral lips and a
considerable reduction in the thickness of the transverse lip. The evidence that
metamorphosis was obviously well under way by the time Manion 8c Stauffer
( 1970) commenced their descriptions of sequential stages is of interest in
the context of a recent paper on the anadromous form of the sea lamprey by
Youson, Wright 8c Ooi (1977). These workers recorded the presence of internal
changes in the endostyle, alimentary canal and kidney in the period four weeks
prior to the attainment of Manion 8c Stauffer’s first stage. Furthermore, they
140
D. J . BIRD AND I. C. POTTER
had a high success rate in detecting which animals would enter metamorphosis
by closely examining the degree of prominence of the eye, a character very
similar to that which we have used to describe our Stages 1 and 2. Although
Youson et ul. (1977) suggest the term prometamorphosis to cover these stages, it
might be more reasonable, as in this study of Lumpetra, to refer to them as the
initial stages of metamorphosis. An important consequence of being able to
detect external metamorphosis at an earlier stage is that it demonstrates that
many of the internal and external changes are initiated at a similar time. A clear
exception to this rule would appear to be the changes that take place in the
pituitary, nasohypophyseal stalk and the accessory olfactory organ (Leach, 1951 ;
Thompson, 197 1).
Although, mainly on the basis of detecting the early phases in the eruption of
the eye, we regard metamorphosis as commencing earlier than suggested by
Manion & Stauffer, there is reasonable correspondence in the criteria for
subsequent stages. The reason for the similarity in these stages is related to the
emphasis placed in both studies on the degree of development of the disc. Thus,
the Stages 1 to 3 described and illustrated for the sea lamprey are similar in
several details to our Stages 3 to 5 in Lampetru, while Stage 4 and the newly
metamorphosed P. marinus are comparable to the Stages 6 and 7 we have
described for the parasitic L.Juuiatilis.
The major internal difference between the earlier stages in the metamorphosis
of the two representatives of paired species is that in parasitic species little or no
gonadal development occurs during this period, whereas the gonads of the
brook lamprey start enlargement and maturation soon after the onset of
transformation (Hardisty & Potter, 197 lc). This contrasts therefore with the
situation regarding the external changes which are clearly very similar up to and
including Stage 4. In L. Juviatilis, the changes taking place towards the end of
metamorphosis are either preparations for a marine existence, e.g. increased
silver pigmentation, or for a parasitic mode of life, e.g. further development of
the teeth, whereas in L. pluneri they parallel those taking place on the upstream
migration of L. Juviatilis which follows the completion of the marine trophic
phase. They are thus changes associated with sexual maturation and lead
ultimately to the secondary sexual characters exhibited at spawning. It is for this
reason that mature male and female L. pluneri appear very similar to miniature
mature L. Juviutilis, with the female exhibiting a fin-like fold just behind the
cloaca and an oedematous swelling along the basal edge of the second dorsal fin
and the male possessing a clearly defined urinogenital papilla (Hardisty 8c Potter,
197 lb). From the above it can thus be seen that the major difference between the
metamorphosis of L. planeri and L. Juviatilis is that maturation occurs concomitantly with metamorphic changes in the brook lamprey whereas these
processes are discrete in the river lamprey.
The changes in the branchial chamber and oral hood appear to be directly
related to adaptations for a parasitic mode of life. That the changes are
essentially the same in both L. Juviatilis and L . planeri would also appear to
provide strong evidence for a view that nonparasitic lampreys evolved from
parasitic species. In other words, there would seem little support for the
contention of Piavis, Howell & Smith ( 1970)that the development of the oral disc
occurred first in nonparasitic lampreys, providing an example of preadaptation,
with the parasitic species being regarded as the derivative rather than the
LAMPREY METAMORPHOSIS. 1
I4 I
ancestral stock. Perhaps even stronger evidence for the ancestral position of
lampreys with a parasitic type of life cycle is the tooth arrangement on the oral
disc and tongue-like piston which must surely have been evolved to aid
attachment and rasping away of host tissue. Here again, the marked similarity
between the patterns of dentition found in the metamorphosing stages of L.
jluuiatilis and L. planeri provides good evidence for a close phylogenetic
relationship between these two species. This similarity can be contrasted with the
very considerable differences that exist between the dentition of the various
parasitic species belonging to different genera (Hubbs 8c Trautman, 1937;
Vladykov, 1955; Vladykov 8c Follett, 1958, 1965; Potter 8c Strahan, 1968; Hubbs
8c Potter, 197 1).
The data presented in this paper emphasize the highly synchronous nature of
lamprey metamorphosis. This point is well illustrated by the fact that in both
197 1 and 1975 the representatives of the rapidly completed second stage were
found in samples from any one site for a period of only three weeks. This implies
that lampreys possess a sensitive internal mechanism responsible for initiating
metamorphosis and that this may be triggered by a change in the environment.
That temperature might be such a factor is suggested by the later onset of
metamorphosis in 197 1 than in 1975, when temperatures during the period
preceding transformation were higher. Although a high degree of synchrony
exists in a particular region of a river, the actual time of onset of metamorphosis
often varies between rivers. For example, metamorphosis was estimated by Dines
( 1973) as commencing several weeks earlier in the River Honddu than the River
Wylye, with Highland Water being intermediate. Dines’ data showed that the
lowest maximum temperatures in the three rivers occurred in the Honddu and
the highest in the Wylye. It would therefore appear that if the temperature is the
trigger, it might be the rate of change which provides the stimulus. On the other
hand, it is possible that threshold temperatures may vary between populations in
different rivers, a feature that could be attributed to exposure to different
environmental regimes during the previous phase in the life cycle.
A similar synchrony to that in metamorphosis is found in the spawning period
of the brook lamprey. In populations of L. planeri in Highland Water, breeding
has sometimes been restricted to a few days, but more frequently extends to three
weeks between late March and the end of April, the latter duration being
consistent with the results given in the detailed study of adult brook lampreys by
Hardisty (1961). Since the onset of spawning has been shown to be related to the
attainment of a water temperature ofapproximately loo-1 1OC (Hardisty 8c Potter,
197 lb), the slightly later spawning period in the Honddu than Highland Water
found in each year is apparently attributable to the colder regimes found in the
former river. Since this situation contrasts with that regarding the onset of
metamorphosis there is evidence that within a geographical region the duration of
post-larval life is greatest in the coldest rivers.
Although our data for L.fluviatilis are more restricted than for L . planeri, there
are indications that while metamorphosis is initiated at the same time in the two
species, it proceeds at a faster rate in the river lamprey. In this study, such a view
is based on the capture of downstream migrants in the Severn Estuary at Oldbury
as early as October, which implies that metamorphosis would have been
completed in these individuals by late September. This is consistent with the
observation that only Stage 6 of L. Jluviatdzs were present in collections from
142
D. J. BIRD AND I . C. POTTER
Bransford Bridge in late September. More substantial evidence for the view that
metamorphosis is more rapid in the river than the brook lamprey is provided by
the rate of change over from the larval to adult condition, both with respect to
haemoglobins (Potter & Brown, 1975) and to haemopoietic sites (Percy & Potter,
1977).
Despite the capture of recently metamorphosed river lampreys in the estuary
in October and also November and December, many animals remain in the
rivers until the following spring (Potter & Huggins, 1973). The situation in the
river lamprey thus has some parallels with that described by Applegate ( 1950) for
the landlocked sea lamprey in the Ocqueoc River. Since both the above studies
provide ample evidence that the downstream migration is correlated with
increased water discharge or movement, the actual trigger for initiating the
migration is probably a disturbance of the substrate in which the animals are
burrowed. Thus, whether an animal migrates downstream in the autumn, or
remains in the river until the following spring, probably depends on whether it
has reached a sufficient stage of development in the autumn to respond to any
increased discharge at that time, prior to the decline in water temperatures
during the winter.
ACKNOWLEDGEMENT
Financial support was provided by the Science Research Council.
REFERENCES
APPLEGATE, V. C., 1950. Natural History of the sea lamprey (Petrumyzon marinus) in Michigan. Special Scientific
Report. United States Department ofthe Interior, Fish and Wildlife Service, 5 5 : 1-237.
BALABAI, P. P., 1948. (The time needed for metamorphosis in Lampetra mariae Berg). TrudJ Instytutu zoolohiyi.
Akademiya nauk Ukrayins’koyi RSR, myiu, I : 29-38. ( I n Ukranian).
BIRD, D. J. & POTTER, I . C., 1979. Metamorphosis in the paired species of lampreys, LampetraJuviatilis (L.)
and Lampetra planeri (Bloch). 2. Quantitative data for body proportions, weights, lengths and sex ratios.
ZoologzcalJournal ofthe Linnean Society, 65 : 145- 160.
DINES, R. A., 1973. Changes in the morphology, lipid and water ofmetamorphosing Lampetra planeri (Bloch) together
with observations on the larval velum andphatyruc. Ph.D. thesis, University of Bath.
HARDISTY, M. W., 1961. Studies o n an isolated spawning population of the brook lamprey (Lampetraplanerd.
Journal ofAnimal Ecology, 30: 339-355.
HARDISTY, M. W., 1971. Gonadogenesis, sex differentiation and gametogenesis. In M. W. Hardisty & I. C.
Potter (Eds),The Biology of Lampreys, I : 295-359. London: Academic Press.
HARDISTY, M. W. & HUGGINS, R. J., 1970. Larval growth in the river lamprey LampctraJuuiatilis (L.).Jounal
ofZoology, 161: 549-559.
HARDISTY, M. W. & POTTER, I . C., 197 la. The behaviour, ecology and growth of larval lampreys. In M. W.
Hardisty & I . C. Potter (Eds), TheBiology ofLampreys, I : 85-125. London: Academic Press.
HARDISTY, M. W. & POTTER, I . C., 197 lb. The general biology of adult lampreys. I n M . W. Hardisty & I . C.
Potter (Eds),The Biology of Lampreys, I : 127-206. London: Academic Press.
HARDISTY, M. W. & POTTER, I. C., 197 lc. Paired species. In M . W. Hardisty & I . C. Potter (Eds), The Biology
ofLampreys, 1 : 249-27 7 . London: Academic Press.
HARDISTY, M. W., POTTER, I. C. & STURGE, R., 1970. A comparison of the metamorphosing and
macrophthalmia stages of the lampreys Lampetrafluuiatilis and L. planeri. Journal of Zoology, 162: 383-400.
HUBBS, C. L., 1925. The life-cycle and growth of lampreys. Papersfrom the Michigan Academy ofscience, Arts and
Letters, 4 : 587-603.
HUBBS, C. L. & POTTER, I . C., 1971. Distribution, phylogeny a n d taxonoxry. In M . W. Hardisty & I. C.
Potter (Eds), The Biology of Lampreys, I : 1-65. London: Academic Press.
HUBBS, C. L. & TRAUTMAN, M . B., 1937. A revision of the lamprey genus Ichthyomyzon. Miscellaneous
Publications of the Museum ofZoology, University of Michigan, 35: 1-109.
LEACH, W. J., 1951. The hypophysis of lampreys in relation to the nasal apparatus.Joum1 of Morphology, 89:
217-256.
MANION, P. J., 1967. Morphological abnormalities among lampreys. Copeia, 1967: 680-681.
LAMPREY METAMORPHIS. 1
143
MANION, P. J. & STAUFFER, T. M., 1970. Metamorphosis of the landlocked sea lamprey, Petromyzon marinus.
Journal of the Fisheries Research Board of Canada, 27: 1735- 1746.
PERCY, R. & POTTER, I . C., 1977. Changes in haemopoietic sites during the nietamorphosis of the lampreys
Lampetrafluuiatilis and Lampetraplaneri. Journal ofZoology, 183: 1 1 1- i23.
PIAVIS, G. W., HOWELL, J. H. & SMITH, A. J., 1970. Experimental hybridisation among five species of
lampreys from the Great Lakes. Copeia, 1970: 29-37.
POTTER, I . C. & BROWN, I. D., 1975. Changes in haemoglobin electropherograms during the life cycle of
two closely related lampreys. Comparatiue Biochemistry and Physiology, 5 IB: 5 17-59 1.
POTTER, I . C. & HUGGINS, R. J., 1973. Observations o n the morphology, behaviour and salinity tolerance
of downstream migrating River lampreys (LampetraJuuiatilis).Journal ofZoology, 169: 365-379.
POTTER, I . C. & OSBORNE, T. S., 1975. The systematics of British larval lampreys. J o u m l ofZoology, 176:
311-329.
POTTER, I. C. & STRAHAN, R., 1968. The taxonomy of the lampreys Geotria and Mordacia and their
distribution in Australia. Proceedings ofthe Linnean Society of London, 179: 229-240.
THOMPSON, A., 197 1. Quantitative and Cytological Studies on the Adenophypophz’sis of Lampetra Ruviatilis and
Lampetra planeri wzth Particular RefPrence to Metamorphosis. M.Sc. thesis, University of Bath.
VLADYKOV, V. D., 1955. Lampetra zanandreai, a new species of lamprey from northern Italy. Copeia, 1 9 5 5 :
215-223.
VLADYKOV, V. D. & FOLLETT, W. I., 1958. Redescription of Lampetra ayrerii (Gunther) of western North
America, a species of lamprey (Petromyzontidae) distinct from Lampetra fluviatilis (Linnaeus) of Europe.
Journal ofthe Fisheries Research Board of Canada, 1 5 : 47-77.
VLADYKOV, V. D. & FOLLETT, W. I., 1965. Lampetra richardsoni, a new nonparasitic species of lamprey
(Petroinyzonidae)from western North America. Journal of the Fisheries Research Board of Canada, 22: 139-158.
WEISSENBERG, R., 1925. Fluss- und Bachneunauge (LampetraJuuiatilis L. und Lampetra planeri Bloch.), ein
morphologische- biologischer Vergleich. Zoologischer Anzeiger, 63: 293-306.
WEISSENBERG, R., 1926. Beitrage zur Kenntnis der Biologie und Morphologie der Neunaugen. I .
Vorderdarni und Mundbewaffnung bei LampetraJuuiatilis und planeri. Zeitschr4ft f u r Mikroskopisch-Anatomzsche
konchung. 5 : 153-284.
WEISSENBERG, R., 1927. Beitrage zur Kenntnis der Biologie und Morphologie der Neunaugen. 11. Das
Reilewachstuin der Gonaden bei Lampetra puuiatilis und planeri. Zeitschriji J i r Mikroskopisch-Anatomische
borschhung, 8: 193-249.
YOUSON, J. H., WRIGHT, G. M. & 001, E. C., 1977. The timing ofchanges in several internal organs during
nictaniorphosis of anadronious larval lamprey, Petromyzon martnus L. Canadian Journal of Zoology, 5 5 :
469-4 73.
ZANANDREA, G., 1959a. Recenti ricerche sulk forme “appaite” di lamprede dell’ Italia e del Danubio.
HoNettirro di %OfJ/UglU. Pubblicalo dell’ Unione Zoologica Italrana. 26: 545-554.
ZANANDREA, G.. 1959b. Speciation among lampreys. Nature, 184: 380.
ZANANDREA, G., 1 9 5 9 ~ .Lamprede parassite e non parassite nel bacino del Danubio c la nuova entita
siste111atic.aEudotitornvzon danfordi uladykoui. Archiriio Zoologtco Itahano, 44: 2 15-250.
ZANANDREA. G., 1961. Studies o n European lampreys. Evolution. 1 5 : 523-534.