Comp. Biochem. Physiol. Vol. 67B, pp. 475 to 484 0305-0491/80/1101-0475502.

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© Pergamon Press Ltd 1980. Printed in Great Britain

PHYSIOLOGICAL EVOLUTION IN THE

BRANCHIOPODS

W. T. W. POTTSand C. T. DURNING
Department of Biological Sciences, University of Lancaster, Lancaster LA1 4YQ, England

Abstract--The interactions of physiological and morphological evolution are discussed in relation to the
branchiopod crustaceans. Many branchiopods are morphologically relatively primitive and evade com-
petition from more advanced forms by physiological adaptations which enable them to survive in
extreme environments. The most recently evolved group of branchiopods, the Cladocera, or water fleas,
have specialisation of morphology and reproduction which have enabled them to return to less extreme
freshwater environments. Most recently they have developed physiological adaptations which enable
them to exploit the marine and other saline environments.

In his book A Molecular Approach to Physiology sea water and some of the earliest fossil branchiopods,
Marcel Florkin (1966) was at pains to emphasize that such as some species of Cyzicus, are found in marine
the organismic and the molecular approaches to rocks (Tasch, 1963) but freshwater species appear in
evolution are complementary, the evidence of one the Devonian and the branchiopods have been exclus-
reinforcing that of the other. Florkin discussed in par- ively freshwater for most of their existence. In the
ticular the evolution of the fibrinopeptides in the arti- Palaeozoic they were probably common in most
doctyls and of haemoglobins in the primates, showing freshwater habitats but with the development of more
how the biochemical evidence confirms, and may even advanced predators, particularly fast swimming fishes,
be used to quantify, the relationships within the two the slow clumsy branchiopods were eventually
orders deduced from comparative anatomy. Florkin reduced to extreme environments where predators
recognised three levels of evolution; changes at the could not follow them.
molecular level, changes at the physiological level, The first adaptations which enabled the branchio-
and finally changes at the anatomical level. While it is pods to escape from the fishes were the development
recognized that changes at the physiological or ana- of resistant eggs and short life cycles which allow the
tomical level cannot be independent of some subtle animals to survive in temporary ponds, an environ-
changes in DNA and in proteins, it is useful to con- ment closed to most fishes. The remarkable stability
sider the interaction of these three levels. Although of branchiopod structure---the conchostracan Cyzicus
changes at the three levels usually occur in parallel, in has survived since the Devonian; the notostracan
some cases they may alternate. A biochemical or Triops since the Triassic--may be related to this
physiological change which allows an animal to peculiar habitat. Fryer has pointed out the paradox
exploit a new habitat may then lead to morphological that all "permanent" water bodies have geologically
diversification, which might in principal be unaccom- limited lives and are subject to continuous change,
panied by further significant physiological or bio- while the essential characteristics of temporary ponds
chemical changes. The cases discussed below illustrate have remained unchanged down the ages (Fryer,
this point. 1979).
The branchiopoda are one of the most ancient, From the temporary pond the branchiopods have
primitive and, until recently, conservative groups of radiated out into other fish-free habitats by virtue of
crustaceans. Two of the living orders, the Notostraca some remarkable physiological specializations.
and the Conchostraca, can be traced back to the Amongst the anostracans Chirocephalus bundyi is
Devonian period or earlier (Tasch, 1963) while the found in pools of exceedingly pure water formed by
Devonian Lepidocaris has close affinities with a third melting snow, where the salt concentration is as low
order, the Anostraca. These three orders consist of as 0.04 mM Na/1 (Horne, 1968). Branchinecta lindahli
morphologically primitive animals with a large thrives in alkaline "soap lakes" where the pH may be
number of segments showing little differentiation as high as 9.8 (Prophet, 1963). Thamnocephalus pla-
along the body (Fig. 1). These primitive forms also tyurus is found in hot springs at temperatures up to
hatch as nauplii, an archaic crustacean feature, and 37°C (Horne, 1967), while Artemia salina can survive
the similarities between the larvae of the three orders in saturated, 10 osmolar, solutions of sodium chloride,
confirm that the branchiopods are indeed a natural approximately ten times as concentrated as sea water,
group and not merely a collection of primitive forms. while still maintaining the concentration of the blood
Although many branchiopods are morphologically less than 1 osmolar. (Croghan, 1958a).
primitive many are physiologically extremely sophisti- The physiological adaptations of Artemia salina, re-
cated, their remarkable physiological abilities com- sponsible for this remarkable feat, closely parallel
pensating to some extent for their archaic structure. those of the marine teleosts. Water balance is main-
The crustacea, like most animal groups, originated in tained by drinking the medium, sodium, chloride and
c.B.v.67/3a--1 475
476 W.T.W. POTTSand C. T. DURNING

la

Fig. 1. Primitive freshwater branchiopods. (a) Triops (Apus), Notostraca. (b) Estheria, Conchostraca. (c)
Branchinecta, Anostraca. Triops and Estheria from Borradaile et al. (1946).

water being taken up from the gut (Croghan, 1958c). the cladocerans in the absence of the nauplius larva.
The excess salt is excreted by specialised cells at the Cyclestheria first appears in the early Tertiary.
body surface (Croghan, 1958b) which are very rich in The Cladocera differ from the Conchostraca such
mitochondria (Copeland, 1967; Conte et al., 1972) and as Cyzicus in several important respects. First, in
Na-K-ATPase (Ewing et al., 1974). These cells are place of the large number of pairs of similar trunk
situated in the neck organ of the nauplius larva and limbs found in the Conchostraca the Cladocera pos-
on the basal epipodites of the adult limbs. The body sess only six, five or four pairs of trunk limbs which,
wall has a low permeability to chloride ions, which in the more advanced forms, become highly differen-
are actively extruded from the body, but is highly tiated to produce a complex and elegant, and highly
permeable to sodium ions, which are close to electro- efficient, feeding apparatus in which each pair of legs
chemical equilibrium across the body wall (Smith, differs from the others. Secondly, the rate of reproduc-
1969). A very similar system of ion balance was later tion is greatly increased by the adoption of partheno-
found in marine teleosts (Potts & Eddy, 1973). genesis. Males are generally absent and only appear
Throughout the Mesozoic and during the first half in adverse conditions. In some species they have never
of the Tertiary period the branchiopods were repre- been found. Lastly, in most species, all larval stages
sented only by the conservative orders Notostraca, are lost, young being retained in a brood chamber
Anostraca and Conchostraca (Fig. 1.) but in the Oli- (Figs 2 and 3) and, in the more advanced forms, are
gocene representatives first appear of the now ex- nourished by a placenta-like organ the "Nahrboden",
tremely successful order Cladocera, the water fleas until they are very large and fully developed. In some
(Fig. 2). The Cladocera are probably older than their species embryos of the third generation are develop-
first known fossils but they are unlikely to antedate ing before the birth of the second.
the Tertiary. The nearest relatives of the Ctenopod With their efficient feeding mechanisms and high
cladocerans appears to be the conehostracan genus reproductive rates the cladocerans have been able to
Cyclestheria which, like the water fleas, has a cyclo- adapt to most freshwaters, in spite of the predation
pean eye formed by fusion of the more usual crusta- that they suffer, and have undergone an explosive
cean pair and which also resembles the majority of diversification so that they now include not only pela-
 Physiological evolution in the branchiopods 477

a b

¢ d

4
q
Fig. 2. Cladoeerans from saline waters. (a) Bosmina coregoni (marine). (b) Penilia avirostris (marine). (c)
Moina hutchinsoni (saline lakes). (d) eodon leucarti (marine). (e) Evadne nordmanni (marine). (f) Pleone
(Podon) polyphemoides (marine). P. avirostris from Lochhead (1954). P. leucarti and E. nordmanni from
Mordukhai-Boltovskoi (1971) Pleone (Podon) polyphemoides from Newell & Newell (1977).

gic filter feeders but also detritus feeders, scrapers and eyes, six or four pairs of short stenopodous legs and
carnivores. The remarkable success of the cladocerans with a carapace reduced to a brood chamber (Gym-
may be illustrated by a few figures. In Britain there nomera) (Fig. 2 d-f and Fig. 3). The Gymnomera are
are no conchostracans but there are at least 89 spp. of unknown as fossils except in post-glacial deposits.
cladocerans (Scourfield & Harding, 1958). In the The remarkable recent success of the cladocerans
U.S.A. there are only 27 conchostracans but 139 spp. has been due primarily to morphological develop-
of cladocerans (Pennak, 1978). In relative biomass the ments but the physiological enterprise apparent in the
difference is much greater than even the number of primitive branehiopods is also found in the clado-
species suggests. cerans and enables them to exploit new habitats.
The majority of the Cladocera are water fleas in the Several genera of cladocerans have returned to the
narrow sense with comb-like limbs enclosed in a oceans where they are now almost ubiquitous. Their
bivalved carapace (Calyptomera) (Fig. 2 a--c) but an rapid rate of reproduction and morphological sophis-
alternative development has been the evolution of tication may give them an advantage over the com-
predaceous or macrophogous forms with very large petitors belonging to more ancient marine crustacean
 478 W.T.W. POTTSand C, T. DURNING

Sea Water
Caspian Water

Fig. 3. The Caspian cladocerans and their origins. (a) Evadne nordmanni. (b) Polyphemus pediculus. (c)
Bythotrephes longimannus. (d) Cercopagis micronyx. (e) C. pingoigracillima. (f) Apagis cylindrata. (g)
Podonevadne camptonyx. (h) P. triaona. (i) P. angusta. (j) Corniger maeoticus. (k) Caspievadne maximowits-
chi. (1) Polyphemus exiguus. E. nordmanni, P. pediculus, B. longimannus from Mordukhai-Boltovskoi
(1968). C. micronyx, A. cylindrata, P. camptonyx, C. maeoticus and C. maximowitschi from Mordukhai-
Boltovskoi (1965). P. exiguus, Mordukhai-Boltovskoi (1971). P. pediculus, M. hutchinsoni and B. coregoni
from Pennak (1953).

stocks, but they retain low blood concentration like euryhaline. Evadne nordmanii has been recorded in
their freshwater ancestors so to survive they must salinities ranging from 1.33-35.49/o (Ramner, 1937)
osmoregulate like teleosts or Artemia. Other species quoted by Baker, 1938); E. spinifera has been reported
are found in coastal and estuarine waters, while in the in fresh waters from the river Ingul, Russia, while
Caspian Sea the cladocerans have diversified into a Pleopis (Evadne) tergestina was one of the first marine
remarkable variety of forms, possibly because the un- animals to be found in the Bitter Lakes after the Suez
usual salinity has reduced competition (Fig. 3). canal was opened, where it was found immediately
Several species of water fleas, including Moina hut- above the beds of rock salt (Gurney, 1927). Clado-
chinsoni and Daphniopsis pusilla (Fig. 2c) live in saline cerans can be found quickly in living marine plankton
lakes while others have a remarkable resistance to by diluting the sample with sufficient freshwater, 50 or
acidic waters. AIonella excisa fluorishes in waters as 100~ by volume, to kill all other animals but leave
acidic as pH 3.3 (Potts & Fryer, 1979). the polyphemoids unharmed.
The most abundant marine cladocerans are species Evadne has an ability to regulate the blood concen-
of the genera Podon, Pleopis and Evadne, members of tration comparable to that of a euryhaline brackish
the Polyphemoidea (Fig. 2) which are probably recent water animal of freshwater origin (Fig. 4) but efforts
immigrants to the oceans. There are only 12 species in at Lancaster to adapt it to freshwater or hypersaline
all and their zonal distribution is determined largely conditions have not been successful. Teleosts and
by temperature. For example Pleopis (Podon) poly- Artemia, the hypo-osmotic regulators previously
phemoides (Gieskes, 1971a) is found in both the north examined, have areas of epithelia specialised for salt
Atlantic and the north Pacific and again in the south secretion. Silver staining to determine the more per-
Pacific and south Atlantic but is rare in the tropics meable portions of the exoskeleton followed by an
(Baker, 1938). Marine polyphemoids are remarkably examination of the underlying tissues by electron
 Physiological evolution in the branchiopods 479

/
14 /J
/
//
//
/
/
/
/
o I0

_d,*." I,
~o~
15
'~ OE
§ -Ppediculus
//
¢Z

¢/
/
//
02 /
//
/

o'z o'~ o'6 o'~ ;o ,!z ,'4 ,'6 ?8 2'o

Concentrationof Medium(~ °C )

Fig. 4. Graph of the freezing point depression (A°C) of the haemolymph of Evadne nordmanni against
that of the external medium. The value for Polyphemus pediculus in fresh water is also included. (E.
nordmanni caught in Liverpool Bay area of the North Sea). Adapted for 18 hr. P. pediculus from
Windermere. Seawater 35%° has a freezing point depression of 1.91°C.

microscopy (Fig. 7) demonstrates that the site of salt dria, which together with an elaborate system of en-
secretion in Evadne is the neck organ or "Haptor- doplasmic tubules or lacunae, form the greater part of
gan". This is a conspicuous feature in certain marine the cell (Fig. 7). The tubules are confluent with the
and freshwater cladocerans and has previously been extracellular fluid through basal or lateral folds of the
considered to be a respiratory organ (Dejdar, 1931). It cell membrane. In these features they resemble the
consists essentially of eight large cells situated under a salt secretory cells found in the epipodites of Artemia
thin window in the exoskeleton, in the neck region and the "chloride" cells or mitochondria-rich cells of
(Fig. 5). These cells are exceedingly rich in mitochon- the fishes. The position of the neck organ indicates

Fig. 5. Dorsal and oblique views of the neck organ of Evadne nordmanni showing eight cells rich in
mitochondria underlying window in shell. From Dejdar (1931).
480 W.T.W. POTTSand C. T. DURNING

Sea water Fresh water

Fig. 6. Diagrammatic representation of possible routes of ion movements through neck organ cells in
seawater and freshwater. Solid lines active transport, broken lines passive diffusion.

that it is probably homologous with that of the naup- rents where it seems unlikely that they could be de-
lius larva of Artemia, although in the Polyphemoidea rived from coastal populations (Gieskes, 1971b). The
all larval stages have been suppressed: an interesting mid-Atlantic spring populations may be descended
example of paedomorphosis, the incorporation of lar- from a very sparse population which winters in the
val characters into the adult. surface waters, although in this case sexual reproduc-
Circumstantial support for the involvement of the tion should not occur, or alternatively the eggs may
neck organ in osmoregulation has been provided by be buoyant.
Khlebovich & Aladin (1976~ who found that the Buoyancy of the whole animal is an interesting and
osmolarity of the "marsupial fluid" in the brood valuable bonus which accrues to hypo-osmotic regu-
chamber of Evadne equalled that of the haemolymph lators in saline waters. Protein, carbohydrates and
until the neck organ of the embryo was formed, at skeletal materials are denser than water and most
which point the contents of the brood pouch rose in pelagic marine invertebrates must either expend
concentration to the value for the surrounding sea energy continuously in maintaining station or invest
water. This ability to regulate the embryonic environ- more energy in low density oil droplets, which have
ment and so protect the early developmental stages the additional disadvantage of being conspicuous to
from extremes of osmotic stress requires the isolation predators. Sea water containing 359oo salt has a den-
of the brood fluid from the external medium. The sity of about 1.028 and the blood of most hypo-
ability to close the brood sac is a unique feature of the osmotic regulators is between 1 and 2~o less dense
polyphemoidean cladocera which may have aided than seawater. Dilute seawater, with a freezing point
them in their colonisation of the sea. It is also inter- depression similar to that of Evadne, 0.85°C (Fig. 4)
esting to note that the polyphemoids, together with has a density of 1.0125, while isotonic sodium chlor-
Penilia and Moina, the three groups which have ide has a density of 1.0102. The body water of marine
invaded high salinity environments, are the only cla- cladocerans, which probably contain proportionately
docerans to possess a "placenta" which secretes a less magnesium and sulphate than sea water, will lie
fluid, presumed to be nutritive, into the brood between these figures.
chamber. Specimens of Evadne can often be seen hanging
Ever since they became adapted to life in tempor- motionlessly near the surface of marine plankton
ary pools the branchiopods have produced resting samples and Lochhead (1954) reports that Penilia also
eggs at some stage of their life cycle. In freshwater floats in this way. In nature the marine cladocerans
cladocerans males only appear in the population in are found mainly in the upper 20 metres of the water
adverse conditions and resting eggs, produced after both by day and night (Bainbridge, 1958; Gieskes,
fertilization, usually sink to the bottom where they 1971) and diurnal vertical migration has only been
hatch when conditions are favourable once again. In reported in the dilute waters of the Caspian
most populations in temperatate latitudes males (Mordukhai-Boltovskoi & Rivier, 1971) and the Che-
appear in the autumn and the eggs hatch in the sapeake Bay (Bosch & Rowland Taylor, 1973). By
spring. It is not clear how this cycle is adapted to maintaining their position in the well lit superficial
oceanic conditions where the depth of the water is too waters the buoyancy which hypotonia confers on the
great to allow the resting egg to sink to the bottom or polyphemoids must be of particular value to these
to allow the newly hatched form to reach the surface. daylight feeding predators.
It is possible that the complete cycle takes place in The Polyphemoidea are macrophagous feeders and
shallow coastal waters but plankton surveys show lack the elaborate filtering mechanisms found in the
that Podon and Evadne appear early in the spring majority of cladocerans. Penilia avirostris, Fig. 2b
almost simultaneously over vast reaches of the Atlan- (Sididae), a more typical "water flea", is quite widely
tic and then extend westwards against the water cur- distributed in coastal waters in the warmer parts of
 Physiological evolution in the branchiopods 481

the world and may be presumed to osmoregulate and 3). The Podonidae and the Cercopagidae have diversi-
to have cells adapted to salt excretion but so far Peni- fied in a most remarkable manner, presumably
lia has not been examined in detail. Moina hutchin- because they have had the opportunity to exploit a
soni, Fig. 2c, (Mohaidae) is widely distributed in salt large environment with little competition. So far no
lakes in north America. A preliminary examination data are available on the blood concentration of these
(Hunter, 1975 unpubl.) showed that in water from forms. The salt content of the Caspian Sea, around
Lake Abert, Oregon, containing 1120 mOs/1, M. hut- 13%o (A0.74°C) in the centre and south, is about the
chinsoni maintained a blood concentration of only concentration where eurythaline fishes and Artemia
480 mOs/1 (Table 1). Silver staining showed that the are iso-osmotic with their media. Mordukhai-
most permeable areas in the exoskeleton were narrow, Boltovskoi (1968a) notes that in the Caspian species
elongated patches on the thoracic limbs, which are the neck organ is peculiarly well developed and that
presumably underlain by the secretory cells. Bosmina the majority of species are found in the more saline
coregoni is widely distributed in fresh waters but a centre and south of the Caspian. These observations
closely related form, Bosmina coregoni marina (Fig. 2a) indicate that both the cercopagids and the podonids
lives in estuaries and coastal waters. In view of its are generally hypo-osmotic regulators. On the other
freshwater origin it may be expected to be hypo- hand Cercopaois penooi and a subspecies of Podone-
osmotic to sea water but this has yet to be demon- vadne trioonia and Cornigerus maeoticus (Fig. 3h, j)
strated and the site of the salt secretory cells, if they are also found in the freshwater of the river Dnieper
occur, is unknown. and have spread into the more brackish regions of the
Podon, Evadne, Penilia and Bosmina are all rela- Sea of Azov but not into the more saline areas. One
tively recent immigrants into die oceans where they marine polyphemid, Pleone (Podon) polyphemoides,
face competition from the host of marine crustaceans. has recently penetrated into the Caspian. The diver-
Where competition is reduced the cladocerans show a sity of bizarre forms which have developed in the Cas-
remarkable ability to expand and diversify. The sali- pian is most remarkable (Fig. 3) but the functions and
nity in the south of the Caspian Sea is approx 13~'o~ selective advantages of their peculiar specialisations
including 136mM Na, 31 mM M~ 151 mM CI and are uncertain.
31 mM SOdl, (Hedgpeth, 1957), about one-third that It is remarkable that Artemia, Podon, Evadne and
of seawater, too high for the majority of freshwater Moina have all maintained a low blood concentration
animals to tolerate but too low for most marine ani- on returning to the sea or to saline lakes and in this
mals. Towards the mouth of the Volga the salinity is they resemble the marine teleosts, the sturgeons, the
even lower. It seems most probable that the present lampreys and some amphibian tadpoles. Closer exam-
peculiar concentration of the Caspian is a recent ination of Artemia and a number of teleosts has
phenomenon. In pre-glacial times the Caspian Sea shown that in both cases the animals have a high
was part of a much more extensive sea which permeability t o sodium but are less permeable to
extended from the Balkans to central Asia, while the chloride ions, which are actively extruded to maintain
Black Sea was a freshwater lake during the glacial the low blood concentration. The remarkable similar-
periods (Hsii, 1978). The Caspian Sea is now the ities observed between teleost chloride cells and the
centre of speciation of a remarkable group of endemic cells of the neck organ of marine cladocerans suggests
cladocerans. 25 distinct species grouped into six that a similar transport system occurs in each. These
genera have been described to date (Mordukhai- striking examples of convergent evolution in different
Boltovskoi 1968a, Mordukhai-Boltovskoi & Rivier, phyla call for some explanation. It has been argued
1971) and a few species are found in neighbouring (Potts, 1959) that hypo-osmotic regulation in marine
waters such as the Volga, the Don and the Sea of animals is an economical adaptation. Although at
Azov. The endemic Caspian cladocerans fall into first sight it would seem to require an unnecessary
three groups, the Podonidae which are of marine ori- dissipation of energy at the body surface, a consider-
gin, descended from some species of Evadne, the Cer- ation of the energy budget required for ionic balance
copagidae, which are of freshwater origin, descended in the body as a whole suggests that the energy saved
from Bythotrephes, and a solitary species of Poly- at the surface of the cells, as a result of the reduced
phemus which must also be of freshwater origin (Fig. sodium concentration in the extracellular fluids,

Table 1. The concentrations of the blood of saline water cladocera and their
freshwater relatives. For comparison the concentration of the blood of Artemia
saline and the eel, Anguilla rostrata, are also included

Mean External
blood medium
Species (mOsm) ( m O s m ) Reference
Evadne nordmanii 457 1102 Durning (1978, unpublished)
Evadne nordmanii 409 688-747Khlebovich & Aladin (1976)
Podon leuekarti 403 688-747Khlebovich & Aladin (1976)
Polyphemus pediculus 224 F.W. Durning (1978, unpublished)
Moina hutchinsoni 480 1120 Hunter (1975, unpublished)
Moina brachiata 160 F.W. Durning (1979, unpublished)
Artemia saline 365 1048 Croghan (1958)
AnguiUa rostrata 441 995 Smith (1932)
482 W. T. W. POT'ISand C. T. DURNING

greatly exceeds the energy required for hypo-osmotic however both Artemia and the teleost chloride cells,
regulation at the body surface. while actively transporting chloride ions, are exceed-
Artemia and the teleosts both maintain hypo- ingly rich in Na-K-ATPase (Ewing et al., 1974; Kar-
osmotic body fluids by the active excretion of chloride naky et al., 1976) but this is confined to the serosal
ions and it may be suspected that the hypo-osmotic side of the cells.
cladocerans do the same. This is the more remarkable The model of chloride transport recently suggested
when all animal cells actively excrete sodium ions. It by Silva et al., 1977, together with the observation
would seem a simple matter to develop a sodium that cells taking up salt in freshwater cladocerans
excreting epithelium by confining sodium transport to occupy the same site as cells excreting salt in marine
the outer side of the epithelial cells. Paradoxically ones, provides a possible explanation of this paradox.

~!!~!!!~ ~ ~i~ii~i~ ~i~ ~ ~i ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ i

Fig. 7. Electron micrograph of a longitudinal section taken near the centre of the neck organ of Evadne
nordmanni showing parts of three mitochondria rich cells underlying the permeable "window" in the
cuticle. ( x 4500). Inset: Neck organ of E. nordmanni (arrow) x 60 (approx)
 Physiological evolution in the branchiopods 483

In freshwater animals sodium transport across the 0.99°C, the body fluids of P. avirostris had a freezing point
cell base from cytoplasm to blood appears to be the depression of A 0.72°C equivalent to 387 mOsm/l. Aladin
primary motive force in salt uptake (Fig 7). Salt is V. (1978) Hypoosmotic regulation in marine cladoceran
actively removed across the serosal membrane lower- Penilia avirostris Zh. Evol. Biokhem. Fixiol. 14 (6), 599-601.
ing the electrochemical potential of sodium in the
cytoplasm until it enters across the mucosal surface.
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