Conquering terra firma: The copper problem from the isopod's point of view
Conquering terra firma: The copper problem from the isopod's point of view
W O L F G A N G
KURZFASSUNG: Eroberung des Festlands: Das Kupferproblem vom Gesichtspunkt der Isopoden. Marine Crustaceen mfil~ten theoretisch in der Lage sein, dem Atemwasser geniigend viel Kupfer zu entnehmen, um selbst schwerste t~iglicheVerluste zu ersetzen. Im Vergleich dazu diiri°cedas in der Pflanzennahrung angebotene Cu mengenm~iffig eine nur geringe Rolle spielen. Dennoch muff das vegetabilis&e Cu ausreichen, um den Bedarf herbivorer terrestrischer Crustaceen an diesem Metall zu decken. Die Probleme, die im Zusammenhang mit der Immigration yore Meer zum Land hinsichtlich der Kupferversorgung entstehen, werden am Beispiel litoraler und terrestrischer Isopoden und Amphipoden - zum Tell in spekulativer Form - diskutiert. Vergleichende Untersuchungen haben ergeben, daff terrestrische und litorale Isopoden die Menge der aufgenommenen Nahrung gegenilber marinen Arten nicht erh/Shen und daff die Assimilation yon Cu aus der Nahrung in ausreichender Weise nut durch die Beihilfe yon Mikroorganismen m/Sglichzu sein scheint. Der Zugang zu einem n~ihrstoffreichen, yon Mikroorganismen gut durchgearbeitetem Substrat muff also eine der Hauptvoraussetzungen ffir eine funktionierende Kupferversorgung aus pflanzlichem Material sein. Aul~erdem nimmt die Menge des im Hepatopancreas gespeicherten Cu in der Reihe marine - litorale - terrestrische Crustaceen zu. Auch die Leistungsf~ihigkeit der Kupferasslmilation ist im Vergleich zu litoralen bei terrestrischen Isopoden gr/Sfer. W~ihrend bei Porcellio scaber die Kupferassimilation in direkter Abh;ingigkeit yore Kupfergehalt der Nahrung steht und Werte fiber 90 °/0 erreichen kann, betr~igt bei Ligia oceanica und Orchestia garnrnarella die Kupferassimilation bei mittlerem Kupfergehalt (0,2 bis 0,3 /~g/mg Trockengewicht) nur etwa 66 °/0, urn dann wieder abzunehmen. Schliefllich wird im Vergleich zu marlnen und litoralen Isopoden der Kupferstoffwechsel terrestrischer Isopoden besser geregelt, indem Cu ausschliefflicher in besonderen Zellen gespeichert und jede umfangreiche Mobilisierung des Metalls yon der Synthese charakteristischer Sekrete begleitet wird, die Stoffe (wahrscheinlich Proteide) enthalten, deren Aufgabe zu sein scheint, freies Cu zu binden. Dies wiirde sowohl dessen toxische EigenschaRen reduzieren, als auch Verluste dieses Metalls an das Blut und in das Darmlumen verhindern.
Institut fiir Zoologie der Universitiit Innsbruck; Innsbruck; Osterreich
I N T R O D U C T I O N
Amongst the numerous problems that faced marine animals when they attempted
to extend their range of existence beyond the sea was that of how to replace the rich
supply of nutrients given to their ancestors in the form of a medium which was not
o n l y a means of transport, but also an excellent solvent for inorganic and organic
compounds. The conquerors of terrestrial habitats found themselves in the position of
having to obtain now all b o d y constituents (with the exception of oxygen and
occasionally - some water) from their food. This not only shiflced the port of entry
for a number of ions from gills and similar epithelia to the gut, it also caused
additional complications in the case of those elements that abundantly occur in ionic form
in sea water, but are present in the food largely as organic complexes. A case in point
is copper; I shall try to outline some of the problems involved in the uptake and use
of this element by referring to isopods (and amphipods) as if they "knew" what they
were up against.
RESULTS A N D C O N C L U S I O N S
Copper is an element of great biological importance since it is present in some
vital enzyme systems as well as in the main respiratory pigment of crustaceans and
molluscs. N o thorough study has been made of the pathway of copper uptake in
marine animals, but the work of ZUCKERtiANDL(1960) and of
KERKUT, MOP,ITZ &
) suggests that in crustaceans at least it is taken up from the medium
via the gills. For cephalopods, however, as
GHIRETTI & VIOLANTE(1964
) have shown,
the main source of copper seems to be the food.
With respect to isopods the position for supplying the organism with a sufficient
amount of copper is roughly the following: An isopod of 2 cm length, 0.5 cm width,
weighing about 100 rag, has a gill area which measures at least 25 mmL By creating
turbulence currents a water layer 1 mm in thickness can be swept by the pleopods.
Assuming a rate of water flow past the gills of 1 cm/sec, a volume of 200 ml/hr or
approximately 5 1/day will be filtered by the gills of the animal. This figure compares
well with the rates of water transport in many ciliary feeders (BA~KER-JoRcENSEN
Seawater contains from 5 to 20 #g of copper per litre (
). In coastal
areas where the transition from sea to land took place, the concentration may even be
higher (recently, I measured 25 to 35/~g/1 near the Zoological Station of
Kristineberg, Sweden). Assuming a copper content of 20 I~g/1, an extraction coefficient of 25 °/0
and the rate of water flow indicated above, the model isopod should be able to extract
from its medium 20 to 25/~g Cu/day. Since isopods of this size contain between 0.1
and 3 ~g Cu in their main storing organ, the hepatopancreas (WIEsER 1965a), it is
clear that any loss of this metal - as, e. g., described by ZUCliERKANI~L(1960) for
moulting Maja squinado - could easily be compensated by uptake from the medium,
provided a diffusion gradient is maintained between the latter and the body fluid.
In contrast, food would appear to offer only a fraction of the copper available
in the medium. From the data presented for Naesa bidentata (WxEsER 1962, 1963),
it can be roughly estimated that herbivorous marine isopods consume a maximum
of 100/~g of dry algal food/rag of fresh body weight/day, which is equivalent to
about 50 mg of fresh algal food per animal and thus to a volume of 0.05 ml of
water, 10-5 times the volume of water passing the animal's gills in the same period
of time. Species of Fucus concentrate copper from sea water by a factor of I00 to
BLACK & MITCHELL 1952
). Thus, even if extraction of this element from
seaweeds could be engineered with the same efficiency as extraction from water, the food
would supply only about 0.5 to 1 °/0 of the total copper available to the animals.
There are, however, several reasons for suspecting that the extraction of copper from
seaweeds is a much more costly process than uptake of this element from water. This
is indicated by the fact that leaching in water hardly liberates any of the copper
present in algae, the reason being that in plants copper forms organic complexes,
mainly with proteins and carbohydrates (
Now, crustaceans that have once migrated on land and thus do not benefit from
the presence of copper dissolved in sea water will have to obtain this metal entirely
through their food. Intertidal forms that are periodically covered by water could
represent a transitional series with increasing dependence on food as the main
source of this and other elements. Despite its relative unimportance as a copper source
for herbivorous marine crustaceans, plant material per se still offers considerable
amounts of this metal to clever consumers. I f food contains 1 % of the copper
available to the animal in sea water, an isopod extracting it with 25 % efficiency
would obtain about 0.2/~g per day, sufficient to compensate for a daily loss of
onefi~h of the copper stores of, say, Idotea neglecta. In order to exploit fully this
potential source, terrestrial crustaceans could employ several stratagems; they could
(1) increase food consumption, (2) improve the selective absorption of copper from
the food material passing through the gut, (3) increase their copper stores, thus
widening safety margins for times of need, (4) reduce copper losses by regulating the
movements of this metal between the stores and other body compartments.
A quick evaluation of these pathways open to terrestrial and semi-terrestrial
crustaceans shows that food consumption does not seem to increase with the
acquisition of terrestrial habits. In the terrestrial isopod Porcellio scaber, specimens weighing
20 mg consume a maximum of 100/~g dry leaf litter per mg per day (WIESER 1965b),
that is, an amount of dry organic material exactly equal to that calculated for
representatives of the marine species Naesa bidentata of similar size. Moreover, an
experimental feeding rate of 100 # g d r y organic matter/mg/d - for reasons given
earlier (WIEsER 1965b) - is almost certainly too high and under natural conditions
might be reduced to 1/~ in the case of P. scaber. An increase in food consumption
therefore does not appear to be the isopod's method of choice for increasing its supply
The second possibility, improvement of selective extraction of copper from
ingested food, turns out to be a tall order. As was shown before (WI~sER 1966),
terrestrial isopods seem to be incapable of assimilating copper from their natural diet,
dead leaves, unless the latter have been artificially enriched to values far beyond
those likely to occur in nature. It was postulated that an additional mechanism has
to come into play in order to give terrestrial, herbivorous crustaceans access to
copper, this mechanism being the participation of microorganisms. P. scaber, feeding
on leaf litter, will at first loose copper through its faeces. Gradually the faeces
accumulate and form a substrate for microbial activity in which organic complexes are
broken down and copper is liberated. By reingesting their faeces, terrestrial isopods
will now be able to assimilate the copper that was denied to them in the first place.
In a limited sense, then, it can be said that micro-organisms replace seawater as the
source of free copper in the ecological series from marine to terrestrial species of
C o p p e r budgets of specimens of L. oceanica a n d O. gammarella, based on feeding e x p e r i m e n t s
w i t h Fucus vesiculosus in n o r m a l condition or artificially enriched w i t h copper salts
p u r s u e t h i s q u e s t i o n , a n i n v e s t i g a t i o n i n t o t h e c o p p e r b u d g e t s o f Ligia oceanica a n d o f
the a m p h i p o d Orchestia garnrnarella was carried out in the summer of 1966 at the
Zoological Station of Kristineberg in Sweden. The study was analogous to the one reported
earlier with Porcellio scaber (WIEsEr, 1966), Fucus vesiculosus from wrack beds - soaked
'in distilled water, sea w a t e r or in various solutions of copper sulfate and copper
t a r t r a t e - serving as the food. The results are set out in Table 1 and in Figure 1,
indicating that, as in P. scaber, assimilation of copper under experimental conditions
i ! ,.°
Copper content of food (IJg/mg dry weight)
seems to be possible only when the metal is present at high concentrations. The
"breaking even p o i n t " - i. e. the concentration at which copper is neither gained nor
lost - is similar for the single species of a m p h i p o d and the two species of isopods,
a p p r o x i m a t i n g 0.15 to 0.2/~g C u / m g d r y food. H o w e v e r , in the case of the
investigation carried out at Kristineberg, the copper content of F. vesiculosus from wrack
beds turned out to be so high (0.07 to 0.38/~g/mg d . w . ) t h a t this seaweed could
conceivably serve as the n a t u r a l source of copper for the local populations of L.
oceanica and O. gammarella. Its copper content is about one order of magnitude
higher than the concentrations reported for F. vesiculosus from P l y m o u t h by
) but of a p p r o x i m a t e l y the same order as t h a t given by the same
authors for Larninaria digitata fronds. C o n t r a r y to the findings with .P. scaber,
enriching the food with copper salts did not increase the assimilation of copper in
O. garnmarella and L. oceanica (see below). At other localities where the water, and,
consequently, the seaweeds, contain less copper than they do at Kristineberg, intertidal
crustaceans would appear to be as much at a loss for obtaining their copper supplies
through the primary vegetable material as P. scaber proved to be. Intertidal species
have the advantage of being able to use the free Cu dissolved in sea water, and it will
have to be the subject of further research to find out exactly to what extent they
employ this possibility for dealing with their copper problems. I f they do not, they
Copper content of hepatopancreas
(pg/mg of wet body weight)
: I V
would either have to call for microbial assistance as their terrestrial cousins do, or
they would have to prey on other crustaceans, exploiting the latter's ready made
copper stores. O. garnrnarella has chosen the former solution since it lives in the wrack
beds along the coast, an environment with a rich and varied microbial flora. In fact,
O. garnrnarelta is instrumental in bringing about the microbial degradation of the
Fucus beds along the shore ( R ~ M ~ T 1960) just as terrestrial isopods are instrumental
in bringing about the microbial degradation of leaf litter on land. L. oceanica may
also be found amongst dead seaweeds, but it is a truly omnivorous species and thus,
theoretically at least, capable of covering its copper requirements by feeding on other
crustaceans, just as Octopus vulgaris maintains its copper stores by preying on
Carcinus rnaenas (GH~RETTI& VIOLANTE1964).
Marine isopods can always replenish their copper reserves from the ever present
medium whereas intertidal and terrestrial species are not always exposed to optimum
conditions for the replacement of lost copper. Consequently, it could be argued that
increasing the copper stores in the body would be a feature of adaptive value in
landbound immigrants from the sea. As has been pointed out before ( W I E S E R 1965a),
such an increase in hepatopancreas copper is in fact observed when isopods and
amphipods are arranged in an ecological series from subtidal to supratidal and
terrestrial species. The data, supplemented by new data for L. oceanica and Oniscus
aselIus from Sweden, are presented in Figure 2. An interesting case is that of
Sphaeroma serraturn, which usually is considered a truly marine species although its copper
content places it amongst the terrestrial species. N o w REMlvI~Ra"(personal information)
has discovered that at least some species of this genus indeed lead a nearly terrestrial
I I i
> / /
N o t only the storing capacity for copper increases in terrestrial isopods, but also
their ability of assimilating this element from artificially enriched food. In P. scaber
the assimilation of copper increases proportionally with the copper content of the
food, reaching m a x i m u m values of more than 90 0/0 at food copper levels higher than
5/~g/mg dry weight (WIEsER 1966). In L. oceanica and O. gammarella copper
assimilation increases up to an input/output ratio of about 3, equivalent to 66 %
assimilation, at food copper levels of 0.2 to 0.3 /~g/mg dry weight. Increasing the
copper content of food still more does not, however, increase the input/output ratio.
On the contrary, in the few experiments in which members of these two species could
be induced to feed on a high copper diet, the extraction efficiency dropped to values
between zero and 30 °/0. It may therefore be concluded that the ability to extract and
to store vast amounts of copper, if this element is presented in digestible form, is an
adaptive characteristic of truly terrestrial species of isopods. Intertidal species may
have high storing capacities too, but their ability (or, rather, their willingness?) to
increase assimilation efficiency in direct proportion with the amount of copper offered
in the diet is limited (Fig. 3). This must reflect their less precarious situation with
respect to this food constituent.
Finally, there is the point of the regulation of copper content within the body.
A marine crab like Maja squinado may lose 50 0/0 or more of its total copper during
. The copper content of the only subtidal species of
isopod investigated so far, Conilera cylindracea, may vary over nearly two orders of
magnitude (WIEsER 1965a). This obviously is not an advantageous state of affairs if
the acquisition of copper is as problematical as it turns out to be in terrestrial
crustaceans. In consequence, the mode of copper storing and of copper mobilization seems
to have changed in step with the conquest of land by isopods. In decapods copper may
be stored in the form of pseudo-crystals or of large refractive bodies in special "copper
cells" of the hepatopancreas
; in isopods it can be found throughout
the hepatopancreas in the form of small granules which represent the metal in an
easily dissociable state that can be complexed with many chelating agents. As far as
can be told, there are small cells in the hepatopancreas of these species in which
copper is concentrated when it becomes plentiful. These "copper storing cells" grow
more prominent as one goes from subtidal to intertidal to terrestrial species. In L.
oceanica most of the copper occurs in small, conoid cells (the "Speicherzellen" or
"S-Zelten" o f FRENZ~L 1894), but one can nearly always observe small amounts of
"free" copper in the other cells of the hepatopancreas as well (Fig. 4a). The same
holds for Sphaeroma serratum in which, however, the hepatopancreas has become so
crowded with copper granules (Fig. 4b) that it is difficult to understand how this
organ is capable of performing any function beyond the storage of copper. These
distribution patterns are interpreted to indicate that in marine and intertidal species
copper, though sometimes stored in specialized cells, is allowed to move rather freely
from cell to cell. This again would suggest a high rate of loss via the hepatopancreatic
lumen or the body fluids. In terrestrial isopods, however, copper is nearly always
confined to the conoid S-cells which are squeezed in between the large, secretory
B-cells (in FRENZEL'Sterminology; Fig. 4c). Whenever copper is being mobilized, for
example during the moulting cycle (WIEs~R 1965c) or during periods of stress
(unpublished observation), a special kind of protein-rich compound (also containing
polysaccharids) is synthesized in the hepatopancreas cells, picking up the free copper
and rendering it undetectable by histochemical means, i. e. changing the metal's state
from "free" to tightly bound. At the end of such a cycle of activity the gluco-proteins
break down, liberating the copper which for a short time may turn up in most of the
cells of the hepatopancreas (Fig. 4f).
However, soon all the copper will be concentrated again in the storing cells. This
process of concentration is particularly striking during phases of holocrine secretion
in which many of the large B-cells have disintegrated, leaving behind large stretches
of the h e p a t i c tubule lined b y small, cuboid cells, j a m p a c k e d w i t h c o p p e r (Fig. 4d).
I have never o b s e r v e d free c o p p e r in the large B-cells unless a c c o m p a i n e d b y the
synthesis of special gluco-proteids, which at the p e a k of their d e v e l o p m e n t m a y fill
most of these cells to the bursting point (Fig. 4e). The whole story behind the synthesis
of this complex material in the isopod's hepatopancreas is far from clear, but there
can be no doubt that it has some functional significance in connection with copper.
Whatever else its role (e. g. in the synthesis of haemocyanin), by complexing the large
stores of easily dissociable copper in the hepatopancreas, it protects the rest of the
cells from this potentially toxic metal, as well as preventing the latter from being
dissipated during the periods of synthesis and secretions which involve the whole
organ. This recalls the remark of MANW~LL& BAIIER(1963) that one of the important
steps in the evolution of catalytic metalloproteids might have been the appearance
of proteins which chelated free metal ions. The catalytic function of these proteids
then developed as a sort of atterthought to their primary role as antitoxins.
Terrestrial isopods, by having manoeuvred themselves into a safety program of
stockpiling copper far beyond what is called for by necessity, perhaps had to reinvent
this old principle of chelation and transport of heavy metals by proteins in order to
guide their stockpiles safely through the maze of metabolic processes going on in the
same organ in which the metal has to be stored.
1. Copper is an element of great importance for crustaceans such as isopods and
amphipods. While their marine relatives can obtain all necessary chemical
components from the surrounding sea water via gills or other epithelia, the species
which have conquered terra firma face the problem of extracting practically all
vital substances from their food.
2. In marine forms, the water flow maintained via ciliary or muscular mechanisms is
sufficient to provide several orders of magnitude more copper than required; food
probably plays only a minor role in copper supply.
3. Terrestrial isopods have to rely entirely on their food as a source of copper. They
can do several things in order to ensure an adequate supply: increase food
consumption, improve the selective absorption of copper from the food material
passing through the gut (possibly in symbiosis with copper concentrating
microorganisms), increase copper stores, thus widening safety margins for times of low
supply, reduce copper losses by regulating the transport of this metal between the
stores and other body parts.
4. It was shown that terrestrial isopods consume about as much food as their marine
5. Extraction of copper from primary vegetable matter seems to be very difficult,
both for terrestrial forms like Porcellio scaber and for intertidal forms such as
Ligia oceanica or the amphipod Orchestia gammarella; extraction is possible only
at very high copper concentrations.
6. A way out of this calamitous situation seems to be in cooperation with
microorganisms which liberate copper from the tightly bound states in which it exists in
the primary plant material. This is true for P. scaber but it probably also holds for
O. gammerella, L. oceanica and other species feeding on decaying algae on the
7. The a m o u n t of copper stored in the h e p a t o p a n c r e a s increases w i t h increasing
dependence of the species on the terrestrial e n v i r o n m e n t , the values o b t a i n e d for
i n t e r t i d a l species being i n t e r m e d i a t e between m a r i n e a n d t r u l y terrestrial species.
8. P, scaber ( a n d p r o b a b l y Oniscus asellus) will extract up to 95 0/0 of the copper
present in artificially enriched leaf litter whereas i n t e r t i d a l forms feeding on Fucus
will n o t extract more t h a n 50 % , mostly o n l y 20 0/0 or less, f r o m artificially enriched
9. C o p p e r is m o r e strictly relegated to "storage cells" of the hepatopancreas in
terrestrial isopods t h a n it is in m a r i n e or i n t e r t i d a l ones. E x t e n s i v e m o v e m e n t s of
copper in P. scaber are a c c o m p a n i e d b y the synthesis of special "carrier proteins",
whereas in m a r i n e or i n t e r t i d a l species this metal seems to be able to move more
freely in a n easily dissociable state between the storage cells a n d other cells of the
L I T E R A T U R E C I T E D
Discussion f o l l o w i n g the paper by WI~SER
PANDIAN: I would like to bring to your attention an unpublished work of a student from
Madras University (India). He was interested in the estimation of ash content of the cuticle
of crustaceans. Generally, the aquatic crustaceans have white ash, but surprisingly, that of
Ligia sp. has blue. He concluded that copper contaminates the Ligia ash and that its cuticle
serves as copper storage. Such studies seem to show that copper may be mobililized and moved
to the cuticle, which then serves as an intermediary or permanent storage organ.
WIESER:This is an interesting observation and I would be grateful for a detailed reference to
your colleague's work.
PAFFrmt6rER: What kind of micro-organisms made the copper available for the crustaceans
WIESER: I don't know'.
HOtIENDORF:Fiir die funktionetle Abh~ingigkeit des Cu-Nutzkoeffizienten vom Kupferangebot
in der Nahrung yon Porcellio scaber zeigten Sie in einem doppelt-logarithmischen
Koordinatensystem eine Gerade. In Wahrheit ist die Beziehung zwis&en der Cu-Aufnahme und dem
Cu-Angebot jedoch keine lineare, sondern eine exponentielle. Dutch Transformation in ein
lineares System erhalten Sie fiir den funktionellen Zusammenhang eine Potenzfunktion, die
in einem gew6hntichen Koordinatensystem durch eine ParabeI h/Sheren Grades repr~isentiert
WIESER: Da die Beziehung zwischen Cu-Assimilation und Cu-Angebot im
doppelt-logarithmischen Koordinatensystem als eine lineare erscheint, mug ihre Form im gew6hnlichen, linearen
System natiirlich einer Exponentialfunktion entsprechen. Ich habe keine Erkl~irung fiir diese
Bezietmng (die aussagt, daft mit steigendem Kupferangebot die Kupferassimilation exponentiell
zunimmt), sondern nut die Vermutung, dag Kupfer in zwei Formen vorliegt: gebunden und
frei. Mit steigendem Kupfergehalt nimmt der Anteii des freien Kupfers in der Nahrung
auf~erordentlich schnell zu, da die Bindungsm/Sgli&keiten abges~ittigt werden. Da freies Kupfer sehr
viel leichter zu assimilieren ist als gebundenes, nimmt au& die Kupferassimilation in
Abh~ingigkeit yore Zuwachs an freiem Kupfer sehr schnell zu. Wie gesagt, dies ist nur eine Vermutung.
0. 2 . . . . . . . . . . . . . . . . . . . . . . . 0.1 1 .0 Coppitr cor/l¢rlt of food (gig/rag dry weight)
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