Cardiovascular control in Antarctic notothenioid fishes

Camp. Poochem. Physd. Vol. 118A, No. 4, pp. 1001-1008, Copyrighr 0 19Y7 Elsewer Sciencr Inc. All rights reserved.

1997

ISSN 0300-Y629/97/$17.00 1‘11SO300-962Y(97)00008~X

ELSEVIER

Cardiovascular Control in Antarctic Notothenioid Fishes William Davison ,* Michael Axelsson, f Stefan Nilsson, f and Malcolm

E. Forster”

*L)EPARTMENT OF Zoo~oc~, UNIVERSTY OF CANTERBURY,PRIVATEBAC;4800, CHRISTCHURCH, NEW ZEALAND;AND ~‘DEPARTMENT OF ZOOPHYSIOLOGY, UNIVERSITYOF G~TEBORG,MEDICINAREGATAN 18, S-413 90 G~TEROR(:, SWEDEN

ABSTRACT. more

The temperatures

viscous

at cold

of adaptations compared

to other

fishes,

(the

factor

increase

tonus

rather

haematocrit

cholinergically

The

that

phenomenon

may

has disposed

is remarkably

bernacchii-and activity

during

changes

periods

Thus,

are unusual

Antarctic

fish, cardiovascular

control,

in which

in common

polar regions, changes

with

the amount

dramatically

prevailing changing

in the

Antarctic the arctic

of solar radiation

as the seasons winter

months

amc>unt of daylight

tivity,

which

has direct

major

impacts

water

temperatures

effects

on the growth

blood through

This has

of polar fish (7). By contrast, water

in the observation

that

implicated

are more stenothermal

energetic

their cardiovascular

cost

t’t al. (20) found

that

of moving

systems

than

more viscous

( 19), and it seems reasonable

ble for most, if not all, of the specialized the blood systems of antarctic and arctic Graham

produc-

on the food chain.

(50,5 1). Blood becomes

potential

The

of ambient

at high latitudes

it is the

latitudes.

This constancy

species

at cold temperatures

with darkness

at high

due to

has been

that

change,

per day

and cold,

temperatures

species

received

stable

of ice cover.

living

In both

affects phytoplankton

are extremely

the presence

are temperate

fish live has physical environment.

to assume viscous

that is responsicharacteristics fish.

the blood

viscosity

of of a

Address r+rmt rcyursts to: S. Ndssw~. Department of ZooFhysdogy. Universlry dGiirelxq, Medlcinaregatan 18. S-413 90 Giitehorg, Sweden. Tel. +46-31-773-3669; Fax +46-31-773-3807; E-md: s.nilsson@oofys. gu.se dnJ ~.~~~l~s~111~1001.~u.sc. Recrivd 22 Aprd 1996; rc\weJ 29 A trgust 1996; acceptd 6 Sqxemher 1996.

large

for a number

changes

III haematocrit

viscosity

of thclr

diminish

cardiac

blood work.

performance

appear

autonomic

chiefly

of erythrocyres

nerves

control

of the autonomic m that

to 80% m the hottom-

to depend

iihres. Sequestering

both

release

control organs

heart, spleen, &.

of these

more‘ or less s~>lel) Scrence

char and a marine from

der, have

temperate in their

glycopeptides

channichthyids,

hemarocrit

sculpin

from arctic

than waters.

of fish species,

antifreeze

of antifreeze The

more

a number

Inc.

innervatic)n,

was lower and less shear-dependent poles,

blood

(12),

increases

theniid

fish (57). The

Notothenia formable rainbow

coriice~s

do not

trout (34). Even among

iids, there are species some

than

hern~~chii, a noto-

to be any

capacity

fish

more

de-

are the erythrocytes

of

the red-blooded

notothen-

with very low red cell counts

with a remarkable

( 13).

dispensed

cells c)f the Antarctic

appear

at low temperatures

viscosity

has been correlated

in Trematomus

red blood

flnun-

and the presence

effectively

with red blood cells, and their presence

at both

the winter

blood

have

latitudes

that of the winter However,

including

or icefish,

with high blood viscosity

is Cl

cells to

of the heart and spleen

appear

autonomic

on modulation hy the spleen

1997. 0 1997 Elsevier

flounder

at I~w Indeed.

altogether. conditions-up

freshwater

The environment

Blood hecomes

high

“resting”

fishes

stable.

is responsible

and thus

of erythrocytes under

COMPBIOCHEM PHYSIOL 118A;4:1001-1008,

controlled.

show

to the

the viscosity,

the studies

among

INTRODUCTION

features

he related

and cholinergic

of demand.

these

of viscosity

Nototheniids

(adrenergic)

of haematocrit, that

high

in cardiac

in excttatory

this increase

Antarctic

Channichthydae)

fish show

KEY WORDS.

this

are not only low. hut also relatively

will reduce

in the reduction

of the Antarctic

system.

on the heart

than

oceans

it is assumed

of the haematocrit

“icefish,”

Trematomus

of this tonus, major

and

Reduction

The cholinergic dwelling

and

of the cardiovascular

temperatures. one group

in the polar

temperatures

to sequester

(35) and

a significant

proportion of their total red cell population within their spleens. One species, Pagothenia borchgreelinki, shows the most

dramatic

changes

in circulating

red cell numbers

re-

corded for any fish (18,49), and these adjustments presumably allow the tish to optimize oxygen transport with respect to energy demands made on the heart (59). The icetish have remarkably high cardiac outputs compared with other teleosts and possess other adaptations to allow them to survive in their permanently anemic conditic>n. The solubility of oxygen in sea water is very high at cold temperatures, and this offsets the burden

of the reduced

c)xygen capacitance

of

W. Davison et al.

1002

their blood. The high oxygen

concentrations

of polar waters

probably allows the lower hematocrits measured in fish from these latitudes, which in turn leads to lower viscosities (56). Only

in the Antarctic

erythrocytes, teristic

do we see fish species

and we might ask whether

peculiar

ences between able about

to that

there

environment

fish species

that

that

explains

the Antarctic

fish fauna

number

of endemic

species,

current

explanation

is that

relatively

Total vascular resistance (Pa min kg ml-‘)

Species

differ-

35 159

Chenocephlus aceraus Pagdtenia borchpevinki Trematomus bemmshii

197

is remark-

is the unusually

in contrast

vascular resistances in Antarctic fish

lack

is any charac-

at the two poles. What

TABLE 1. Total

high

to arctic

seas. The

few species

survived

Data from (I), with estimate for icefish taken from (23).

on the polar side of the Antarctic convergence when that formed after the final breakup of Gondwana around 30 mil-

features

in common

lion years ago and that the convergence

generate

a correspondingly

mal barrier sphere,

to movements

large land masses promote

with warmer

water

traveling

of water temperature absence of a sudden found

north

latitudinal 95 species

northern

and a general

extremities

of fish regarded

as “AntarcHowever,

fish are found

and

the

region

dominant

only

where

groups

than specifically being

found

Some,

cold-water

are generally

such

as the hagfish have

notothenioids

Southern species

Ocean

as the

in the High

rarely rise above

is the fact that demic

(13). Among

Channichythidae, the time the

All other

are endemic. convergence

where

water

and tem-

Nototheniidae

families,

Kock

including

(32)

noted

transition

advanced

3-7

By contrast,

(5-6 degrees.

and the presence

of the antifreeze

sculpins

a species

whose

but only at resistance systems

and

this one about

of

group.

cardiovas-

on studies

also applies

of so few

to teleost

tish in Arctic

pleuronectid

fish in

waters

are

flattishes.

in cold temperate

Al-

control

mechanisms

in some detail at Giiteborg much of the Arctic

to that polar region,

A

have

and elsewhere.

fish fauna is not endemic

it is unlikely

nisms have evolved

waters.

is the cod (Gadus morhua),

cardiovascular

been investigated

that novel control

mecha-

in the cold waters of the northern

hemi-

sphere.

CHARACTERISTICS SYSTEMS

(cf.

Resting

the

mobilized,

that

at

mybp), “This

range

gene in Notothenia

angustata from New Zealand waters (DeVries, personal communication), suggests that many of the current subantarctic nototheniids originated in the Antarctic. The Antarctic notothenioids themselves are recent additions to the fauna, appearing after the development of the Antarctic convergence and radiating rapidly into unoccupied ecological niches.

OF THE

BLOOD

OF NOTOTHENIOID

FISHES

values for the total vascular non-scombrid

teleost

from ca. 200 to 450 Pa

tances

1). Branchial

min

vascular

calculated

kg

ml-’

of non-imwaters

(6). Resis-

and T. (Pagothenia) resistance

to be approximately

(Z), which

of the range (6). These as both an adaptation

resistances

fish from temperate

are lower in P. borchgrevinki

nacchii (Table

resistance

This,

fish based

is also found

has been

migration

upon

in generalizing

of such an animal

systemic

the northward

can

though species such as the arctic cod (Boreogadus saida) can he regarded as strictly cold-water animals, most of the Arc-

grevinki

allowed

of the blood

the most abundant

cods,

of the cold

have

dangers

this caution

water fauna and may explain the presence of notothenioids on the Patagonian and on the southern New Zealand shelf.”

would

peculiarities

has

that

interest 95 are enmembers

of the Miocene-Pliocene

Antarctic

of

as the most primitive

15 are in the family

nototheniids).

biomass

species,

of the group,

and

several

the non-endemic

regarded

(39).

Thus, because

of the

of notothenioids,

10 are bovichtids, 34 endemic

and

0°C (15). Of particular

of 120 species

to Antarctica

to the north.

both in biomass

Antarctic,

general

tic ichthyofauna

waters,

large stroke volume,

in Antarctic

although

good example

glutinosa)

most

control

species,

gadid

nototheniids

such as a heart

of investigations

are obvious

The non-nototheni-

a very wide distribution. constitute

concentration

the

icefish,

fish fauna possibly reflect the radiation of the from a common ancestor and possibly also

to Antarctic waters

(Myxine

fish and are dominant

numbers

peratures

endemic

also in the sub-Antarctic

chondrychthians, The

specialists.

not

the

temper-

Myctophidae (35 species), Liparididae (31 species) and Zoarcidae (22 species) can be regarded as deep-water rather oid fishes

of the red-blooded with

They also share a very low vascular

the Antarctic notothenioids

cular

in the

such

system

low pressures.

There

of the Antarctic

are warmer

blood

(1). So the perceived

lowering

are notothenioids.

of the non-notothenioid

atures

formation,

range.

are at least 274 species

tic” (13). Of these, many

gyral current

hemi-

with increase in latitude. Thus, in the temperature change, northern fish are

over a wider

There

now acts as a ther-

of fish. In the northern

The

ber-

of P. borch25% of

is also a value at the low end

low vascular resistances can be seen to the potentially high viscosity of

blood at low temperatures the high cardiac outputs.

and a necessary consequence of Various factors can modulate

pressures and the patterns of blood flow in teleost fish (39). Autonomic nerves and endocrine glands exert effects on cardiac muscle and on the smooth muscles of the cardiovascular system. A small number factors in Antarctic fish.

of studies have looked at these

Cardiovascular

Control

in Antarctic

CONTROL

OF THE

1003

Fishes

HEART

The gross morphology of the heart in the notothenioids is not different from other studied teleosts, with four chambers arranged

in series: sinus venosus,

bus arteriosus. pressed

The

heart

as percentage

most teleosts, Among

atrium,

index

including

the teleosts,

those cardiac

indices

values found for small mammals.

(Cyclostomata),

ied have

a cholinergic

inhibitory

most

teleosts

in the cardiac

branch

fibers

cholinergic

cardiac

found renergic

ing catecholnmines

systems

varies

control

in Antarctic

influence

(6,14).

of circulating

catethat

to the concentrations

via adrenegic

of circulating

in T. bernacchii

by Davison

that heart

rate increased

indicating

a low reliance

control

but to what

nerves

known

inter-

during

of about

in the

greuinki, the cholinergic (i.e., the heart cholinergic around

tone

rather teleosts

is smaller

beats/min

(54%)

species.

rate after a combined

a cholin-

which

in both

but still high

Intrinsic blockade

influence

ture compensation.

species

heart

rate

of both

the

on the heart)

P. borchgrevinki

indicating

is the

P. borch-

(Fig. 1) ( 1). This is in line with the intrinsic

rates of many temperate rate

recorded,

fish ( 1). In the cryopelagic

and the adrenergic

22-24

bernacchii

fish spe-

In T. bemucchii,

80% has been

for any teleost with

adaptation

in Antarctic

in support

and

is T.

heart

a strong tempera-

It is clear that the much lower “resting”

is a function

processes

and

of metabolic

fish. We do not know

to most

rather

reliance than

other

teleosts,

there

in the notheniids

force

cold

the reasons

also seems

on changes

to alter cardiac

output

to be a

in frequency

( 1).

FACTORS MODIFYING GILL VASCULAR RESISTANCE In fish, the gills and the systemic

to be well developed.

compared

evidence

stress

mechanisms

of the heart in Antarctic

ergic highest

the rates of biological

is further

contrast

stress

handling

depress

the finding

(8), it was shown

on adrenergic

control

Atropine + Sotalol

FIG. 1, Heart rate in I? borchgrevinki and T. hemacchii before and after intravascular injection of atropine and sotalol. Control heart rate was recorded 24 hr postsurgically and the values for atropine and the subsequent sotalol injection was taken 30 min after each treatment. Data from (1).

greater

but only by a few beats per minute,

cies seems tone

Atropine

why the parasympathetic system should he more influential than the sympathetic in the two nototheniids studied. In

and the Antin the plasma

catecholamines and coworkers

or circulat-

(2). One

of acute

Control

tures generally

a small ad-

of the heart.

The cholinergic

heart

is

fish have shown

has been described,

In the study of the effects

species. species

more species.

esting difference hetween temperate teleosts arctic species is the apparent lack of increase concentrations

of the

between

including

is not presently

in-

can also contain

tonic

(8). In P. borchgrevinki,

tone on the heart

stud-

fibers running

relative

of Antarctic

this tone is mediated

of the

excitatory

nerve

are low and similar teleosts

and

of the heart,

an adrenergic

of the concentration

levels

in other

innervation

are needed,

in the plasma

the basal

extent

The

and more studies

Measurements

(54).

all fish species

of the vagus, which

(36).

about

cholamincs

waters

the exception

the cholinergic

and adrenergic

Information scant,

also have

of the heart,

adrenergic

ex-

that are close to the

With

and lampreys

n

to that of

only the icefish (Channichthydae)

hagfishes

nervation

weight

from temperate

T bernacchii P borchgrevinkr

and bul-

(i.e., the heart

of body mass) is also similar

the tuna show extreme

and

ventricle

0 m

25

of a large cholinergic

tone

and a

series. where

circulation

are coupled

The heart pumps deoxygenated blood it is oxygenated before being distributed

in

to the gills to the vari-

ous parts of the body. The gill circulation in itself is complex with an arterio-arterial path and an arterio-venous, or nutritive, pathway resistances tance,

and with a complex

(38,61).

especially

post-branchial perfusion teresting

regulation

in the arterio-arterial pressure,

of the vascular

in the branchial

which

vascular

pathway,

is the driving

resis-

affect

pressure

the

for the

of the entire systemic circulation. One of the inquestions is whether the optimization gill vascu-

of

lar resistance is possible

Changes

in relation

without

to gas transfer

compromising

and osmotic

the systemic

balance

driving

pres-

much smaller adrenergic influence (Fig. 1). These findings have supported suggestions that cholinergic control is rela-

sure. In the Atlantic cod (G. morhua) and the rainbow trcout (Oncorhynchus mykiss), there is a reduction in the branchial

tively more significant than adrenergic control cold waters (see also section on spleen control). ance on the brake rather than the accelerator

vascular resistance at moderate swimming speeds (2,30). In contrast, in a study of P. borchgrevinki fitted with a ventral aortic flow probe, and with pre- and postbranchial arteries

heart

rate might

not be expected,

given

in fish of This relito control

that cold tempera-

cannulated

to allow calculations

of systemic

and branchial

1004

W. Davison

resistance,

branchial

exercised treatment

in a swimming tunnel (Fig. 2) (2). After prewith atropine, a muscarinic receptor antagonist,

vascular

resistance

rose when

fish were

the increase in gill vascular resistance during exercise was abolished, indicating a cholinergic vasoconstrictor mechanism.

The

branchial

Padrenoceptor

antagonist

vasoconstrictor

lost in atropinised

response

hsh, indicating

ated vasodilation

sotalol

restored

to exercise

a /3-adrenoceptor

sodilatory

tonus was dominant tonus

Rankin

(48) found

vascular

resistance,

gill, but whether

both

that

gill arches

and branchial

arteries

aadrenergic

tion in the gill, particularly Davison,

A.H. Forster

vations).

In these

branchial

able. However, indicate strictor there

our recent

that 5hydroxytyptamine than is adrenaline is a profound

effect

vasodila-

circulation

(W.

unpublished

the adrenergic studies

of CY-

of isolated,

of P. borchgrevinki

in the afferent

of notothenioid

obser-

responses

of the

fishes are unremark-

on gill blood

vessels

is a more potent

in the presence

vasocon-

of sotalol.

on the branchial

Q

also

vascular

resis-

of intravascular

-

O=P,

oxygenation of blood

at the gill, presumably and perhaps

M.E. Forster

sults). Adrenaline dorsal and ventral

. = R,,,,

tryptamine)

P ifi

0 =

gen tension.

Blocking

pine caused

a decrease

e K 2

min

FIG. 2. Blood pressure and vascular resistances during a brief period of exercise in I? borchgrevinki. Note that, as in other teleosts studied, the ventral aortic blood pressure (PVA) increases but there is at the same time a fall in the dorsal aortic blood pressure (PDA). This is a result of the increase in branchial resistance (I&,,). The systemic vascular resistance (I&) decreases.

oxygen

exercise

(Fig. 3).

by altering

permeability

and S. Nilsson,

the patterns (M. Axelsson,

unpublished

re-

injections caused a slight increase in both aortic PO?, whereas serotonin (5hytroxy-

-aI‘

blood

of 5hydroxytyptamine,

seen during

with an extra-corporeal blood loop have that administration of drugs can alter blood

perfusion

W. Davison,

s

injections

the response

Experiments demonstrated = P,

min

FIG. 3. Effects of intra-arterially injected 5.hydroxytrypta. mine on the ventral ( PVA)and dorsal (Z&) aortic blood pressure in l? borchgretiki. Note the similarities with the pressure development seen during exercise (Fig. 2).

tance

0

2

5-HT

In uko,

mimicking

01

aorta

perfused

mediating

and M.E. Forster,

respects,

vasculature

studies

receptors

61 Dorsal

decreased

was due to stimulation Recent

0'

va-

Chaenocephalus

noradrenaline

is not known.

l-

was also that the

in e~ivo and in an isolated

this response

or /%adrenoceptors have confirmed

pi:!

medi-

over the fladrenergic

in the gill. In the icefish,

ucerutus,

perfused

6 1 Ventral aorta

(2).

An a-adrenergic vasoconstrictory component found in these experiments and it was concluded a-adrenergic

the

that had been

et al.

produced

tension.

a massive

fall in the dorsal aortic oxy-

the muscarinic in both Nothing

receptors

the ventral is known

using atro-

and dorsal aortic about

the exact

mechanism behind these changes or the localization of the receptors mediating these responses. This ambiguity should not be a surprise, given the number of factors in whole animals, such as stroke volume, heart rate and blood pressure, that may affect lamellar recruitment

and which

in turn may affect gas exchange

across the

gill surfaces. Our work also demonstrated an inverse correlation between dorsal aortic blood PO: and the pressure drop across the gills, suggesting that a reduction in branchial vascular resistance would favor oxygen exchange. In the exercising animals, the hranchial resistance increased hy ap-

1005

Cardiovascular G>ntml in Antarctic Fishes

proximately

30% that, according to the inverse relationship

(Fig. 2). Thus, control

animals,

atropine-treated

atropine-plus-sotalol-treated

crease in branchial

animals all showed large falls in systemic resistance.

consistent

resistance

characteristic,

during exercise

but on exercise

is a highly

the dorsal aortic

animals

animals,

found, should lead to a reduced dorsal aortic PO: The in-

and prazosin-treated This

suggests that yet other possibly local modulators exist.

PO! fell in some fish and rose in others, indicating a complex control

of oxygen uptake. It is possible that fish that are

spontaneously

active will not show such a rise. As noted

above, stressful stimuli did not elicit a rise in plasma catecholamine

titers (8,14).

However,

handing

stress did ele-

vate heart rate and ventral aortic blood pressure in T. bernacchii (8). 0ur importance

findings, therefore,

of sympathetic

point to the potential

nerves in controlling

systemic perfusion in nototheniids. investigated,

including non-notothenioids,

whether this phenomenon

branchial/

More species need to be before we know

applies only to Antarctic

noto-

theniids or generally to polar fishes.

PERIPHERAL Control

VASCULAR

of the peripheral

largely unknown.

RESISTANCE

vasculature Control

in antarctic

fish is

of systemic resistance

water, fish catecholamines

soconstriction

is

cause systemic va-

and hence an increase in dorsal aortic blood

pressure (?,48).

The splenic artery appears to be controlled

mainly by catecholamines

(41). After injection

of adrena-

line, there was a large increase in cardiac output in Pagothenia borchgrrvinki,

but the increase in systemic resistance

was small and transitory

(2).

In the same study, prazosin

produced n marked fall in systemic resistance, a-adrenergic

indicating an

tonus. Viewed in concert with the observation

that circulating

catecholamines

may not be important

in

these animals (8,14), the systemic vascular adrenergic tone could be controlled by sympathetic nerves rather than blood-borne

catecholamines.

the innervation

However, so far no studies on

pattern of the systemic vasculature exist.

The renin-angiotensin totheniids

system is present in antarctic

with both angiotensin

no-

1 and II having marked

effects on blood pressure and systemic resistance (2). In our study, angiotensin recent

did not affect branchial

wc)rk (Pavison,

Forster

resistance,

and Forster,

and

unpublished

data) has shown little, if any, response of isolated branchial blood vessel\. Angiotensin fect downstream Cholinergic

the major site of oxygen

a5

uptake in fish. This is undoubtedly

true for Antarctic

fish,

although cutaneous uptake makes a significant contribution in some species (23). Kunzmann (3 3) measured gill dimensions of two red-blooded

nototheniids

mation available on many Antarctic

and reviewed inforfishes. He concluded

that gill total areas are small, and gill-blood water distances

ate-water fishes hecause of the high stahle oxygen content

complex and under the influence of several modulators. As in temperate

The gills are generally regarded

are large, in all Antarctic fish. However, he emphasized that these cannot be directly compared with values from temper-

Peripheral resistances are low, and blood

flows are high (2,22,48).

CUTANEOUS BLOOD FLOW AND OXYGEN UPTAKE

thus seems to have its major ef-

to the gills.

nerves have been implicated

as major con-

of the cold Antarctic water. The :oarcid L~codichthys (Rhigophila) dearborni obtains 32% of its oxygen via the skin at rest (55),

a figure that suggests the skin is being used as a

respiratory organ rather than representing respiration by the epidermis

(45).

capillarization

Jakuhowski

(28)

of the skin of

estimated

that the total

Chamocr~h&s

acerutus

was

equal to that of the gills, implying a major role for the skin in oxygen uptake in icefish. Hemmingsen

and Douglas (2 1)

recorded cutaneous uptake in icetish at hctwcen 30 and 40% of total

oxygen

uptake.

The

red-blooded

bathydraconid

Gymnodraco acuticrps has a small gill surface area and wellcapillarized skin (29). Th ese 1 d’imensions and measurements suggest that icehsh in particular

may possess mechanisms

for the control of skin blood flow. We suggest it is unlikely that similar mechanisms well developed in the red-blooded nototheniids.

will be

Wells (55)

estimated that skin oxygen uptake was 12- 16% of the total in P. horchgrellinki and T. hernucchii, but Davison et al. (10) measured only 5% uptake hy the skin in P. borchgrrvinki and a similar value has been recorded for T. hernucchii (L)avison, unpublished data). In addition, the amount of oxygen taken up hy the skin in these f&h was unaffected

by hypoxia or

disruption of the gill vasculature by till disease (10). This suggests that in red-blooded

nototheniid

fish, the oxygen

taken up by the skin is used for respiratic)n in the epidermis and dermis and is not used as a 5~1pplyfor the rest of the body.

trollers ot the heart and gills, and they also have a role in control of the systemic circulation.

Injection

of the antago-

nist atropinc produced a marked decrease in systemic resistance (without affecting gill resistance) despite a large increase in blc~c)d tlc>w caused by an increase in heart rate. This indicates a distinct cholinergic

tonic control.

CONTROL

OF THE SPLEEN

The spleen of teleost tish is a discrete organ, with its own vascular and nervous supply. Splenic functions include im-

Of interest in the Axelsson et al. (2) study was the obser-

mune responses and the formation of blood cells, erythrocyte degradation and the sequestering, storage and release

vation that swimming caused a 50% decrease in systemic vascular resistance, irrespective of any prior drug treatment

of erythrocytes (16,47). The autonomic innervation of the teleost controls the sequestering and release of erythrocytes,

W. Davison et al.

1006

a mechanism

common

37,40,42-44). Erythrocytes

in many vertebrate

may be released into the bloodstream

leost fish during elevated sympathetic during hypoxia or exercise).

groups (16,

201

1

T

I

of te-

nervous activity (e.g.,

This increases the hematocrit

and thus the oxygen-carrying capacity of the blood. In salmonids, the spleen has been shown to be responsible for a rise in the levels of red blood cells during exercise or hypoxia (46,47,52,59).

In the rainbow trout, Pearson and Ste-

vens (46) demonstrated

a release of red cells from the spleen

during stress corresponding

to about one-third

served hematocrit

The release was shown to be

increase.

due to an a-adrenoceptor-mediated and cholinergic

components

increase in hematocrit Seriola quinqueradiata,

of the ob-

control

were absent

was demonstrated

mechanism,

(47).

A similar

in the yellowtail

and this increase was believed to de-

pend to about 40% on splenic release of erythrocytes However,

the importance

(62).

firmation (58). It has been suggested that adrenaline has a major role in controlling

the spleen of fish from temperate waters, either

through adrenergic nerves (40) or via circulating amines

(31).

Various

0 Control

of the effect needs further con-

catechol-

forms of stress would elevate

plasma levels of catecholamines

the

in these fish, and these

4. Atropine-induced changes in hematocrit (Hct) and spleno-somatic index (SSI) [= 100 X (spleen weight/body weight)] in PagotheniaborchgrevinkiHct and SSI were determined in cannulated fish 3 hr after intravascular injection of saline (Control) or atropine (Atropine, 1.0 mglkg). Both the Hct and SSI changes are statistically significant from control values. Data from (4 1). FIG.

same stressors (e.g., hypoxia or exhaustive exercise) produce splenic

contraction

and erythrocyte

fish, stress causes splenic plasma levels of circulating (8,I4). There is an inhibitory

cholinergic

control in mammals. In the Atlantic tylcholine

release.

In antarctic

contraction (11,18), but the catecholamines are unaffected

produces contraction

component

in splenic

cod (G. morhua), ace-

of the splenic smooth mus-

cle similar to the effect of catecholamines.

In the cod, the

linergic component

in the innervation

inki spleen. Further evidence of cholinergic

of the I’. borchgreu-

innervation

of the spleen

of both the cod (24,25) and P. borchgrevinki (41) comes from the results with the acetylcholinesterase inhibitor BW 284 c5 1. This drug affects the specific (acetyl-) ase of the cholinergic

neurons (26,27).

cholinester-

Treatment

284 c5 1 increases the sensitivity to acetylcholine

with BW in experi-

nerve supply to the spleen runs from the coeliac ganglion

ments with isolated spleen strips from these fish, demon-

in a distinct branch of the anterior splanchnic

strating the presence of acetylcholinesterase

trical stimulation

nerve. Elec-

of the nerve produced expulsion of eryth-

rocytes in a perfused spleen. The involved in this mechanism

autonomic

nerve fibers

included both adrenergic

and

very likely a cholinergic into account hematocrit

innervation

the large effects of injected

and spleno-somatic

and therefore

of the spleen. Taking atropine

of the

index and the fact that atro-

cholinergic components (42,60). A series of studies have added to the knowledge about the nature of the splenic in-

pine inhibits all or most of the response to nerve stimulation

nervation

vous control

in teleosts,

including histochemical

demonstra-

tion of adrenergic fibres (17,24,25,42,43). The spleen of I’. borchgrevinki is an important

reservoir

in P. borchgreuinki, it would appear that the autonomic

ner-

of the spleen in this species is mainly, if not

solely, cholinergic

in nature (41).

of red blood cells that can be released into the blood during increased oxygen demand (9,18). In the study by Nilsson et al. (41), it was found that intra-peritoneal atropine injection produced a marked increase in spleno-somatic index (from 0.60 to 0.89) and that atropine treatment also generated a substantial decrease of the hematocrit (Fig. 4). The results suggest that loss of a functional cholinergic innervation of the spleen causes splenodilation and sequestering of erythrocytes. In addition, it was shown that electrical stimulation of the nervous supply to the perfused P. borchgrevinki spleen caused large effects on the perfusion flow and that these effects could be blocked by atropine (Fig. 5). This effect of atropine is compatible

with the view of major cho-

CONCLUSIONS We must acknowledge that our understanding

of cardiovas-

cular control in antarctic fishes is patchy and based on studies of only some organ systems in a handful of species. For example, nothing is known about the blood supply to the gastrointestinal tract in polar fishes. This is a significant outflow in all vertebrates and one that can be severely reduced at times of activity (3,4,53). Nototheniid fishes under laboratory conditions show remarkably large changes in hematocrit, which can be related to the high viscosity of their blood at temperatures below 0°C. We know that the heart and

Cardiovascular

.c E

Control

in Antarctic

1007

Fishes

30

t Q g g E

20

2 E 2

010

_OI_

\e

r1

‘L

1’

-

‘~/-+-j?+-

t Atr lO“jM

I

I 5 min

FIG. 5. Recording of outflow (drops per min) from an &I situ perfused spleen of Pagothenia borchgrevinki. Markers indicate electrical stimulation of the splenic nerve supply to the spleen with 20vsec trains of pulses at 10 Hz, 2-msec pulse duration at 6 V. The marked resuonse to electrical stimulation of the nerve supply is abolished by addition of atropine (10 ’ M) to the perfusion fluid. ReprodLced with permission from (41).

spleen

are unusual

in that both organs are more or less solely

cholinergically

controlled

nothing

about the innervation

known

tors in the heart, cent evidence important

branchial

suggests

modulators

this mechanism

(2,41),

needs

but

and systemic

of branchial

is virtually

of and types of recep-

that serotonergic further

there

vasculature. neurones

vascular

10.

Re-

could be

resistance,

but

11.

elucidation. 12.

Our otun rwcach on Antarctic fish has been generously supported by the Neu, Zealand Antarctic Research Progrumme (NZAP) , the Universitv oj Canterburr Research Grams Committee, the Swedish Natural Science Research Council (NFR) and the Forestry and Agriculture Research Council (S.IFR)

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