Upload
d-j
View
215
Download
0
Embed Size (px)
Citation preview
Differences between North Arnerican and EuropeanPopulations of Balanus balanoides Revealed t y
Transplantationl
Bv D. J . Cnrse
[]n,ivers'ity College oJ lVorth WalesMar'ine Sc,ience Laboratories, Menai Br,id,ge, Anglesey, Wales
ABSTRACT
Transplants of specimens of Balanus balanoicles from North \Vales to Newfoundland,Canada, confirmed two innate differences between European and North American forms ofthe species. Breecling took place later in transplanted European populations. The eggs of theEuropean form, though maturing later and therefore at a slightly lower temperature than theNorth American form, were distinctly smaller.
The time of breeding both in the North American arrd European forms was earlier at higherlatitudes, at higher shore levels, and in shelter.
INTRODUCTION
TnB enBBnING sEASoN of several population of t l-re circumboreal Arctic speciesBalanus balanoides from different localit ies betrveen latitudes 40o and 45oNon the North American side of the Atlantic has been given by Barnes (1958)and may be cornpared with that of populations of the same species from awider latitudinal range on the coast of Europe, extending from NorthernNorway to southwest England (Crisp, 1959a). if the populations studiedcan be regarded as representative of those throughout the European andNorth American sides of the Atlantic Ocean, there appear to be minor, butsignificant, differences in reproductive physiology in these morphologicallyindistinguishable races. The North American race not only breeds earlier atcorresponding latitudes, but its embryos develop more rapidly at the sametemperature, and its eggs are significantly larger. The differences l 'vere retainedat least for a year after transplantation from North America to Europe, andwere therefore thought l ikely to be innate (Crisp, 196+).
Further observations have nor,v been made on breeding in this speciesover a rvider latitudinal range on the North American coast, and an exper-imental population rvas transferred in the reverse direction, from Britain toNewfoundland, to compare the reproductive cycle of the t$'o races underidentical climatic conditions.
METHODS
Specimens oI B. balanoides attached to mussel shells were sent by airto St. John's, Newfoundland, and transplanted, using quick-setting cement,
lReceived for publication March 13, 1968.
2633J. Frsn. RBs. Bo. CaNro.t, 25(12):2633-2641, 1968.Printed in Canada.
J. F
ish.
Res
. Bd.
Can
. Dow
nloa
ded
from
ww
w.n
rcre
sear
chpr
ess.
com
by
CO
NC
OR
DIA
UN
IV o
n 11
/12/
14Fo
r pe
rson
al u
se o
nly.
2634 JoURNAL FTSHERTES RESEARCH BoARD oF cANADA, vor- .2s, No. 12, 1968
to a position in the normal Balanus zone near, or slightly above, mean tidelevel. A semi-sheltered shore, Horse Cove in Conception Bay, was chosenfor this experiment. Transplantation was completed betrveen August 11 and18, 1962, rvell in advance of the breeding season.
Samples were removed weekly for examination of the reproductive stateduring the period of ferti l isation and oviposition, and thereafter at longerintervals. The percentage carrying ferti l ised egg masses, the stage of em-bryonic development of the eggs, the dimensions of the eggs, and the con-dition of the male reproductive system were noted in each sample.
Corresponding observations were made on samples ol B. balano'idesnative to Newfoundland growing in the same environment as the transplants,and on samples native to Wales grorving at the site from which the transplantshad been collected. Two samples were obtained from Woods Hole, Mass.,during October t962 and rn'ere examined for further comparison; other pop-ulations rvere examined in the field in Nova Scotia during the breeding season.To conform with the Canadian Government's legislation on the introductionof living exotic fish, the transplantation experiment was terminated andall imported barnacles removed on February 10, 1963 before any l iberationof naupli i had taken place.
The samples collected in Nova Scotia 'r 'vere studied to determine theinfluence of such environmental factors as tidal level, u.ave exposure, and theage of the individual on the time of ferti l isation. The median date of fer-ti l isation of samples taken from different environments tras obtained by back-dating early embryo stages present in the mantle cavity (Crisp, 1959b).
RESULTS OF TRANSPLANT EXPERIMENTS
TnB BnnBornc Cycr,B
Figure 1 i l lustrates the progress of ferti l isation and embryonic develop-ment in the native Ner'r 'foundland population, the transplanted populationfrom North Wales, and the original population remaining in North Wales.The median date of ferti l isation of the North Wales population, rvhether inNorth Wales (53"13'N lat) or in Conception Bay, Newfoundland (47'34'N
lat), lay between November 10 and 13, 1962, and u,as evidently influencedvery l itt le by transplantation. The median date of ferti l isation of the New-foundland population was much earlier, on about October 4, 1962. A few hadbeen ferti l ised by late September and all were ferti l ised by the middle ofOctober. By comparison, the median date of ferti l isation of B. balano'idesgrowing at mean tide level at Woods Hole, Mass. (41"32'N lat) was on ap-proximately October 22, t962. The median date at various locations in NovaScotia varied from October 9 to 20, 1962, according to tidal level and exposure(Table I), and thus was intermediate in time between Newfoundland andWoods Hole, though the two samples from Cape Breton Island, N.S., rn'ereexceptionally late in relation to their high latitude, due perhaps to exposureto higher sea temperatures caused by local outflow of warm water from theGulf of St. Lawrence during late summer or fall. It is known from studies of
J. F
ish.
Res
. Bd.
Can
. Dow
nloa
ded
from
ww
w.n
rcre
sear
chpr
ess.
com
by
CO
NC
OR
DIA
UN
IV o
n 11
/12/
14Fo
r pe
rson
al u
se o
nly.
CRISP: NA & EUROPEAN BALANUS BALANOIDES , ,6?<
Frc. 1. Breedine and embrvonic develooment of Balanus bal-anoides native to\orth Walei and to Newioundland. The progressof fertilisation is shown by open circles (stage 1). Full circles andsquares represent embryonic development to the stage of earlylimb bud rudiments (stage 7), and eyed nauplii (stage l2') re-spectively. P.L. : period over which penis is shed. Upper: NorthWales population in Menai Bridge (solid lines) and after trans-plantation to Newfoundland (broken lines and crossed symbols).Lower: breeding behaviour of population indigenous to New-foundland. Ord.'ituate: percentage of population having reached the
reproductive stage indicated. Abscissa: date of observation.
this species in Europe that the date of breeding is influenced by environmentalfactors operating at this time (Crisp and Clegg, 1960) and rnay be delayedby higher temperatures (Crisp, t957, 1959a).
Teet-e I. Latitudinal variation in n-redian date of fertilisation of. Bal,anus balanoid.es in October1962 .
Place N lat Tidal levelMedian date of
fertilisation(Oct. 1962)
lo(
o
_n,,e,_.a '
/. P L
).-
o c r N O V D E C J A N - I - L t s
f,u.
-r
a '/-
l' l' 'Pl
/
a
/
Woods Hole, Mass., USAYarmouth, N.S.I-unenburg, N.S.Peggy's Cove, N.S.Herring Cove, N.S.Smith's Beach, N.S.Purcell's Cove, N.S.Parker's Cove, N.S.
Liscomb, N.S.Margaretsville, N.S.Port Hood, Cape Breton Is., N.S.Neil's Harbour, Cape Breton Is., N.S.Horse Cove, Conception Bay, Nfld.
41"32'43"49',44020144"30',44032',44"34'44"3s',44050',
45"02'.45"02',46007'46"46'+7"34',
M.T.L.-H.W.N."M.T.i..-H.W.N.H.W.M.T.L.M.T.L.H.W.t{.T.L.H.W.L.W.H.W.M.T.L.-H.W.N.H.W.H.W.\,I.T.t..-H.W.N.
22I J
t 220I J
10t9I J
209
t2I +
1.54
"M.T.L. : mean tidal level; H.W.N'. : high water neap; H.W. : high water; L.W. :low water.
J. F
ish.
Res
. Bd.
Can
. Dow
nloa
ded
from
ww
w.n
rcre
sear
chpr
ess.
com
by
CO
NC
OR
DIA
UN
IV o
n 11
/12/
14Fo
r pe
rson
al u
se o
nly.
2636 JOURNAL FTSHERTES RESEARCH BOARD oF CANADA, voL.2s, No. 12, 1s68
From sea temperatures published by Fuglister G9a7) and correspondingair temperatures (United States Navy Department, 1955) there is in Augusta reduction of sea temperature betrveen Cap Cod and southeast Nova Scotiaf rom about 20 to about 16 C, and in November f rom about 10 to about 7 C;similarly the sea temperatures in southeast Ner'vfoundland are approximately3 degrees C lorver. Air temperatures fluctuate more widely and fall moresharply with the approaching lvinter, but shorv the same latitudinal trend.
Thus, despite minor local anomalies, earlier breeding of more northerlypopulations rvithin the latitudinal range covered is a characteristic of NorthAmerican populations just as it is of European ones. But the North Americanpopulations, when cornpared with European populations at similar latitudes,breed at least a month earlier.
Figure 1 also shows the progress of development. The Nervfoundlandpopulation, having ferti l ised a rnonth earlier, maintained their lead in de-velopment throughout the winter. The transplanted specimens developedonly slightly more slowly in Ner,vfoundland than they did at their place oforigin in North Wales. Unfortunatellr, because of the aforementioned gover-ment regulations, the experiment had to be terminated before hatching andliberation took place.
After ferti l isation, B. bolanoides undergoes a period of anecdysis ter-minated by a moult in r 'vhich the penis is lost;the testes and vesiculae seminalesatrophy at this time. Both native North American and transplanted Europeanbarnacles sho'lved similar changes, but the former were some 6 weeks in advanceof the latter. Half the native Ner,vfoundland barnacles had shed their penesbetween October 24 and November 2, 1962, whereas the corresponding datefor t lre transplanted European barnacles rvas between December 7,1962 and
January 8, 1963.
Ecc SrzB
The sizes of the eggs obtained from sarnples of 50 individuals are givenin Table II. It rvil l be seen that the size is l i tt le altered by transplantation.Barnacles from the coast of North America produce significantly larger, andthe European specimens smaller, eggs r,vhether they mature and develop inEurope or in America. The population l iving in Newfoundland, well to thenorth of Woods Hole, produce somewhat larger eggs than those of barnaclesfrom the Woods Hole district. As expected, late stage eggs rvere distinctly largerthan early stage eggs.
EFFECT OF ENVIRONMENT ON DATtr OF BREEDING
Trnar, LBvBr
Table III gives the percentage of individuals carrying eggs in samplestaken at high and lor'v levels betr'veen the tide marks in various localit ies inNova Scotia. In all cases the breeding of the high-water populations hadprogressed further, a higher percentage carrying egg masses. Breeding thusoccurs earlier higher up the shore.
J. F
ish.
Res
. Bd.
Can
. Dow
nloa
ded
from
ww
w.n
rcre
sear
chpr
ess.
com
by
CO
NC
OR
DIA
UN
IV o
n 11
/12/
14Fo
r pe
rson
al u
se o
nly.
CRISP: NA & EUROPEAN BALANUS BALANOIDES
Tesls II. Influence of environment and origin on egg size.
2637
P]ace oforigin
Environmentduring breeding
season
Early stageeggs'
Late stageeggs'
[-ength Breadth Length Breadth
Horse Cove, Nfld.,Canada
Menai Bridge,North \&/ales,U.K,
Woods Hole,Mass., USA
I-Iorse Cove
Menai Bridge
Ilorse CoveWoods HoleMenai Bridge
u
338+7
265 +5
272+6J U / : L )
328t13
r / J f J
137 +3
143+4155+4162+6
It392+6
305+10
325+7338+6J + l t /
p
196+3
160:t4
L I L _ +
180+5t78+6
astages up to appearance of limb buds classified as early istages 1-9, Crisp, 1954); staeeswith-setae and eyes classified as late (stages 10-13). Standard eirors associated with measuremeitsare included.
Teer,n III. Effect of tidal level on breedins.
/6 of sample populationbearing egg masses at
Locality and date H.W.. L.W."
Smith's Beachnear Halifax
MargaretsvilleArgyle Sound
AdultsSpat
Parkers's Cove
Oct.196210
t220
22
J /
59
9695
100
29
339
86
"I{.W. : high water; L.W. : low water.
At Horse Cove, Newfoundland, where the tidal range was much smallerthan in Nova Scotia, a similar effect was apparent from observations madein November. Individuals growing near the high-water mark had in generalmore advanced embryos than those lower down the shore. However, in thesample collected on December 7, 1962 there lvere a few very small 1st-yearindividuals, 4-6 mm diam, carrying embryos that were much less advancedthan those of the normal sized individuals of 8 10 mm diam. This phenomenonwill be considered in the section dealing with the effect of age on breeding.
WavB ExposunB AND STTELTER
At several localit ies in Nova Scotia the breeding state of barnacles growingin exposed positions was compared with that of barnacles l iving at the sametidal level in shelter. Table IV shor,vs that ferti l isation invariably took placeearlier in sheltered situations.
J. F
ish.
Res
. Bd.
Can
. Dow
nloa
ded
from
ww
w.n
rcre
sear
chpr
ess.
com
by
CO
NC
OR
DIA
UN
IV o
n 11
/12/
14Fo
r pe
rson
al u
se o
nly.
2638 JOURNAL FISHERIES RESEARCH BOARD OF CANADA, VOL,25 ' NO' 12 ' 1968
Taer-e IV. Effect of wave exposure and shelter on breeding.
./6 o.f sample populationbearlng egg masses wnen
Locality and date Sheltered Wave exposed
Smith's Beach nearHalifax, high water
Lunenburg, high water
Jeddore Oyster PondLiscombPort HoodPeggy's Cove
Oct.196210
12l3I J
20
52
9087875873
D
4 J
251050
AcB op Ixorvrtu.tr.s
In most localit ies the individuals that have settled in the previous spring
form a readily separable size-class. They are referred to as spat, to distinguish
them from adults in their 2nd or later year of growth. Table V gives the results
of two counts in which adults and spat were compared. In both cases the adults
ferti l ised in advance of spat.A proportion of the smallest spat present at the extreme upper l imit of
the barnacle zone, especially those living in cracks where growth is reduced,
failed to become fertilised in their first year. As mentioned above (p. 2637)'
there was evidence that a few of such individuals may mature and become fer-
ti l ised very much later than adults.
TasI-B V. Effect of age on breeding.
/6 of sample populationbearing egg masses among
Locality and date )1 year o ld (1 year o ld
AllendaleArgyle Sound
Oct.20,1962Oct.20, 1962
87 1 t l
49
DISCUSSION
Balanus balano'id'es breeds annually every autumn, and the time at which
the eggs are laid is remarkably regular (Crisp, 1959a). The date of breeding
is affected, not by the normal variations in temperature and other environmental
conditions at t l-re time, but by those some weeks earlier (Crisp and Clegg,
1960). However, if barnacles are collected in late spring or early summer and
held in a constant environment in the dark at a temperature of from 4 to
J. F
ish.
Res
. Bd.
Can
. Dow
nloa
ded
from
ww
w.n
rcre
sear
chpr
ess.
com
by
CO
NC
OR
DIA
UN
IV o
n 11
/12/
14Fo
r pe
rson
al u
se o
nly.
CRISP: N.A. & EUROPEAN BITLANLIS BALANOLDES 2639
10 C, they r,vil l breed lrithin a lveek or two of the normal t inre (D. J. Crispand B. Patel, unpublished observations). It appears, therefore' that they are
sensitive to environrnental influences only for a l imited period in late summerand autumn, quite unlike species that can be induced to breed by raising thetemperature (Patel and Crisp, 1960). Therefore, the climate at other timesof year appears not to be important to the breeding cycle"
The factors that influence breeding at the relevant t ime are chiefly l ight
and temperature; experiments indicate that a regime of predominantly lol 'r 'l ight intensity at a temperature of less than 10 C for several lveeks is a nec-
essary conditioning experience (Crisp, 1957; Barnes, 1963). In the field,
breeding is advanced in places where there is greater shading, greater shelterfrom lvave exposure or water currents, and greater exposure to the air athigher tidal levels (for discussion see Crisp, 1959a) . Breeding is also advancedat higher latitudes, though there are of course variations from place to place
in response to local differences in meteorological conditions and sea temper-atures. These environmental and latitudinal factors have been shor'vn to
operate in exactly the same manner on populations on the North Americancoast and in Europe, but the American form differs from the European in theearlier onset of breeding in identical habitats, the larger size of the egg, and
the more rapid development of the embryo. These differences persist aftertransplantation in either direction, and are therefore quite independent of theenvironment during the period of gonad maturation. A further difference be-tureen the tu.o races l ies in the greater susceptibil i ty of the North Americanform to parasitism by Hemion'iscus balan'i, as is shorvn in Fig. 2, based on datafrom Crisp (1968). All these differences probably result from genetic responsesto the environment, notably to the harsher rvinters during rvhich the etnbryosdevelop, the earlier plankton blooms (see Crisp, 1964), and to the rarity of
tlre parasite Hemionisctts in the \\'estern Atlantic.
l(Ja
2o5U-o
z
9FUUL
=
Frc. 2. Infection by Hemioniscus of. Newfoundlandspecimens transplanted to Britain. Native North Walesspecimens growing in the same locality showed a low
rate of infection.
MONTHS AFTER TRANSPLANTING
J. F
ish.
Res
. Bd.
Can
. Dow
nloa
ded
from
ww
w.n
rcre
sear
chpr
ess.
com
by
CO
NC
OR
DIA
UN
IV o
n 11
/12/
14Fo
r pe
rson
al u
se o
nly.
2640 JoURNAL FTsHERTES RESE-A,RCH BoARD oF CANADA, vot-. 2s, No. 12, 1968
The distribution of this species extends to much more southerly latitudeson the American coast, and its centre of abundance there is considerably furthersouth than in Europe. For this reason the comparison between the breedingof the species in Wales and in Newfoundland is the only one where the latitudeis closely comparable. The temperature of the sea during the period of mat-uration for the 6 weeks prior to ferti l isation was about the same at this latitudeon the two sides of the Atlantic, though the Newfoundland population fer-ti l ised over a month earlier. The populations further south, in Nova Scotiaand New England, though they ferti l ised somewhat later than the New-foundland population, because of the lower latitude did so at temperaturesrather higher than those prevailing in North Wales at the time of maturationand breeding (1a C dropping to 10 C) or in Nervfoundland when the nativepopulation there was maturing (13 C dropping to 9 C). Thus while the WoodsHole population were maturing, sea temperatures fell only from t7 to 12C and air temperatures lvere not much lower. These temperatures are higherthan those hitherto quoted (10 C) for conditioning the species in Europe (Crisp,1957; Barnes, 1963) and suggest that in America, over the southern part ofits range at least, B. balano,ides is probably adapted to mature at higher tem-peratures than it does in Europe. Probably the rate of fall in temperature,the change in day length, and other factors as well as the actual temperaturelevel may combine in determining'ivhen maturation and breeding take place.The two races clearly react differently and breed at different times rvhen tl-reenvironmental conditions are identical.
ACKNOWLEDGMENTS
I am greatly indebted to \t l iss Elizabeth Brown for assistance in collectingtransplanted specirnens from Newfoundland, and to Mr P. S. \lleadon's forcollecting samples of. Balanus balanoid,es from Nlenai Bridge and dispatchingthem by air. The Nuffleld Foundation, Memorial University of St. John's,Nfld., and Dalhousie University, Halifax, N.S., supported me while I tasengaged in this research. I wish to thank \{r H. R. Found and Mr H. Bradley,Department of Fisheries of Canada, for their help in arranging for a veterinaryinspection of the barnacles at the port of immigration and in obtaining specialsanction from the Canadian Government for the temporary introduction ofexotic f ish.
REFERENCES
Benxns, H. 1958. Regarding the southern limits of Balanus bol'anoiiles L. Oikos, 9: 139-157.1963. Light, temperature and the breeding of Bal'anus bal.anoid.es. J. Marine Biol,
Assoc. U.K., 43: 717-725.
Cnrsr, D. J. 1954. The breeding of Balanus porcatus (da Costa) in the Irish Sea. Ibid.,33:473496.
1957. Effect of low temperature on the breeding of marine animals. Nature, London,1 7 9 : 1 1 3 8 - 1 1 3 9 .
1959a. Factors influencing the time of breeding of. Balanus bal.onoides. Oikos, l027 5-289.
J. F
ish.
Res
. Bd.
Can
. Dow
nloa
ded
from
ww
w.n
rcre
sear
chpr
ess.
com
by
CO
NC
OR
DIA
UN
IV o
n 11
/12/
14Fo
r pe
rson
al u
se o
nly.
CRISP: NA & EUROPEAN BALANUS BALANOIDES 264L
1959b. The rate of development of. Balanus bal,anoid.es (L.) embryos in aitro. J, AnimalEcol.. 28: Ll9-132.
1964. Racial differences between North American and European forms of Balanusbalanoid,es. J. Marine Biol. Assoc. U.K., 44: 33-45.
1968. Distribution of the parasitic isopod Hemioniscus balani with special reference tothe east coast of North America. J. Fish. Res. Bd. Canada,25(6): 1161-1167.
Cnrsr, D. J., eno D. J. Clncc. 1960. The induction of the breeding condition in Bal,anusbal'anodd.es (L.). Oikos, 11: 265-275.
Fucr-rsren, F. C. 1947. Average monthly sea surface temperatures of the western NorthAtlantic Ocean. Papers Phys. Oceanog. Meteorol., 10(2): 25 p.
Pernl, B., eNo D. J. Cnrsr. 1960. The influence of temperature on the breeding and moultingof some warm-water species of operculate barnacles. J. Marine Biol. Assoc. U.K.,39:667-680.
Uxrrno S:rerps Nevy DBpatntpNr. 1955, Marine climatic atlas of the world. Vol. 1. NorthAtlantic Ocean. NAVAER 50-1C-528, Washington, D.C.275 p.
J. F
ish.
Res
. Bd.
Can
. Dow
nloa
ded
from
ww
w.n
rcre
sear
chpr
ess.
com
by
CO
NC
OR
DIA
UN
IV o
n 11
/12/
14Fo
r pe
rson
al u
se o
nly.