FISKERIDIREKTORArPErT'S S K R I F T E R
S E R I E RAV%JK";DERSBKELSER V O L , 34,
XC3,4
DIRECTORATE O F F I S H E R I E S B E R G E N ~ N O R W A Y
1 9 6 8
RELATION BETWEEN THE NORWEGIAN SPRING- SPAWNING STOCK AND THE SPRIKG-SPAWNING GROUP OF HERRING I N T H E NORTH-EASTERN
SEA
BY
STEINAR HARALDSVIK Institute of Marine Research, Bergen
INTRODUCTION
It has been stated by several workers ( B a o c ~ 1909, BJERKAN 1917,
JOHANSEN 1924, KREFFT 1954) that the north-eastern North Sea is a mixing area for spring- and autumn-spawning groups of herring.
Early in this century spring-spa~vners doininated the catches from this part of the North Sea during spring, summer and autumn (B J E R K A N 191 7 ) . In recent years, however, the spring-spawners have been in majority only during the slzol-t seasons fi-om late July to early September (HARALDSVIK 1966 a) while the autumn-spawners have domi- nated the rest; of the year.
T h e spring-spa.cvning group in the northern North Sea is suggested to be a mixed population of Shetland spring-spawners (WOOD 1936), Viking Bank spring-spawners (RUNNSTRWM 194 I ) , Skagerak spring- spawners (ANDERSSON 1949) and Norwegian spring-spawners. The occurence of Norwegian spring-spawners in the northern North Sea has been demonstrated by n~orphological characters (BROCH 1909, HJORT and LEA 191 1, B J E R K A N 191 7) and by tagging experiments (AASEN 1953).
Since 1960 herring in pi-e:pa~vi~ing coi~clition have arrived at the west coast of :outhem Nor~\iny in January, spa~vized in inshore waters in March and April, and disappeared again in May. I n length, age ancl scale type these herring differ from herring at the spawning g~-ornzcls further north, and it has been suggested that the southern herring were originating f ~ o i n the North Sea.
T h i s report presents zorne remits of an i n v e s t i ~ ~ t i o n carried o u t
011 spring-spa~vniszg herrilzg in the north-eastern North Sea during the years 1961-63. An attempt is also made to detect £1-om analysis of racial characters the admixture of the t ~ v o stocks of spring-spa.r.vni11g herring ~vhiclz occur along the coast of Nor~vay.
MATERIAL AND METHODS
Twentythree samples were collected from September 1961 to May 1963, comprising a total of 3825 specimens. Most of the material originate froin commercial catches, b u t 6 samples were collected on- board research vessels.
Table 1
.
Sampling localities and composition of spring- and autumn-spawners in the samples (%) from north-eastern North Sea. 1961 -63.
Sample
number Date
I
GearI
Locality/
spawners Spring/
spawners Autumn1
UncertainTrawl Trawl Trawl Trawl Trawl Traw l Trawl Drift Trawl Drift Drift Trawl Trawl Trawl Drift Trawl Drift Drift Drift Trawl Trawl Trawl Purse-seine
Total . . .
1
25.0 68.8 6.2 3 825Otolith characters were used to separate spring-spawning herring from autumn-spawners (PARRISH and SHARMAN 1958). This procedure left 956 spring-spa~vners to be s~tudied.
Sailipling localities, gears and the proportion of spring- and autumn-spawners in the samples are given in Table 1.
T h e sainples from the spring-spawning stock on the west coast of southern Nor~vay were collected to the west and south of Kergen during March and April 1962 and 1963.
Four samples from east Icelandic waters during July and Ailgust 1962 have also beell i i ~ v e s t i ~ t e d . Tlie inembers of the Norxvegian spring-spawning stock in these samples were separated from the Ice- landic spring- ancl summer-spa~vning herring by scale character&.
All the herring were examined as to age and stage of maturity.
Stage of- maturity tirere determined according to the maturity scale recommended in 1962 by the ICES Herring committee (ANON. 1963).
Both scales and otoliths were used for age determinations. Sec- ondary rings ~ v i t h i n the suinlnei- gi-o~vth zones, transparency of oto- liths and regellei-ated scales sometimes complicated the determinatiol~s or made readings impossible. In the samples from trawl and drift-net several specimens had lost all scales suitable for age readings. There- fore, ages coulcl only be cletermined from 55 per cent of the scales and from 85 per cent of the otoliths. Horvever, c o ~ ~ s i d e r i n g the two methods together, posltive age cleterininations were achieved for about 90 percent of the total material.
Number of vertebrae, first g ~ o w t h zone measurement 011 otoliths and 11, 12 and 13 lengths were determined for part of the material.
T h e first g-so~vth zone in otolitlls was measured from the centre of the opaque i ~ r r c I e ~ ~ s , along an axis to the post-rostrum to the distal edge of- the first winter-ring.
T h e gro~vtll of the herring w7as estimated from scales applying the modified growth formula by LEA (1938).
RESULTS AND DISCUSSION AGE COMPOSITION
T h e samples of spring herring from the north-eastern North Sea have been g-rouped into periods of 4 months and the age cornpositions are illustrated in Fig. 1. T h e ages ranged from 1 to 12 years, but
~ ~ i t h a strong dominance of the younger year-classes. T h e 1959 year- class tvas dominant in 1961 and 1962. I n 1963, however, it was replaced by the 1961 year-class. T h e reduction of the 1959 year-class
YEAR - CLASS YEAR - C L A S S YEAR - CLASS
Fig. 1. Age colllpositio~l of spring-spawning herring from north-eastern North Sea, 1961 -63.
1) Sept.-Dec. 1961, N = 94, 4) Sept.-Dec. 1962, N -- 234, 2) Jan. - April 1962, N = 194, 5) J a n - M a y 1963, N = 84.
3) May- Aug. 1962, N = 253,
111 winter and spring 1963 inay either be due to an emigration or to a high abundance of the 1961 year-class. Tlre latter explanation seerns to be the most reasoilable since tile 1961 year-class provecl to he strong in the north-eastern North Sea in both 1964 and 1965 (HARAL'DSVIK
196G b and 1967). I n 3'18. 2 are s l r o ~ \ ~ n the age compositions in the sanlples collected i n 1962 noit11 and south of latitude 59"N. From
these histograms it appears that the 1 and 2 year old herring were most ab~ulclant in the southein area, and this may indicate that the spi-ing-ipa~vning group of hei-ring i n the no1 tll-eastern North Sea is recruited froin the soutllern area.
T h e age compositions for the ~pring-spa~vners at the west coast of
~outhei-11 Nor~vay are sho~vn i n Fig. 3. I t appears that the 1958 year- clas,s i n 1962 ancl the 1960 year-class in 1963 were move abundant in this are? than in the nort11-eastern Nortli Sea.
T h e Noi-~vegian spring-spa~irning ctocli 1uas in the years 1961 and 1962 dominated by the 1950 year-class, which contributed about 60 perccnt of the herring. T h e 1958 and 1959 year-classes were lepre- sented by less than 1 percent during the same years (DEVOLD and
~ S T V C D T 1963 and 1964).
z -
1950 52 54 56 58 60 62 Y E A R - C L A S S
Fig. 2. Age coinpositioil of spring- Fig. 3. Age coinpositioll of spring- spawning herring sampled north and spawners from the wcst coast of southern south of latitude 59" N in north-eastern Norway, 1962 and 1963.
North Sea, 1962. 1) 1962, N = 177,
1) North of N 59", N = 321, 2) 1963, IT = 188.
2) South of N 59", N = 283.
T h e age torrrpositioiis therefore do not indicate any evident con- nection beit~veen the spring-spax\rniiig group of llerrillg in the north- eastern Noi-t11 Sea and the t ~ v o spring-spawning stocks along the coast of Noi-way.
VERTEBRAE
T h e frequency distributions of the vertebrae counts in the samples horn the iiorth-eastern North Sea are given in Table 2. T h e meall number of vertebrae ranged from 56.90 to 57.32, but no geo-
$1-aphical trend or trend in time \\,as observed. An allalysis of variance sho~vecl that the dilerences of vertebrae couilts within samples Tvcre iilsignificaiit comparecl ~ v i t h the differences betweell means of sn~nples (F = 1.076, p <0.05). I t inay therefore be concluded that the samples are clra~vii lroin the saiile stock or same mixture of stocks. It is then, Ilo~vever, presupposed that a real difference in vertebrae number occur between the various spring-spawning stocks. In Table 3 the vertebrae frequency distributioll of- tlle spring-spa~vning group from the North Sea iv compared with the vertebrae frequency distribution for the Nonvegian spring-spa~vning stock and the spring-spawners at the west coast of souther11 Norway. T h e significances of the differences
Table 2
.
Vertebrae counts of spring-spawners from north-eastern North Sea. 1961 - 63 .I
Date1
Vertebral Countnumber 55
1
561
571
581
591
60I
.
l) x = average deviation from ((working mean)). 57 vertebrae
.
1 . . . 1119 -61
. . .
2 2419 -61 3
. . .
16/10 -61 4 . . . 19/12 -61. . .
5 19/12 -61 6
. . .
1911 -62 7 . . . 2011 -62 8 . . . 113 -62 9. . .
2413 -62 10 . . . 615 -62 11. . .
715 -6212
. . .
2215 -62 13 . . . 716 -62 14. . .
2717 -62 15 . . . 2818 -62 16 . . . 319 -62 17. . .
2519 -62 18 . . . 9/10 -62 19. . .
20/11 -62 20 . . . 2211 -63 21 . . . 2012 -63 22. . .
23/3-63 23 . . . 315 -63Total
1
ill mean vertebrae count have been tested. giving t = 1.588 (0.1
<
p <0.2) between the spring-spawners fi-om the North Sea and the Norxvegian spring-spawning stock. and t = 2.931 ( p <0.01) between the spring-spawners from the North Sea and those from the west coast of southern Nor~vay
.
I t should. ho~vever. be noted that the results of this test are pro~bably not reliable as different year-classes are domi- nating in the different groups of herring considered.
Further.the mean vertebrae count of the spring-spawners from the west const of southern Nor~vay is based upon only three samples in which the means varied considerably (57.3 1. 57.20, 57.09).
An admixture of the two spring-spawning stocks from the coast of Norxvay cannot therefore be excluded by the available data on the vertebrae count
.
T h e mean vertebrae numbers in the present material show good conformity with earlier findings on spring spaw- ning herring in the northern North Sea ( R U N N S T R ~ M 1941.WOOD
1936).
- 3 5 2 - - 10 -0.1000 0.5444
- 3 4 1 1 - 9 0.0000 1.0000
- 1 1 6 5 - - 22 0.1818 0.2511
- 4 1 7 6 - - 27 0.0741 0.3789
- 1 23 13 - - 37 0.3243 0.2808
- 4 3 4 7 1 - 46 0.1087 0.3213
- 15 32 13 1 - 61 0.0000 0.5333
I 18 53 11 2 - 85 -0.0588 0.4846
- 1 7 1 - - 9 0.0000 0.2500
- 2 1 6 4 - - 22 0.0909 0.2771
- 5 1 3 7 - - 25 0.0800 0.4933
- 2 10 3 - - 15 0.0667 0.3524
- 4 1 2 6 - - 22 0.0909 0.4675
- 20 63 21 1 - 105 0.0286 0.4319
- 10 49 23 - - 82 0.1585 0.3820
1 21 92 41 - 1 156 0.1346 0.4656
- 2 14 2 - - 18 0.0000 0.2353
- 11 44 12 1 - 68 0.0441 0.4010
- 5 17 14 1 - 37 0.2973 0.5480
- 11 23 11 1 - 46 0.0435 0.5758
- 4 2 4 3 - - 31 -0.0323 0.2323
- 2 2 2 - - 6 0.0000 0.8000
- - 9 2 - - 11 0.1818 0.1636
2 149 579 210 9 1 950 0.0821 0.4274
Fig. 4. Percentage compositioll of maturity stages in spring-spawning herring from north-eastern North Sea, 196 1 - 63.
1) Maturity stage I, 5) Maturity stage V, 2) Maturity stage 11, 6) Maturity stage VII, 3) Maturity stage 111, 7) Maturity stage VIII.
4) Maturity stage IV,
Tablc 3. Vertebrae counts of the Norwegian spring-spawning stock, spring-spawners from the west coast of Southern Norway and the spring-spawning group in north-
eastern North Sea.
Vertebral Count
Categories
/
551
561
571
581
591
60I
Norwegian spring- spawning stock, 1962 Spring-spawners, SW coast of Norway 1962 and 1963
. . .
.Spring-spawners, North Sea, 1962.
.
..
-
l ) x = average deviation from ctworking mean)), 57 vertebrae.
MA TURITY
T h e samples from the north-eastern Nortli Sea have been collected throughout the year and the maturity investigations may therefore give a rough picture of the maturing cycle for the spring-spawning herring in tlris area (Fig. 4). T h e low percentage of llerring in spaw- ning condition, and the low abundance of- sl>ring-spawners in the samples fro111 the end of March in 1962 and 1963 (Table 1) may indicate that the s p a ~ ~ r n i n g gro~lncls are situatecl outside the north- eastern Nortll Sea.
1 2 3 4 5 5 +
A G E
Fig. 5. Colnpositions of immature herring, herring in maturity stage I11 and mature herring amongst 1-5+
year old spring-spawners in north-eastern North Sea during the winter and spring 1962 - 1963.
1) Maturity stage 1-11, 2) Maturity stage 111, 3) Maturity stage IV-VIII.
Spent herving in stage VIil were rccorcled in tile samples from the encl of hfarch and the beginning of May. A duration of t h e e weeks of this nlaturity stage (JAKOBSSON 1962) should indicate a spawning seasoil from second half of February to mid April. Recovering spent llerl-ing were in cloininance from the end of March to the first half of August. Stage I11 occurred in mos~t of the samples, but were clorni- nant from micl August to the beginning of October. Stages IW mcl V were found froin1 the end of August to the beginning of hfarc!l, but had their maxima before and after the turn of the year respectively.
I t mlrst:, ho~vever, be empilasized that the ilumbei- of sanlples ailcl the number of sl3ecimens within several of the samples are few and one must tilerefore be very careful in generalizing froin the present data.
T h e N o r ~ v e g i a ~ l spring-spa~vniug stock and the sprii~g-spa~vners at ilie -\vest coast of soutlrern Norxvay lzad in the years I 9 6 1 ailcl 1963 their spa~vning season f1-on1 the end of February to the eilcl of AtIarch ancl from lnicl hfarcll to Inid April respectively. These spawning periods were thus inside the range of tile spaxvning season for the spring-spa~vning 91-onp of herring in ~zorth-eastern North Sen. X con-
~lectioil bct~veen the spring-spawners in the north-eastern North Sea and the spawning g~-ounds at the coast of Nor~vay cannot therefore be excluded.
Maturing cycle of the two spawning stocks at the coast of Norway is ruzk~lown. Investigations in Icelanclic waters during surnnler suggest, horvever, that the fierring of the Norwegian spring-spa~viiing stock pass over from stage VPII t o stage I11 in the first half of July
( ~ S T V E D T 1962), i.e. about one month earlier than indicated for the spring-spawning g,orxp in the north-eastern North Sea.
AGE A T FIRST SPAWNING
I t was impolslslible to ditlereiltiate the winter-rings on the scales of the spring-spa~vning herring in north-eastern North Sea into cccoastal,,, ccoceanicn and <<spawning>> rings
( R U N N S T R ~ M
1936), except for six llerring belonging to the northerii type of the Norwegian spring-~ p a ~ v n i n g stock. Theretore a different approach was used to cletermine age a t first spa~vning. T h e age a t first sparvni~lg has been based upon the maturity cornpoisitio~~s by age in the samples collected during the 13eriod January to July. Herring in stage 111 in this period are clas- sified a, rtncertain. i.e. they may be immature and do not spawn l ~ e t o r e the next season, or herring in stage 111 ,lt the beginning of
he period may reach maturity and further, herring in stage I11 at the elid of the period may have spawned and already recovered their gonads). T h e p~ercentage composition of immatures (stage I and IT), uncertain (stage 111) and spawned herring (stages IV-VIII) in each age <group are presented in Fig. 5. I t will be seen that a few herring already spawned at an age of two years, but the majority, about 77 percent, were spawning at an age of three. Only about 2 percent of the four year old herring were immature.
T h e Norwegian spring-spawners may attain maturity at a n age between three and nine years. However, i n 1962 and 1963 the three year-old spawners were scanty represented on the spawning grounds off Msre (DEVOLD and ~ S T V E D T 1964, ~ S T V E D T 1965). The herring at the west coast of southern Norway were, on the other hand, in the same years dominated by three year olds, which were all in spawning condirion.
FIRST GROWTH ZONE MEASUREMENT MADE ON OTOLITHS
T h e six herring, belonging to the northern type of the Norwegian spring-spawning stock, had typical otoliths which were easily picked out. These otoliths had thin, sharp winter-rings and a growth pattern similar to that on tlie scales< In the rest of the spring-spawning herring from the north-eastern North Sea it was impossible to recognize distinct otolith types. 'The major part of the otoliths had relatively large first and second growth zones and ccsoftx first and second winter-rings.
T h e ranges and means of tlie first growth zone measurements are presented in Table 4. I t appears that the ranges and means were of the same order in the samples from 1961 and 1962. T h e high values obtained in 1963 may be explained by growth differences between year-classes. As stated before the 1960 year-class dominated the samples froni 1963, ~vlrile the 1959 year-class was the mast prominent one in 1961 and 1962. Considering the total material the first growth zone measurements ranged from 13 to 29 units (one unit = 0.0409 mm), and had a mean value of 22.90 units (standard error
-.
$- 0.153).T h e values of first growth zone measurements Ivere less than those recorded previous for the autumn-spawning group of herring in the same area (HARALDSVIK 1966a). The difference is probably connected with differelices in age at formation of the first winter-ring. T h e spring-spawners lay down a winter-ring during the first winter, while the autumn-spawners do not form winter-rings before the second winter.
Table 4 . Ranges and means of first growth zone measurement on otoliths from the spring-spawning group of herring in north-eastern North
Sea (1 units = 0.0409 mm), 1961 -63
.
Sample
number
I
Date1
Range1
Mean/
N6 . . . 1911 -62 7 . . . 2011 -62 8 . . . 113 6 2 9 . . . 2413 -62 10 . . . 6 / 5 - 6 2 11 . . . 7 / 5 - 6 2 12 . . . 2215 -62 13 . . . 716 -62 14 . . . 2717 -62 15 . . . 2818 -62 16 . . . 3 / 9 - 6 2 17 . . . 2519 -62 18 . . . 9/10 -62 19 . . . 28/11 -62 Sum 1962 . . .
111 Fig
.
6 are shown the distributions of first growth zone mensure- ments for the spring-spawning g ~ o u p of herring in north-eastern North Sea. for the Nomvegian spring-spawning stock and for the spring-sipa~vners at the west coast of southern Norway.
T h e 1959 year- class is dominating in the stocks considered.
The figure shows good conformity between the spring-spawners in north-eastern North Sea and those at the west coast of southern Norway.
Suggesting that the size of the first growth zone is linked to the food supply during the first year. the good comformity in the first growth zone measure-. . .
20 2211 -63
21 . . . 2012 -63 . . .
22 2313 -63
23 . . . 315 -63
22 - 29 24.9 35
20-27 23.2 24
22 - 26 23.3 6
21-24 22.7 11
Sum 1963 . . .
1
20-29 23.9 76. . .
Grand total
1
13-29 22.9 855ment may indicate that the spring-spawning Iielriiig in north-eastern Nortfi Sea ancl those a t the west coast ot southeril Norway have the same feeding g r o u ~ i c l ~ d ~ t r i n g theiu iirst year of life.
Fig. 6. Frequency distributions of otolith zone measurements, 1961- 1963.
1) Spring-spawners from north-eastern North Sea, 2) Norwegian spring-spawning stocli,
3) Spring-spawners from the west coast of southern Norway.
GRO W T H
T h e growth of the herring is o i ~ e of the mail1 characters used to distinguish between various herring stoclts. LEA (1910, 1938) has s h o ~ t ~ i i that the relation between scale length and total le11gth of the herring is approxiinately linear. T h e I , distribution? of the 1959 year- class of the spiing-spa~vning gi-oup of herriilg fro111 north-eastern North Sea, the Norwegian spring-spa~vning stock (S-type) ancl the spring-spa~i~ncrs at the west coast of soutl~ern Nor~vay are given in Fig. 7. T h e mean 11, l 2 ancl I d values for the same stoclzr are presented in Table 5 . From these data it appears that the gro~vtli of tlle S-typed herring of the Nor~vegian spring-spawning stock deviated considerably from the growth of the two oither stock?. T h e I , distrihntion and the rneaii values of 1 1 , l 2 aiid 1:: Sol- the spring-spawners ill north-eastern North Sea were slightly lower than those for the spring-spa~viiers a t the west coast of southern Norway. I t should be noted that the
L E N G T H - C M
Fig. 7. Frequency distributions of 1, of three year-olds in 1962.
1) Spring-spawners fro111 north-eastcrn Xorth Sca, 2) Norwegian spring-spawning stock, 3) Spring-spawners from the west coast of
southern Norwav.
Table 5. Mean l,, 1, and 1, values of three year-old (1959 year-class) spring-spawning herring from the north-eastern North Sea and the coast of Norway, 1962.
Categories
I
I ,I
NI
1 2I
NI
'3I
I
I
rln -s awners, S p ' g P
NE North Sea . . . Spring-spawners,
S W coast of Norway
.
98 Norwegian spring-spawningstock (S-type)
1
9.85 15222.89 135
23.40 96
16.94 152
1
24.07 15227.68 88
28.66" 98
* Total mean length of three year olds in April.
herring from the west coast of southern N o w a y were caught by net with a large mesh size (winter herring net), and the selectivity of the net may probably affect an overestimation of the mean I,, 1, and 1, values for this stock.
Taking this into consideration and assuming that the growth rate of the fish is related to the feeding, i t seems reasonable to postulate that the spring-spawned herring in the north-eastern North Sea and thosie at the west coast of southern Nortvay have inhabited the same feeding grounds during the first, seconcl and third year of life.
CONCLUDING REMARKS
In an attempt to outline the connection between the spring-spawning group of herring in the north-eastern North Sea and the t.itro spring- spawning stocks at the coast of Norway, i.e. the Norwegian spring- spawning stock and the spring-spa~vners at the vest coast of southern Nonvay. some biological characters for these groups of hei-ring have been con~pared. Due to the plasticity of these characters it is impos- sible to identify the individual fish, but comparing several characters and large samples this n ~ e t h o d may, however, provide valuable infor- mations in this identification work.
T h e age composition, age at first spawning, scale type, growth characteristics for the spring-spawning group of herring in the north- eastern North Sea deviated considerably from those obtained for the Norxvegian spring-spawning stock. I t is therefore concluded that the occurence of herring from the Nonvegian spring-spawning stock was negligible in the north-eastern North Sea during the years 1961-63.
This is in contrast to results obtained by BROCH (1909),
H J ~ R T
and LEA (191 1) and BJERKAN (1917), who found the Norwegian spring- spa~vning stock to be dominating within the spring-spawners in this area. T h e absence of Nor~vegian spring-spawners in the north-eastern North Sea in recent years may be explained by the change of spawning grounds for this stock (DEVOLD 1963). The spawning grounds have since 1960 been off R/l@re and it is reasonable to assume that the m i g ~ a t i o n route to and from the feeding area in the Norwegian Sea in recent years is north of the North Sea.Comparing the spring-spawning group of herring in the north- eastern North Sea and the spring-spawners at the west coast of southern Norway, good agreement is found in age at first spawning, scale type and growth rate during first, second and third year of life.
These characters are susceptible to environmental influence, and the good conformity may argue for the herring compared to have the same feeding and overwintering areas during the three first year of
life. T h e characters deviate fvom those of herring which have their nursery and adolescent stages in coastal waters ( R U N N S T R ~ M 1936), and it is therefore suggested that the spring-spa~vners at the west coast of southei-11 Norway have spent their three first years in the North Sea.
T h e spring-spawning stock at the west coast of southern Norway differ from the spring-spawning group of herring ill the northern North Sea by being spawning in inshore waters of relative low salinity and temperature, having different abundance of year-classes and probably also a higer mean number of vertebrae. Outside the spawn- ing season this spring-spawning stoak probably mix with the spring- spawners in the north-eastern North Sea. T h e low total mean num- ber of vertebrae, and the low abundance of the 1960 year-class in the spring-spawning group of herring in the north-eastern North Sea may, however, indicate that the spring-spawners from the west coast of southern Nor~vay only constitute a minor part of the spring-spawning group of herring in the north-eastern North Sea.
S U M M A R Y
1. Age composition, number of vertebrae, age at first inaturity, scale type and g-ro1\7th cl~aracteristics for the spl-ing-spawned herring in the north-eastern North Sea in 1961-1963 have been analysed.
2. Some of these characters have been compared with those for the two spring-spawning s~tocks at the coast of Norway; i.e. the herring spawning off M@re and the herring spawning at the west coast of southern Norway.
3. Less agreement with the spa1\7ners off MGre, indicates that menlbers of this stock were scanty represented in the spring-spawning group in the north-easltern North Sea.
4. Good agreement with the spawners at the west coast of southern Nonvay, indicabes that this herring stock outside the spawning season may be distributed in the north-eastern North Sea.
R E F E R E N C E S
AASEN, 0. 1953. Tagging experiments. Annls biol., Copenh., 9 : 171- 173.
ANDERSSON, K. A . 1949. Swedish investigations. Annls biol., Copenh., 5 : 82-84.
A N O N . 1963. Herring Committee. Proces-Verbal Reun. Cons. perm. int. Explor. Mer, 1962:
66-77.
BJERKAN, P. 1917. Age, maturity and quality o f North Sea herring during the years 1910- 1913. FiskDir. Skr. Ser. HavUndcrs0k., 3 (1) : 1 - 119.
BROCH, H . 1909. Norwegische Heringsuntersuchungen warend der Jahre 1904-06.
Bergens Mzis. Aarb., 1909 (1) : 1 - 69.
DEVOLD, F. 1963. T h e life history of the Atlanto-Scandian herring. Rapp. P.-o. Reun.
Cons. perm. int. Explor. Mer, 154: 98- 108.
DEVOLD, F. and BSTVEDT, 0. J. 1963. T h e Norwegian herring fisheries in 1961. Annls biol., Copetzh., 18: 148- 149.
- 1964. The Norwegian herring fishery, 1962. A d s biol., Col~eilh., 19: 124- 129.
HARALDSVIK, S. 1966 a. T h e autumn spawning group of herring in the north-eastern North Sea. Co~in. il4eel. int. Coz~n. E.xI11or. Sea, 1966 ( H 26) : 1 - 15, 11 tab., 9 fig.
[Minleo. J
- 1966 b. The Norwegian herring fisheries in the North Sea and Skagerak in 1964. Anizls biol., Cope~zh., 21: 147- 149.
- 1967. T h e Norwegian herring fisheries in the North Sca and Skagerak in 1965.
Annls biol., Copenh., 22: 148- 153.
HJORT, j. and LEA, E. 191 1. Some rcsults of the inter~lational herring investigations 1907 - 19 1 1. Pztbls Circonst. Cons. perm. int. Explor. Mer, 61: 8 - 34.
JAKOBSSOX, J. 1962. T h e annual cycle of the maturity stages of the Icelandic herring.
Cozln. i\/leel. int. Coun. Explor. Sea, 1962 (paper 97): 1-2, 2 tab., 3 fig. [Mimeo.]
JOHANSEN, A. C. 1924. O n tile sunlmcr and autumn-spawning herring of the North Sea.
iVeddr Ko~iz~nn Havz~nders., Serie : Fiskeri, 7 (5) : 1 - 1 19.
KREFFT, G. 1955. Untcrsuchungen zur Rassenfrage beim Hering. iWitt. Inst. Seefisclz., 6 : 12-23.
LEA, E. 1910. 011 the methods used in the hcrring investigations. Pubis Circonst. Cons.
perm. iizt. Explor. Afm, 53: 7- 33.
- 1938. A modefication of the formula lor calculatio~l of the growth of herring.
Ra@ P.-v. Reun. Cons. perm. int. Explor. ilJer, 108: 14-22.
PARRISH, B. B. and SHARMAN, D. 1'. 1958. Some renlarlts oil methods used in herring ccracial,> investigation with special reference to otolith studies. Rapp. P.-tl. Rel~tz.
Cons. pernz, int. Esplor. Mer, 143: 66-80.
RUXNSTRDM, S. 1936. A study on the lifc history and lnigrations of the N o r w e g i a ~ ~ spring-herring based on the analysis of the winter-rings and s u ~ u m c r zones of the scale. FiskDir. Skr. Ser. HauUizilersok., 5 (2) : 1 - 103.
- 1941. Racial analysis of the hcrring in I';orwegian waters. FiskDir. Skr. Ser.
HavUndersok., G ( 7 ) : 1 - 110.
M'ood, H. 1936. Race investigation of the herring population of Scottish waters.
Scie~zt. Invest. Fislzetly Bd Scotl., 13: 1 - 52.
~ S T V E D T , 0. J. 1962. Maturity stages in the Norwegian spring spawning herring in relation to time of spawning. Cou1z. Meet. int. Co11iz. Explor. Sea, 1962 (paper 154) :
1 - 3, 5 fig. [Mimeo.]
- 1965. The Norwegian herring fishery, 1963. 3. Biological data. Annls biol., Copetzh., 20: 166- 168.
Received 3 February 1968 Printed 13 Sepenltber 1968
F~skDi,. ,Ski. Ser. HiiuUiiders., 14: 199-228
THE GAS BLADDER AS A HYDROSTATIC ORGAN IN T H Y M A L L US T H Y M A L L US L., OSiZilERUS EPERLArVUS L.
AND IWALLO TUIS VILLOSUS MUI,L.
BY
GORAN F A H L ~ N 2001. Inst., Luncl, Sweclen
I N T R O D U C T I O N
T h e suborder Salmoi~oiclei xvithin the orcler Clupeiformes (BERG 1940) has typically a physoston~ous gas blaclcler. The suborder comprises several families, some of ~ z d ~ i c l ~ contain only deep-sea species. I n these the gas blaclcler either is absent - as in the family Bathylagiclae (MAR-
SHALL 1960) - or has become modified to a type suited to the high hydrostatic pressure of great depths; it has lost the pileumatic duct and developed rctia mitabilia ancl a posterior resorbent chamber (COHEN 1958, FANGE 1958, MARSHALL 1960, F A H L ~ N 1965). Of tllose families which have retained a physostomous gas blaclder, only a few are represented in Scandinavian waters. Therc are several species of the fanlily Thymallidae in N. America and Asia, b ~ t only 011e in Scandinavia, Thymallus t h m a l - lus ( L . ) . The family Osmeridae comprises three genera, two of uihich, Osrnerzts and Mallotz~s, are each represented by one species in Scandinavia, Osmerus eficrlanzls (L.) and iVfallotus t'illosus (MULL.). T h e other Salmonoicl families, apart from the family Salmonidae, which is wide-spread ill the Northern hemisphere, are found principally in eastern Asia, S. America and Australia.
T h e gas bladders of the three species mentioned have been subjected to 17ery little attention. Ho~vever, their general morphology was early described by CUVIER and VALENCIENNES (1848). BEAUFORT (1909) mentioned the bladders of these species very briefly, thougll without adding anything to the description given by CUVIER and VALENCIENNES
(1 848). 1~10re detailed investigations on the morphology of the Salmonoid gas bladder dealt exclusively with species belonging to the genera ,S'alnzo (CORNING 1888, EISSELE 1922, JASINSKI 1963) and Coregotzus (JASIN- SKI 1963, F A H L ~ N 1967b), as dicl also physiological works (SUNDNES, ENNS and SCHOLANDER 1958, WITTENBERG 1958, SUNDNES 1963). SAUN-
DERS (1953) is the only one who carried out experiments on one of the three species mentioned. He analyzed the contents of the gas bladder of Osnzerzis eperla~zus and measured the flotation pressure of the fish.
T h e present investigation is an attempt to reveal those morphological structures which are necessary for a possible function of the gas bladder as a hydrostatic organ. T h e mechanism by wllicl~ gases are introduced
into the Salmonoid gas bladder is unknowi~. T h e formerly prevailing opinion, that all fishes with a pl~ysostomous gas bladder fill it only by swallowiilg air a t the surface, has lately been strongly debated. WITTEN-
BERG (1958) stated that Salmo species are alsle to fill their gas bladders, though very slowly, even if they are deniecl access to the surface. And as early as 1892 HUFNER pointed out that deep water Coregonids have to introduce gas into the bladder against considerable pressure gradients.
SAUNDERS (1953) stated the same for Osmerus and Lez~cichthys. T h e secre- tion of gas into the bladder of Coregonzis has been assumed to be of the same nature as the gas secretion of the physoclistous gas bladder (SUND-
NES 1963). Though the physiological expcriments are very few (SAUNDERS 1953), it has been assumed that some sort of secretion also may occur in the gas bladders of Osmerus, Thymallus and Adallotus.
T h e principle of gas secretion in the Salmonoid gas bladder is not clear. S U N D N E ~ (1963) suggests that the nzechanism might be tlze same as that of the physoclist bladder. KUHN, MARTI, I<UEIN and RAMEL (1963) and STEEN (1963), however, show that the counter current capillary system, present in all physoclist gas bladders and also in the eel, is necessary for building up a partial pressure of the gases in the blood, which makes it possible for the gases to pass into the gas bladder. Among fishes with a physostomous gas bladder, the families Cyprinidae and Esocidae are able to secrete gases into the bladder (JACOBS 1934), and they possess counter current systems (RAUTHER 1923). T h e Clupeicl gas bladder has no ~etia mirahilia and no gas secretion ( F A H L ~ N 1967a). I n Coregonus, a counter current system is present ( F A H L ~ N 1967b), and there is a secretioil of the same gases as in the physoclist bladder, which is reflected in the composition of the gas (FANGE 1953, S U N D N E ~ 1963).
M A T E R I A L
Thymallzls thymallzls : 6 specimens, caught in Lilla Lule River, Nortllern Sweden.
Osmerzls eperlanus : 1 specimen, caught in the Baltic in nets.
Mnllotus villosus : About 40 specimens, caught in the Barent Sea by ineans of trawling.
M E T H O D S
T h e gas analyses of Mallotus villosus were made in a I<rogh microgas analyzer (KROGH 1926) with K O H and pyrogalloll as absorbents for carbon dioxide and oxygen respectively, on the Norwegiail research vessel 'G. 0. SARS'.
T h e sole specimen of Osmerus eperlnnus was fixed in BOUIN'S fluid.
The gross morpl-rology of the gas bladder of the other two species was studied on fresh specimens and on specimens fixed in 4% formalde- hyde. Injections of the vascular system were made with Indian ink.
Fixation for histological and histochemical investigations were made with BOUIN'S fluid or its modification B 15 containing also chromic acid and urea (ALLEN)", in uranylacetate-sublimate, potassiumdichromate
(SCHILLER)~ or in osmiumtetroxyde-chromic acid fixation (CHAMPY).*
For electron microscopic investigations fixation was carriecl out in buf- fered osmiumtetrox)~de (PALADE)* or in osmiumtetroxyde-chromic acid (DALTON).* AS imbedding media paraffin or polyester wax was used for l-ristological and histocl-remical studies and metachrylate for the electron microscopic investigations. Cutting for the last mentioned purpose Tvas carriecl out on an LKB Ultrotome ultramicsotolz.ie, and the electron microscope used was an Akashi T R S 50.
Paraffin- and wax-imbedded material was stained according to differ- ent l-rematoxyline methods (HEIDENHAIN, EHRLICH, M~EIGERT)* with counterstains and azocarmine with counterstains. Silver-impregnation for nerves and cell nuclei was carried out according to the BODIAN*
method. For histochemical purposes the periodic acid-Schiff technique according to HOTCHKISS (PARS)* was usecl for carbohydrate-coiztaining proteins, the paraldehyde-fuchsin metllod (GABE 1953) for muco- polysaccharides, the alcian blue method for acid mucopolysaccharides and the carmine method for glycogen (BEST)*.
111 order to ii~cluce gas secretion, drugs were injected into a n u n ~ b e r of speciemens of Mallotus villosus. Pilocarpine is a secretion-stimulatii~g clrug and is reported to induce gas secretioil in Esox (DRESER 1892). Yolzimbine and dibenzyline are sympathicolythic substances. T h e former has been shown to incluce secretion in Cor~gonus ( F A H L ~ N 1967b), the latter causes inhibition of gas loss from the gas bladder (HARVEY, in press).
R E S U L T S
T H E GAS BLADDER OF TH1712/IALLUS TH17MALLUS To~ogr@hjr.
CUVIER and VALENCIENNES (1848) describe the gas bladcler of the grayling, Thymallus thymallus, as extremely big and communicating with the oesophagus by an unusually short pneumatic duct. BEAUFORT (1909) has nothing to add to this description. According to the present investi- gation the organ comprises 5 -6% of the total volume of the animal, which
*
Descriptions of histological and histochemical methods, referred to by name only, are found in ROMEIS (1948) and PEARSE (1960).202
is normal for Salmonoicl lislles. I t is of the orclinary Salmo~ioicl fusiforrn shape, stretches from tl-te supracarclial region to the anus and the liind- most part of the abdominal cavity. As is usual for Salmonoicl gas bladders, it is only loosely conliected wit11 the surrouncling organs ancl tissues.
The blaclder is ventrally covered by tlie inesothelium ol the peritoiieal cavity. T h e posterior part ends blindly in a roulidecl tip ilnliiediately above the anus, and anteriorly the bladder tapers towards the moutli of the plieuinatic duct. This originates a t the anterior enci and irnmecli- ately bencls beck~varcls. Thus tliere is a relatively sharp boundary be- tween tlie gas bladder proper aild the piieumatic cluct. I n a gas lslaclcler of about 60 mni length it first runs lsackwards about 5 nim, the11 sl~arply lsends for~varcls aiid after about 5 miii it encls in tlle ventral wall of the oesophagus. The diameter of the cluct is practically constalzt. Only where it leaves the gas blaclder it is somewhat xvidcr than in tlle rest of its course. Tlie clelso~~ch of the pneumatic duct into tlle gas blaclcler is nornially wide o~e11 and seems never to he closed by a sphincter. At the other eild, however, the opening in the wall of the oesolshag~~s is often tightly closed.
T h e vessels reaching the gas bladder are two branches of the coeliaco- snesenteric artery, running along the pileumatic duct. They give off only fexv vessels to this part of the organ, and these penetrate the sub- muscularis aiid the muscularis as arterioles and venules and form in the lamina propria a capillary network, which lies close to the lsase of tlie inner epithelium. Then the vessels run laterally along the gas blaclder backwards. These longitudinal arteries give off lsraszclies wl~ich again branch repeatedly and dichotomously. T h e drainage of tlie gas bladder is carried out by branches of the hepatic portal vein, which accompany the arteries to the gas bladder. T h e veins branch in the same way as the arteries do, and flat buliclles are formed which colisist of three or more vessels, ~ v i t h alternating arterial and venous capillaries (Figs. 1, 3 ) . Tlie number of vessels forming the bundles is about 100 in a trailsversal - section of a gas bladder of 60 m m length. There seems to be no difference in frequency of the vascular bundles in the different parts of the gas blaclder. T h e total length of all vessels running in bundles in one and the same gas bladder is estimated a t about 6 meters.
The vascular bundles all run in the submuscular coiinective tissue layer. At irregular intervals they cross the muscularis ancl enter the subepitl~elial layer of connective tissue, the lanii~ia propria. Here the vessels form a capillary network in clirect contact ~vitli the base of the
epithelium. The vessels sometimes run sorne nlillimeters together after they have reacl~ed the lamina propria and split illto capillaries, but vascular lsuilclles of the same type as in the submuscularis arc formed oiily occasionally. The capillaries form a net~vork, ~vhicli is son~exvllat clraxvn out in the loilgitudinal plane of the gas bladder. The average distance between tlie lor~gitudinal capillaries is about 20 microns. The diameter of tlic capillaries is abortt 8 microns.
Histology.
Tlle layers known iron1 other physostomous gas hladders are present also in that of the grayling. As usual, the organ is ventrally covered by the peritoneal epithelium, whiclz here is cubical. Beneatli tlie epitlielium ventrally, and a t the outernlost layer dorsally, the tunica extcrna forms a tough slzeatll round the organ (Fig. 1). However, the tuilica externa
Fig. 1. TlgJtnalbts tlynzallzis.
Transverse section of gas bladder wall.
e = epithelium, m = muscularis, s = submusc~~laris, t = tunica externa, v = vascular bundle.
400x.
in tlie gas lsladder of the grayling is consideralsly thinner than in other Salmonoids investigated ( F A H L ~ N 1967b, F A H L ~ N , unpublished obser- vations). I t consists of a network of connective tissue fibers, some of them elastic but mostly collagenous. Smooth muscle fibers occur very rarely in this layer. T h e submuscularis is the predominating layer of the grayling gas bladder, and it is built up by somewhat irregularly but mainly circularly arranged fibers of mostly collagenous connective tissue. Single elastic fibers are also present. This layer lodges the vascular bundles described above (Figs. 1, 3). - The muscularis in a relaxed gas bladder is thinner than in any other physostomous gas bladder investigated. Its thickness is only about 10 microns and it consists mainly of circular fibers.
T h e outermost part of the muscularis contains longitudinal muscle fibers.
Intermingled with these, longitudinal nerve bundles run from the peri- karya situated in the wall of the pneumatic duct, and from these bundles nerve fibers run to tlie separate muscle fibers of the muscularis. T h e muscle layer is crossed by the vessels which come from the vascular bundles of the submuscularis. As stated before, they often also cross the muscularis together in bundles.
T h e outer layers of the wall of the pneumatic duct are built up in the same way as those of the gas lsladder proper, but the proportional thickness of different layers varies (Fig. 4). An outer layer of connective tissue, continuous with the submuscularis of the bladder, is predominant close to this but becomes gradually thinner nearer to tlie oesophagus.
When the duct enters the wall of the oesophagus, the thin submuscularis runs over into the very thin outer layer of connective tissue of the ali- mentary canal. T h e muscularis of the duct does not undergo the same changes as the subm~~scularis. Continuous with the muscularis of the gas lsladder, it is thicker than this. I t is built up almost entirely by circular smootli muscle fibers, though the outer of these have a tendency to run diagonally. However, no separate outer muscle layer is present. When the pneumatic duct enters the wall of the oesophagus, the muscula- ris unites with the thick muscle layer of the oesophagus. This consists entirely of striated muscle fibers. The muscularis of the pneumatic duct is thinner a t the debouch into the oesopl~agus, and a t the entrance into the bladder its thickness does not exceed that of the bladder muscularis.
T h e striated muscle fibers of the oesophagus, which are mainly circularly arranged, surround the debouch of the duct and may act as a sphincter when contracted. I n intact gas bladders this opening is often seen to be closed. - The lamina ~ r o p r i a of the gas bladder proper is extremely thin. I t consists of collagenous fibers and is only 2-3 microns thick, except where tlie capillaries of the subepitlielial plexus run. No elastic fibers could be found in the lamina propria.
Fig. 2. Tltynzallz~s tlytnallza. Section of gas bladder epithelium. Chief cells and one ciliated ccll. 1500x.
T h e epithelium, which is only light-microscopically investigated, is cubical, sometimes even flattened (Fig. 2). Three cell types are present in the epithelium, one of which are no real epithelial cells but lympho- cytes, invading the epithelium from beneath. T h e lymphocytes are found between the epithelial cells, mostly in a basal position. T h e main part of the epithelium is 11uilt up of cells of cubical type. T h e chief cells are of the size 10 x 10 microns. The nucleus is rounded, rather large and situ- ated centrally or somewllat basally. The cytoplasm is devoid of visible inclusions and stains rather weakly wit11 all sorts of colours. T h e distal part, however, shows a weak basophilia. T h e part of the cytoplasm which
Fig. 3. Thymallus thynzallzls. Transverse section of flat vascular bundle in the submuscularis. 800x.
lies close to tlie subepithelial vessels never sho~vs any ~liffe~entiatioii. The cell membranes are quite uncomplicated laterally and basally, but the distal cell rne~nb'aiie has a I~rush border, probably consisting of micro- villi. T h e other type of epithelial cell differs from the cliief cell mainly in that it has no lsrusli border but instead a tuft of cilia, which stain with silver and have distinct basal Isodies. The ciliated cells are rather un- frequent - about 1 ciliated cell to 25 chief cells in tlie gas bladder proper.
Histochemical tests sliow that tlie iiucleodistal part of the epithelial cells shows a very weak positive reactioii to PARS and paraldehyde- fuchsii~ and reacts negatively to the BEST carmine mctliod. T h e alcian blue method gives a weak but definite reaction in the distal border of the cell. This seems to be limited to tlie distal cell membrane and the brush borclcr. I t could not Ise observed wit11 certainty if this positive reaction comprises not oiily the chief cells but also the ciliated cells.
T h e two inner layers of the wall in the pneumatic duct (Figs. 4, 5), tlie lamina propria and the epithelium, are strongly folded even when the muscularis is practically 1-elaxecl. T h e lamilia propria consists elltirely of collagenous coiinectivc tissue. I t lodges the subepithelial capillary layer. T h e folds of the inner epithelium fill up a large part of tlie lumeli
Fig. 4. Tlymallzrs thymallus. Transverse section of the pneumatic duct. e = epithelium, m = muscularis, s = submuscularis. Note the almost disal~peared lumen, due to
sphincter effect of the muscularis. 80x.
Fig. 5. Tly~~zallzts tlpmalllts. Epitheli~un of the pneumatic ctuct. 1 2 8 0 ~ . of the duct. The folds are sometimes so deep that real crypts are formed.
These are in contact with the central lumen only 1 3 7 narrow canals.
Here too the epithelium is invadecl by lymphocytes. I t consists of co1un1- nar cells, 15-20 microns high ancl 5 microns broad. They are of the the two types known from the gas bladcler proper. Tlle chief cell type has a nucleus, situated in the basal half of the cell. The apical cytoplasm is weakly basophilic and in many cells is seen to differentiate into a cup, similar to that of goblet cells of the intestine. No differentiations could I-Je observed light-microscopically in the basal cytoplasm or in any other part of the cell. The cell membranes seem to be unfolded.
T h e ciliated cell type is found also in the pneunlatic cluct, where it is more common than in the gas bladder proper - one of five cells is of this type and about the same ratio applies along the whole duct. Struc- turally they are similar to the chief cells except that the distal cytoplasm shows still weaker basophilia in the ciliated cells.
T H E GAS BLADDER OF OSMERUS EPERLANUS Topography.
T h e gas bladder of the european smelt, Osm~.rus epe~lnnus, as usual in Salmonoid gas bladders, is an elongated sac, situated dorsally to the peritoneal cavity and connected with the oesophagus by an open canal,
Fig. 6. Ostnc~zls ejerlat~us. Anterior part of gas bladder and oesophagus. Note the blind sac, at the anterior part of which vessels and nervcs reach the bladder.
the pneumatic duct. So it was described by CUVIER and VALENCIENNES (1848). At the side of the pneumatic duct a blind sac from the gas bladder proper protrudes about one mm (Fig. 6 ) . T h e posterior end of tlie gas bladder ends blindly above tlie anus. T h e organ lies veiltrally to the kidneys and is veiltrally covered by tlie cubical, ciliated serous epithelium.
The arterial supply of the gas bladder is mainly furnished by a branch of the coeliaco-mesenteric artery. I t divides on the oesophagus into several branches. Some of the small ones accompany the pneumatic duct and apparently their principal task is to supply only the duct with blood, Other arteries, bigger tliail those along tlie pneumatic duct, run in a ligament, together with some of the nerves to the bladder, to the tip of tlie blind sac protruding at one side of the duct (Fig. 6). There they enter tlie wall of the gas bladder and run along the organ to its posterior end. I t seems that these vessels are the only arterial supply of the gas bladder proper. No brailclies of the go~ladal or ilitercostal arteries or from the-other arteries to the alimentary canal are given off for the gas bladder.
T h e drainage of the gas bladder is effected exclusively by veins belonging to the hepatic portal system. Venous vessels accompaliy all the arteries described above and fuse on the oesophagus to a common vein which empties into the hepatic portal vein.
T h e longitudinal arteries and veins run parallel in the submuscular connective tissue layer of the bladder wall. Irregularly they give off branches in such a way that one artery and one vein always go together.
These pairs of vessels cross the ln~tscularis and enter the lamina propria which is a rather thick layer of connective tissue (Fig. 7). Here the vessels branch into arterioles and venules, and the paired arrangement of the vessels is lost. T h e arterioles and venules split further, and a network of capillaries is formed in the lamina propria.
T h e layers of the wall are the same a s in other pllysostomous gas bladders (Fig. 7). T h e terminology suggested for this type of gas bladder ( F A H L ~ N 1967a) is used here. T h e ventral side of the bladder is covered with the peritoneal epithelium, which consists of cubical, ciliated cells.
T h e outermost layer of the gas bladder wall proper is tlie tunica externa, which contains smooth muscle fibers. I n the posterior part of the bladder the tunica externa is thick and very rich in muscle fibers. Inside this layer follows the submuscularis, a layer of circularly arranged bundles of connective tissue, collagenous and elastic mixed. T h e muscular layer consists of smooth muscle fibers which form a coat around the bladder.
Breaks in this coat, due to the passage of vessels, do occur but are not
Fig. 7. Osmerus efierlanzls. Transverse section of the gas bladder wall. e = epithelium, 1 = lamina propria, m = muscularis, s = submuscularis, v = blood vessels. 160x.
Fig. 8. Osn~eizrs e)erlnnzis. Section of gas bladder epithelium. Chief cells with the apical cup visible it1 niost of thcm. 900x.
frequent. I n the posterior part of the gas bladder, the muscularis consists almost wholly of circular fibers, which form a 20-30 microns thick layer. Loilgituclinal muscle fibers are rare here and are arranged in bundles outside the circular coat, mainly along the big vessels. I n the middle of the bladder, the circular muscle coat is soniewhat thicker, and the longitudinal fibers have increased in number and form on the ventral side an allnost complete layer. O n the dorsal side they are still single bundles. I n the anterior part, the circular layer has not increased in thickness, but the longitudinal fibers now form an almost continuous layer outside the circular one and about as thick as this. I n the blind sac, the muscle coats lose their limitations and lsecolne mixed up with one another. I n the pneumatic duct the muscularis first becomes thinner, but when the duct enters the vial1 of the oesophagus it is surrounded by a muscle coat, 100-150 micro~ls thick and consisting mainly of circular smooth muscle fibers (Fig. 13). Furthermore, striated muscle fibers of the muscularis externa of the oesophagus are arranged circularly around the mouth of the pneumatic duct.
T h e lamina propria in the gas bladcler of tile smelt has a considerable thickness, about the same as the muscularis. I t consists of -connective tissue, mainly collagenous fibers, irregularly arranged. Intermingled
