ICES CM 1999/U: OS- Theme session U:
"l\1-74 SYNDROME AND SIMILAR REFRODUCTIVE DISTURBANCES IN l\1AIUNE ÅNlMALS"
Some possible explanations to Baltic cod (Gadus morhua L.)
reproduction disturbances with special emphasis on lipids- an overview
Jana Pickova1, Per-O lov Larsson2 and A.nders Kiessling3
1 Departrnent ofFood Science, SLU, P.O. Box 7051, S-750 07 Uppsala, s~'eden,.
2Institute of Marine Research, P,O,Box 4, S-453 21 Lysekil, Sweden;
1. 'a l , o • , ro o T o ~ ... l o ... • -,. T , . . . , . . " • -.. ..- • T • -,. T
- lVlatre Aquacutture ::itanon, lnsntute or !Vlanne Kesearcn, 1~-)'1~4 MatreaaJ, Norway.
Abstract
Disturbances in Baltic cod reproduction, additional to the basic problems related to low salinity and oxygen content, are discussed. Abnonnal cod embryos appeared first in 1979 and have been observed since, Still recruitment has been relative! y we!! correlated to the
"reproduction voiume" (sufficient saiinity and oxygen content) untii year-dass i 991. Since that year, year~class strengths have been lov.rer than expected considering available
reproduction volurne. Many experimental investigations on Baltic cod reproduction have shown a lower hatching success compared to other cod stocks. Simultaneously \vith cod, other fish species in the Baltic Sea have experienced reproduction problems. Several hypotheses regarding the causes of the reproductive disturbances are reviewed, inciuding a
mis~match ofhatching an.d environn1ental factors, including food avai1ability and predator abundances. Also the impact of xenobiotic substances on peroxidation of unsaturated li pi ds (polyunsaturated fatty acids and cholesterol) as well as reactive intennediates, as D1",JA adducts, and their effects on the quality of spawning products are discussed. Also other fatty acid xenobiotic interactions are highlighted. Insufiicient hormone ievei for induction of maV..rration a...~d spa,'1~TJ.ng, causing a delay in spa'-:vning activities, is a1so suggested to be caused by anthropogenic substances. We conclude that the causes of reproductive problems in Baltic Sea cod ittclude factors other than overfishing and salinity - oxygen interactions.
Key words: Baltic Sea, egg quality, fatty acids, Gadus morhua, larva! quality, lipid oxidation, xenobiotics
Fishery and other mortalities
Several investigations showing a decreased reproductive success in the Baltic cod popuiation (Grauman and Sukhorukova 1982, Westernhagen et al. 1988, reviewed by 1"-!orrgren et al. 1998) have been performcd during the 1980 - 90s. A strong decline in the population size from the mid 1980s until today is partly caused by poor management resulting in over-fishing. The peak yearly catch was approximately 400,000 tonnes in i984.
The v~..riation of population size is large, lo·v.;est yearly catch being about 45,000 toP ... '1es in the iatest years (i 993, Figure l), partly due to the impact of low salinity and often
restrictingly lovv oxygen content. Baltic cod is an important resource gi ving the most important fishery in many Baltic countries. The Baltic cod population consists oftwo stocks, the eastern Baltic stock which is the larger both in size and space and a western stock (Brander 1994). A. reproduction volu..rne, defined as the 'vater volume having sufficient ieveis ofsaiinity (>ca il.5 psu) and oxygen (>ca 2 ml/1) (Larsson 1994), detennines to a high degree the year-class strcngth ruJ.d subscqucnt recruitrr1ent of Bal tie cod. Since 1991 the relation between renroduction volume and corresoondimr vear-cla.'" .... .._ ' - ' ,.1 - -- - - - -
strength has bee.n changed, wii.h generally smaller year-dasses than expected (Larsson i994;
reviewed by Norrgren et al. 1998).
Simultaneously "vith the low recn1ittucnt sincc 1991 a dclay (approximately tv..·o n1onths) of the peak of and spreading in time of the spawning was observed (Wieland 1995).
Larsson (1996) discussed ifthis shift in tnnmg cuuld have led io an increased mortality by deteriorating enviro11ment e.g. lower oxygen content and higher temperatures later in the summer and faii, andior increased predation, e.g. high abundance of medusae during late sun1rner, fu'1d!or lovv food availability during the cod larvac first fccding. He found no conclusive evidence for effects on cod larvae morta1ity by any ofthese factors. Also the quality of the food available has to be considered as stressed by Beil and Sargent (1996) based on li p id and fatty acid composition of p!ar1kton during different periods. The y suggest the content of essentiai fatty acid in different plankton species to be of importance.
It has been suggested (Nissling and Vallin 1996) that a low proportion oflarge females in the present Baltic cod population is detrim.ental for the reproducbve success. Tnis should be due to larger cod females ha ving a higher fecundity tha..TJ. first time spawners and at least in some species iarger eggsiiarvae (generaiiy from iarger femaies) have a higher survivai expectancy (e.g. } .. 1iller et al. 1988; see ho\.vever belov;). On the other hand the proportion oflarge, older females is mainly determined by relative size ofyear-classes. In Figure 2 the relation between proportion of older fen1ales ( 5+) in the spaw11ing stock and the
subsequent recruitment for the yearclasses 1979- 1996 is sho'Nll. The regression of
recruitmem on proponion o id femaies is very poor (r' = 0.02 )for the period chosen, which at least sho\vs that there are other important factors involved in the recn1itment process.
Possible explanations for the spawrling tin1e shift could be an alteration in endocrine honnone levels caused by un_k_nown factors3 as for example in_hibition of prostaglandins
and/or steroid hormones by hormone-like substa.ticeS.· Also impact on spawning behaviour by hormone-like substances and poiiutants are suggested (reviewed by Jones and Reynoids - - 1997).
Simultaneously with cod, other fish species in the Bal tie Sea have experienced reproduction problems. For example the M74 syndrome in Baltic salmon (Salmo sa/ar) and totally faiiing reproduction of pike (Esox iucius) and perch (Perca ;7uviatiiis) in some coastai areas substances have been reported in the Baltic Sea (reviewed by Norrgren et al. 1998).
Egg quality
During 1992-1997 several attempts were done to culture Baltic cod for experimental and research purposes in Denmark, Germany and Sweden (Buclunan et aL 1993, 't.Jissling and Westin 1991, Pickova and Larsson 1992). Several studies indicated that Baltic cod eggs have a higher frequency of irreguiar eariy biastomere cieavages foiiowed by iower hatching
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observed that the Baltic cod eggs had dramatically lower hatching rates than the eggs from the Barent Sea. Investigations on proiisl inft:ctions in Bal
tie
cod eggs (Pedersen et al. 1994, KjOrsvik et al. 1999) did not sho'v ar1y dra...'!latic effects on egg and la...rval survivaLThe suggestion abovc by }~issling and Vallin (1996) that relatively fe\ver large, old cod females in later years re sult in overall higher mortality of larvae, is based on the assumption that larger larvae from larger eggs have a higher survival. This conclusion can however be discussed. In a study on haddock (}..!elanogrammmus aeglefinus) Trippel et aL (1999) showed that total dry matter and totai iipid composition did not affect egg quaiity.
size in late season eggs but the survival oflarvae was not affected. These studies are in contrary to the suggestion ofNissiing and Valiin. The conclusions in their study are based on the lengt..h of larval survival prior to first feeding. This method can be discussed since no investigation on point of no return was performed and does therefore not evaiuate survivai during U"'le important stage until fccding has succeeded.
The large importance of fatty acid composition for successful early developn1ent has been shown in
ma.11y
fish species a.11d was reviewed by Sargent et aL (1995) and Wiegand (1996).Pickova et ai. (i 997) investigated fatty acid composition of eggs from different cod stocks.
correlated to a lower hatching rate and higher degree of blastomere cleavage asymmetri es. In addition, a higher content of docosahexaenoic acid (DHA, 22:6n-3) was found in those eggs.
Since DHA is the most unsaturated fatty acid~ its sn~ceptibility to peroxidation is the highest (Cosgrove 1987). Simiiar resuiis in fatty acid composition affecting survival were
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Impact oftoxic substances on reproduction offish and larva! survival by hormone-!ike subsiances and direct toxiciLy is well recognised (reviewed by Kime 1995). The load of known and U!l_k_nown anth..ropogenic substances has been frequently discussed in connection with Baliic cod reproduction. A study by Petersen et ai. (i 997) indicates that there is a
correlation in eva.."'"'; burdens of lipophilic xenobiotics
vvith i.a. cod egg and larval
survival.This might also be tbe most plausible explanation for the increase in DNA adducts observed in Baltic· cod at early life stages as suggested by Ericson et al. (1996).
lmpact of xenobiotics on !ipid quality
\Ve suggest that lipids have to be considered to a higher degree as they are lhe ffaction which is not only carrier of the halogenated substances but as a fraction which \Vill get seriously affected by those. Chiorinated fatty acids have been detected in Baitic fish species (\Vesen et al. 1995) .. Same shorter chlorinated fatty acids, probably as results of~
oxidation seem to be stable and therefore
it
was conduded in Wesen et al. (1995) that they are able to disturb the reproductive processes. Despite an overaii decrease in PCB ioad it\vas sho\vn that coplanar PCBs have .increased in salmon tissue (revicwcd by }.J orrgren et al. 1998). The polyunsaturated fatty acids eicosanoid fatty acid and arachidonic fatty acid are precursors of eicosanoids which are the base for prostaglandins and other biologicaliy importønt molecules (Sargent et all995). Merc-ure an.d Van Der Kraak (1995) have
shov·.rn
ihat different fatty acid content influence steroid hormone production in te1eosts. In a study on arachidonic acid !vfercure and V an Der Kraak ( 1996) concluded that it stimulated testosterone production and this action was mediated by prostaglandin (PGE-2).Cholesterol is a base of all steroid honnone synthesis Hl fish as well as 1n rnarnmals (Teshima 1990). Peroxidation of unsaturated fatty acids and of cholesterol resu!ts in toxic products which are harmfui to the organisms (Pettersson and Ligneii 1996, Pickova 1998).
In addition, the highly polyunsaturated fatty acids are L.,e most susceptible to oxidative reactions (Cosgrove et al. 1987) and tberefore tbe molecules which usually initiate the free radical induced chain reactions. Therefore to understand. the ro le of lipid based hormonal complex ønd lipoproteins in the reproduction of fish in relation to xenobiotics has significance nor o ni y for fish but aiso for the iower animais in the Baitic Sea food chain.
Further, it has been sho\vn that polychlorinated biphenyls (PCBs) are able to cause cl'illnges in lipid metabolism by changing fatty acid composition in livers of different animals
(Borlakoglu et al 1990, Krunei et al. 1996, ~vfatsusue et al 1997). In experirnents groups treated by injection of PCB showed an increased !ino!enic acid (18:3n-3) proportion in al!
glycerophosholipids of liver. On the other hand the content of arachidonic acid decreased significan.tly. Changes in the activity of desattrrase isozymes have been postulated to exp1ain this unusuai lipid metabolism and also its contribution to toxicity (Matsusue et al.
1997). In geneial a decrease in antioxida11t levels is observed in fish exposed to PCBs, dioxins and other halogenated substances (Otto and Moon. 1996; Winston and Di Giulio 1991). in a pre1iminary study on Arciic charr (Salvelinus alpinus) fed with diet added the
c.ommercial PCB mixture .Aroclor 1254, \Ve fou..11d a different fatty acid composition of the
liver when compared to the contro1 group t1sh (own unpublished results).Conclusions
IViany different factors have been investigaied in order to explain the low reproductive
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been identified. Many studies indicate that factors other than expioitation, saiinity and oxygen are influencing reproductive succcss. The free radical induced peroxidation, combined with a !ow antioxidative defence might well be one of the underlying factors.
Other effects ofiipid- haiogenated xenobiotic interaction might also be ofitnportance. \Ve suggest that maturation and spawning of cod in the Baltic Sea are also influenced by the load of anthropogenic substances. It can be conciuded that human activities resuiting in environ1nental pollution are involvcd in the reproductive disorders in Baltic fish species.
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l \1 l l l l I.l l l
nl l l l
nl l l
700
l l --- l
ouul l l --- t
bUUl l - t l
400l li l li
- . - l
~l l l IJ"'J l l l l l l l l l l l l l Ill
300"C
o
?ft
10
tn tl..l l l /1
~l l l l l l l l l l l l
li l rN___J 1 1 \ l l l l l l l l l l n l l l li
li l l l l l l l l l l n l l l l l li
i
o ~ li l l
19[l l l l l kl l rq l l l l l l l l l l l l l l l l l l l l l
nl l l l l l l l li+
200li l l l l l l 1\ l l l l l 11
~l l l l l l l l l li
li l l l l l
li M+kJ ~hl N-1 I.l li l
Jl li
- li l l l l l l ...11 li+
100b
tl l l l l l l l
1~11li l l l l l l l l l l 1"'1 l l l l l l l l l l l l l l li li l l l l l l l l l l l l l l l l l l l l l l l l l l li - l l l l l l l l l l l l l l l l l l l l l l l l l l l l li
u l " ' ' l l l l l: l l l l l l ' l l : l l l l ' l l l l l l l l l' l l l l l l l l l l
o
1979 19_1 1983 1985 1987 1989 1991 1993 1995 1997
Figuie 2. Pioportion of old (5+) fer-nales of spawning stock and subsequeni recruiimeni 1979 - 1996 of Baltic cod, eastern stock. Data from ICES Baltic Fisheries Assessment \.''Jorking Gmup reports.
o
..-><
:::
U) :l....
I.l (!)
