Pheno ypic plas ici y in g ow h and ecundi y induced by
s ong popula ion luc ua ions a ec s ep oduc i e ai s o
emale ish
Juha Ka jalainen
1
, Olli U panen
1,2
, Tapio Keskinen
1,3
, Hannu Huuskonen
4
, Jouko Sa ala
5
,
Pen i Valkeaj€
a i
3
& Timo J. Ma jom€
aki
1
1
Depa men o Biological and En i onmen al Science, Uni e si y o Jy €
askyl€
a, P.O. Box 35, Jy €
askyl€
a FI-40014, Finland
2
Me s€
ahalli us, Jy €
askyl€
a, P.O. BOX 36, Jy €
askyl€
a FI-40100, Finland
3
Na u al Resou ces Ins i u e Finland, Su on ie 9A, Jy €
askyl€
a FI-40500, Finland
4
Depa men o Biology, Uni e si y o Eas e n Finland, P.O. Box 111, Joensuu FI-80101, Finland
5
Depa men o Biology, Sec ion o Ecology, Uni e si y o Tu ku, Tu ku FI-20014, Finland
Keywo ds
Age o ma u a ion, co egonids, emb yonic
de elopmen , ishe ies, la al de elopmen ,
ma e nal e ec , s ock luc ua ions.
Co espondence
Juha Ka jalainen, Depa men o Biological
and En i onmen al Science, Uni e si y o
Jy €
askyl€
a, P.O. Box 35, Jy €
askyl€
a FI-40014,
Finland.
Tel: +358405134865;
Fax: +35814617239;
E-mail: [email p o ec ed]
Funding In o ma ion
This wo k was inancially suppo ed by he
Minis y o Ag icul u e and Fo es y and
Finnish Cul u al Founda ion/Cen al Finland.
Recei ed: 18 June 2015; Re ised: 7
Decembe 2015; Accep ed: 9 Decembe
2015
Ecology and E olu ion 2016; 6(3):
779–790
doi: 10.1002/ece3.1936
Abs ac
Fish a e known o hei high pheno ypic plas ici y in li e-his o y ai s in ela-
ion o en i onmen al a iabili y, and his is pa icula ly p onounced among
salmonids in he No he n Hemisphe e. Resou ce limi a ion leads o ade-o s
in pheno ypic plas ici y be ween li e-his o y ai s ela ed o he ep oduc ion,
g ow h, and su i al o indi idual ish, which ha e consequences o he age
and size dis ibu ions o popula ions, as well as hei dynamics and p oduc i -
i y. We s udied he e ec o plas ici y in g ow h and ecundi y o endace
emales on hei ep oduc i e ai s using a se ies o long- e m incuba ion
expe imen s. The wild pa en al ish o igina ed om ou sepa a e popula ions
wi h ma kedly di e en densi ies, and hence na u ally induced di e ences in
hei g ow h and ecundi y. The ene gy alloca ion o soma ic issues and eggs
p io o spawning se ed as a p oxy o o al esou ce a ailabili y o indi idual
emales, and i s e ec s on o sp ing su i al and g ow h we e analyzed. Vendace
emales alloca ed a a he cons an p opo ion o a ailable ene gy o eggs (pe
body mass) despi e di e en g ow h pa e ns depending on he o al esou ces
in he di e en lakes; in es men in o eggs hus dic a ed he sha e emaining
o g ow h. The ene gy alloca ion o eggs pe mass was highe in young han in
old spawne s and he egg size and he ela i e ecundi y di e ed be ween hem:
Young emales p oduced mo e and smalle eggs and la ae han old spawne s.
In con as o ea lie obse a ions o salmonids, a sho age o ma e nal ood
esou ces did no inc ease o sp ing size and su i al. Vendace emales in spa se
popula ions wi h ample esou ces and high g ow h p oduced la ge eggs and
la ae. Vendace accommoda e s ong popula ion luc ua ions by hei high plas-
ici y in g ow h and ecundi y, which a ec hei o sp ing size and conse-
quen ly hei ec ui men and p oduc i i y, and accoun o hei pe sis ence
and esilience in he ace o high ishing mo ali y.
In oduc ion
Pheno ypic plas ici y occu s when he pheno ype
exp essed by a gi en geno ype changes as en i onmen al
condi ions a y (Nussey e al. 2007). Fish a e known o
hei high pheno ypic plas ici y in many li e-his o y ai s
in ela ion o en i onmen al a iabili y, and his is pa ic-
ula ly p onounced among salmonids (Salmonidae) in he
No he n Hemisphe e (Skulason and Smi h 1995). T ade-
o s in pheno ypic plas ici y be ween li e-his o y ai s
ela ed o he ep oduc ion, g ow h, and su i al o indi-
idual ish may ha e consequences o he age and size
dis ibu ions o popula ions, as well as hei dynamics
and p oduc i i y (S ea ns and Koella 1986; Heino e al.
2002). Age and size a ma u a ion o ishes wi h mode -
a e- o-high ecundi y, high age a ma u a ion, and low
ª2016 The Au ho s. Ecology and E olu ion published by John Wiley & Sons L d.
This is an open access a icle unde he e ms o he C ea i e Commons A ibu ion License, which pe mi s use,
dis ibu ion and ep oduc ion in any medium, p o ided he o iginal wo k is p ope ly ci ed.
779
p ema u a ion su i al ha e been widely s udied using
he eac ion no m app oach (Heino e al. 2002; E ans
e al. 2010; Jonsson e al. 2012; Kokkonen e al. 2015).
Those species ha e high a ia ion in age and size a ma u-
a ion ela i e o ce ain salmonid species, such as en-
dace (Co egonus albula (L.), Fig. 1), wi h ea ly
ma u a ion, high ep oduc i e e o , small size, sho li e
span, high demog aphic esilience, and low ju enile su -
i o ship (Ka jalainen and Viljanen 1994). Fu he mo e,
g ow h o endace is s ongly dependen on he popula-
ion densi y due o in aspeci ic ood compe i ion (Vilja-
nen 1986; Helminen e al. 1992; Ma jom€
aki and
Ki jasniemi 1995; Au inen e al. 2000), so ha he we
mass o imma u e ish a e he i s g ow h season can
a y by as much as ou old be ween successi e yea s
(Helminen e al. 1992).
In endace popula ions, in e coho compe i ion has
been p oposed o induce a quan i a i e ma e nal e ec on
o sp ing quali y du ing he g owing season p io o
spawning (Ham in and Pe sson 1986). This in e ac ion
can be illus a ed by he ollowing chain o associa ion:
High young-o - he-yea abundance causes se e e ood
compe i ion be ween young-o - he-yea and ma u e ish
which leads o slow g ow h and weakened condi ion o
ma u e ish wi h de e io a ion in some essen ial quali y o
quan i y componen s in he eggs. Rep oduc i e p oduc s
o poo quali y will lead o a coho e ec o low su i al
o emb yos o la ae, and hus less success ul ec ui men
o he nex yea class. Fu he , a high mo ali y o en-
dace due o in ensi e ha es ing will simpli y he age
s uc u e o he spawning popula ion om a mul icoho
i e opa ous s a e o an almos o ally single-coho semel-
pa ous s a e and main ains he induced 2-yea gene a ion
cyclici y in he popula ion dynamics (Ham in and Pe s-
son 1986) as well as he g ow h o indi idual ish (Helmi-
nen and Sa ala 1994). Thus, ha es ing may signi ican ly
adjus he ep oduc i e ai s o indi iduals and popula-
ions in endace, ou model species.
Vendace is a special case among i e opa ous ishes,
because he age a he i s ep oduc ion o emales in
many endace s ocks has e y li le a ia ion: Almos all
emales spawn o he i s ime in hei second au umn
(young, no ice spawne s a age o 1+) (Ham in and Pe s-
son 1986; Huusko and Hy €
a inen 2005), and only a small
p opo ion o hem su i e o epea spawning in he ol-
lowing yea s. Howe e , some endace popula ions wi h
highe and mo e a iable age a ma u a ion a e also
known (G ege sen e al. 2011), and he spawning expe i-
ence and age o a emale may ha e a signi ican e ec on
he ep oduc i e success o ish (Kamle e al. 1982; E ans
e al. 1996; Busch e al. 2009).
We s udied he e ec o plas ici y in g ow h and ecun-
di y o endace emales on hei ep oduc i e ai s using a
se ies o long- e m incuba ion expe imen s. The wild pa -
en al ish o igina ed om ou sepa a e popula ions wi h
ma kedly di e en densi ies and hence lake-speci ic na u-
ally induced di e ences in hei g ow h and ecundi y. We
in e p e ed he e ha he la ge di e ences in g ow h o pa -
en al ish we e mainly caused by hei pheno ypic plas ici y
in esponse o he popula ion densi y, and al hough local
adap a ions may e ol e in ish popula ions apidly (Eiza-
gui e e al. 2012; Wes ley e al. 2012), hei ole in ou
analysis is insigni ican . The ene gy alloca ion o soma ic
issues and eggs p io o spawning ( a iable P
S+R
) se ed as
a p oxy o o al esou ce a ailabili y o an indi idual
emale, and i s e ec s on o sp ing su i al and g ow h
we e analyzed. Fi s ly, we examined whe he he P
S+R
di -
e ed be ween he emales om he di e en lakes, he ela-
i e p io i y o g ow h and eggs in he ene gy alloca ion by
young and old spawne s, and how he P
S+R
a ec ed he egg
p oduc ion ( ela i e ecundi y, egg size) o emales. Sec-
ondly, di e ences in su i al and g ow h o o sp ing om
young and old spawne s wi h di e en P
S+R
we e s udied
using common ga den e iliza ion and incuba ion expe i-
men s. Sho age in ma e nal ood esou ces has been
obse ed o inc ease he egg size ia a ade-o be ween egg
numbe and size and subsequen ly o a ec o sp ing size
and su i al (Hu chings 1991). Finally, we explo ed
whe he he alloca ion mechanisms e ealed by ou expe i-
men s can explain he high a iabili y in he ec ui men o
endace in ou s udy lakes.
Ma e ials and Me hods
S udy lakes and popula ions
Ma u e endace o p o ide eggs and mil we e caugh
om ou Finnish lakes: Pyh€
aj€
a i (I), Pyh€
aselk€
a (II),
Puula esi (III), and Sou he n Konne esi (IV); he ea e
he lakes a e e e ed o by hei oman nume als I–IV.
The lakes we e selec ed o ep esen he wide ange o
Figu e 1. Ou s udy species endace (Co egonus albula (L.)).
Pho og aph by Jussi Mu osaa i.
780 ª2016 The Au ho s. Ecology and E olu ion published by John Wiley & Sons L d.
Pheno ypic Plas ici y in G ow h o Female Fish J. Ka jalainen e al.
endace popula ion densi ies in Finland: The densi y o
he ma u e adul (age ≥1+) endace in 2004–2006 anged
om abou 20 o 4000 indi iduals ha
1
in au umn, and
he o al biomass o endace in au umn anged om 12
o 42 kgha
1
(Table 1). The densi y es ima es we e based
on he emo al me hod (Helminen e al. 1993) and
coho analysis (Pope 1972) in he in ensi ely ished Lake
I and combined esul s o echo-sounding and CPUE in
Lakes III and IV (Ma jom€
aki & Huolila 1995; Valkeaj€
a i
and Ma jom€
aki 2013). Da a o adul ish om Lake II
we e sca ce, and age-speci ic densi y es ima es we e no
a ailable o he s udy yea s. Howe e , om o al ca ch
s a is ics i s densi y was oughly es ima ed o be he sec-
ond lowes . Fishing mo ali y di e ed be ween lakes being
highes in Lake I (Table 1, Appendix S1), which is shal-
lowe and mo e p oduc i e han he o he lakes and has a
longe open-wa e pe iod han he o he lakes
(Appendix S1).
The annual popula ion ecundi y was calcula ed by
mul iplying emale (sex a io assumed o be 1:1) spawn-
ing s ock densi y (ind. ha
1
) by he mean ecundi y
(eggs emale
1
) o ma u e emales in each lake. The
densi ies o newly ha ched la ae o endace (ind. ha
1
)
in sp ing 2004–2007 we e es ima ed o all lakes using a
s a i ied sampling design (U panen e al. 2009).
Ene gy alloca ion by emale endace o
soma ic g ow h and eggs
To al ene gy alloca ed o soma ic g ow h and eggs (P
S+R
)
du ing he g owing season (kJg
1
o ish we mass) was
es ima ed om andomly sampled ipe emales (eggs no
unning). To al leng h (mm) and we mass (g) o hese
emales we e measu ed. Bo h o a ies we e emo ed and
weighed o he nea es 0.01 g. Th ee subsamples aken
om di e en pa s o he gonads we e weighed, and he
numbe o eggs pe subsample was coun ed unde a dis-
sec ing mic oscope. Mean egg numbe o he subsamples
was mul iplied by he a io o he o al sample mass o
he mean subsample mass o ob ain an es ima e o abso-
lu e ecundi y o each emale. Vendace is a de e mina e
and o al spawne species: The whole clu ch o de eloped
oocy es is laid down du ing a single pe iod wi h no u -
he ec ui men o oocy es be o e he s a o spawning
(Dlugosz and Wo niallo 1985; Mu ua e al. 2003). Thus,
he oocy e numbe p io o spawning gi es an adequa e
es ima e o he o al indi idual ecundi y (Kjesbu e al.
2010) which makes i possible o es ima e he o al ene gy
alloca ed o ep oduc i e issue. In ou analysis, P
S+R
was
assumed o e lec he le el o ma e nal ood esou ces
(indi ec ly) and g ow h condi ions (di ec ly), and he
in e annual a ia ion in popula ion densi y induced he
a ia ion in P
S+R.
Rela i e ecundi y o emales was calcula ed by di iding
absolu e numbe o eggs by o al mass o ish including
gonads (W
T
, we mass). One subsample o un e ilized
eggs om each emale was ozen a 80°C o he de e -
mina ion o he ene gy con en o eggs by hei ca bon
con en . Th ee pooled ( i e eggs) eplica es om each
emale we e weighed and eeze-d ied and hen g ound o
a ine powde using a mo a and pes le. App oxima ely
0.6 mg o powde ed sample was weighed in o a small in
cup o he ca bon analysis. Analyses we e ca ied ou
using a FlashEA 1112 elemen al analyze connec ed o a
Table 1. Cha ac e is ics o endace popula ions [mean (SD)] in he s udy lakes in 2004–2007. We mass o emales a e i s yea in second
sp ing was es ima ed om he scale by he Monas y sky’s equa ion (Monas y sky 1930).
Lake I Lake II Lake III Lake IV
SW Pyh€
aj€
a i Pyh€
aselk€
a Puula esi S Konne esi
To al ca ch, kgha
1
13 (1.0) 1 (0.2) 4 (0.5) 3 (0.5)
To al mo ali y, % >90 –50 50
To al densi y o spawne s, ind. ha
1
157 (116) –1072 (353) 2770 (834)
To al biomass o spawne s, kgha
1
10 (6) –15 (4) 18 (5)
Densi y 0+in au umn, ind. ha
1
1063 (265) –953 (715) 1541 (1610)
Biomass 0+in au umn, kgha
1
20 (9) –4 (3) 4 (4)
To al biomass in au umn, kgha
1
30 (10) –19 (5) 22 (9)
We mass o 1-yea old emales, g 29 (8) 8 (3) 4 (1) 3 (2)
We mass o no ice emales, g 78 (22) 25 (6) 11 (2) 9 (5)
We mass o epea ed spawne s, g 127(48) 34 (10) 19 (5) 10 (3)
To al leng h o all ma u e emales, mm 216 (24) 155 (18) 124 (14) 112 (23)
Fecundi y o ma u e emales, eggs 9791 (3966) 3593 (1317) 1739 (714) 999 (333)
% o ma u e indi iduals a age 1+99 (1) 98 (2) 100 100
% o no ice spawne s 84 (9) 58 (36) 40 (45) 45 (32)
Densi y o ha ched la ae, ind. ha
1
5865 (4590) 1520 (1021) 8726 (7038) 22105 (26036)
–=no da a a ailable.
ª2016 The Au ho s. Ecology and E olu ion published by John Wiley & Sons L d. 781
J. Ka jalainen e al. Pheno ypic Plas ici y in G ow h o Female Fish
The mo Finnigan DELTAplus Ad an age mass spec ome-
e . Ca bon con en was ans o med o he ene gy con-
en using a coe icien o 44.9 kJg
1
C (M. Paala uo, P.
Muje & J. Ka jalainen, unpublished da a).
Age o emale endace was de e mined om he scales
and o oli hs (sagi ae), and he adius o each annulus in
he scales was measu ed. Leng h a age 1, he beginning
o he las g owing season, was back-calcula ed using
Monas y sky’s equa ion (Monas y sky 1930), and he
alue o he exponen (b=0.607) was de e mined om
ou own da a (n=817).
To al ene gy alloca ed o soma ic g ow h and eggs
(P
S+R, i
,kJg
1
) was es ima ed indi idually o each
emale (i)
P
S+R, i
=(W
T, , i

^
W
S, 1, i
)*E
i
/Ẅ
1 , i
whe e
W
T, , i
=obse ed o al we mass a ime o emale i,
^
W
S, 1, i
=es ima ed soma ic we mass a he begin-
ning o he las g owing season, a ime 1,
E
i
= he g oss ene gy con en es ima e (kJg
1
)o
emale i.
Ẅ
1 , i
=mean weigh o he emale idu ing he las
g owing season.
Es ima ed soma ic we mass a ime 1is
^
W
S, 1, i
=a*

L
1, ib
*[W
T, , i
/(c*L
, id
)]
whe e

L
1, i
=back-calcula ed leng h o emale ia 1,
L
, i
=i s obse ed leng h a ,
aand ba e he in e cep and he slope o log-linea
eg ession o soma ic we mass (W
S,
) on o al leng h
(L
,
) o emale endace (a=0.0000044, b=3.06,
R
2
=0.98, n=461), espec i ely, and
cand da e he in e cep and he slope o log-linea
eg ession o o al we mass (W
T,
) on o al leng h (L
)o
emale endace (c=0.0000051, d=3.09, R
2
=0.98,
n=461), espec i ely.
The mean mass o he emale idu ing he las g owing
season is
Ẅ
1 , i
=(W
T, , i
+
^
W
S, 1, i
)/2
E
i
= he g oss ene gy con en (kJg
1
) o emale iis
based on i s Ẅ
1 , i
.
E
i
was es ima ed om log-linea eg ession be ween
g oss ene gy con en and W
T
o age >0+ endace
(R
2
=0.937, n=861, M. Paala uo, P. Muje & J.
Ka jalainen, unpublished da a):
E
i
=4.231 *Ẅ
1 , i0.112
Ene gy alloca ion o eggs (P
R,i
,kJg
1
) is es ima ed om
P
R,i
=(F
i
*E
a
)/Ẅ
1 , i
whe e
F
i
=indi idual absolu e ecundi y and
E
a
=mean ene gy con en o egg a gi en age g oup a,
and was de e mined o each age g oup om e e y lake
and yea om he ca bon con en o he eggs.
Fe iliza ion and incuba ion expe imen s
The expe imen s we e ca ied ou simila ly in all pe iods
2004/2005, 2005/2006, and 2006/2007. All ish we e caugh
by local ishe men in he middle o he spawning season
om he las week o Oc obe o he i s week o No em-
be . Fish we e caugh wi h ap ne s (Lake I), gill ne s
(Lake II), and seine ne s (Lakes III and IV) and be o e he
e iliza ion ish we e kep a he same empe a u e as he
wa e empe a u e in he spawning a ea (2–3°C). Only li e
indi iduals om he ca ch wi h unning mil and eggs
we e used o he e iliza ion expe imen . Annually in
each popula ion, 9 eady- o-spawn emales and 27 males
we e picked om a andom sample o ca. 100 ma u e ish
(Appendix S2). Bo h young (1+) and old spawne s (>1+)
we e included in he e iliza ions. L
T
and W
T
o each ish
we e measu ed be o e emo ing he eggs and mil o he
e iliza ion. Fe iliza ion was pe o med immedia ely a e
ish we e caugh in he well-s ocked ield labo a o y es ab-
lished in a an. F om each emale, h ee se s o a mini-
mum o 100 eggs we e s ipped in o plas ic Pe i dishes.
Each se was e ilized wi h a mix u e o mil om h ee
males o ensu e su icien mil and o simula e he com-
munal spawning in na u e. A e adding he mil , a small
olume o lake wa e was added o he dishes o ac i a e
he spe m and he dishes we e gen ly wa ed o sp ead he
spe m uni o mly. The dishes we e placed in one-li e plas-
ic bags wi h lake wa e a 2–5°C and anspo ed wi hin
2–4 h o a ha che y a he Konne esi Resea ch S a ion o
he Uni e si y o Jy €
askyl€
a, whe e he se s o eggs we e
dis ibu ed in o incuba ion pla es in andomized o de
and incuba ed in ac ylic plas ic pla es (5 95 cm) wi h
gen le con inuous e ical wa e low h ough hei mesh
bo om.
Fe iliza ion success o eggs, ha is, he p opo ion o
e ilized eggs o all eggs ( andom sample o 50–100 eggs
pe se ), was de e mined 24–48 h a e e iliza ion unde
a dissec ing mic oscope. Fe ilized eggs we e iden i ied by
isible cell di ision. Fungal g ow h was con olled by
weekly ea men wi h malachi e g een un il he emb yos
eached he eyed s age. Dead eggs we e coun ed and
emo ed weekly and wa e empe a u e eco ded daily
h oughou he incuba ion pe iod. Mean (SD) wa e
empe a u es du ing incuba ions we e 3.0 1.1,
3.2 1.0 and 2.7 0.7°C du ing he incuba ion pe iod
in 2004/2005, 2005/2006, and 2006/2007, espec i ely. The
o al du a ion o he incuba ion pe iod in di e en yea s,
om e iliza ion o 90% ha ching, was 170–196, 164–
184, 171–194, and 171–195 days o eggs om Lakes I, II,
III, and IV, espec i ely.
The ins an aneous o al mo ali y (Z) o emb yos and
la ae du ing expe imen s was calcula ed sepa a ely o
each egg and ea ing se :
782 ª2016 The Au ho s. Ecology and E olu ion published by John Wiley & Sons L d.
Pheno ypic Plas ici y in G ow h o Female Fish J. Ka jalainen e al.
Z=ln (N
e
/N
b
),
whe e N
e
= he numbe o li e emb yos o la ae a he
end o a pe iod and N
b
= hei numbe a he beginning
o ha pe iod. A mean Z o each emale was calcula ed
as a mean o he h ee eplica es (egg se s), and popula-
ion-speci ic es ima es we e calcula ed as a mean o he
nine emales. Mo ali y a es we e calcula ed sepa a ely
o wo pe iods: Z
F
= e iliza ion ailu e and Z
E
= o al
emb yonic mo ali y om e iliza ion o 100% ha ching
(including Z
F
and Z
L
). Values o p opo ional o al mo -
ali y (A, %) we e calcula ed om
A=1–exp(-Z).
The p opo ion o ha ched la ae ali e (H%) was also
eco ded.
The mean egg we mass o each o he nine emales
pe lake was measu ed om 50 eggs (Appendix S2). Du -
ing he ha ching pe iod, he numbe o dead eggs and
ha ched la ae was eco ded daily. One subse (n=10) o
ha ched la ae om each emale was p ese ed in 70%
e hanol o he measu emen s o L
T
and W
T
.
La al g ow h, su i al, and swimming
pe o mance expe imen s
Ha ched la ae om he labo a o y incuba ions we e
mo ed daily o low- h ough anks (26 li e s) and la ae
om each lake and om 3 o 5 emales we e kep sepa a ely
in he collec ing anks o a maximum o 3 days wi hou
ood in o de o collec enough la ae o ea ing expe i-
men s. Subsequen ly, newly ha ched la ae we e di ided
in o ae a ed low- h ough aqua ia (leng h 40 cm 9wid h
25 cm 9heigh 20 cm), and 65 la ae pe aqua ium wi h
2–5 eplica es pe lake we e ea ed o 23 days o moni o
hei g ow h and mo ali y. The pho ope iod du ing ea -
ing expe imen s was se a 18-h ligh : 6-h da k, and he la -
ae we e ed ad libi um on ha ched A emia nauplii wi hou
cys s (daily a ion adjus ed o 100% o he W
T
o he la -
ae). The aqua ia we e cleaned daily by siphoning ou eces
and unea en A emia. The numbe o dead la ae and wa e
empe a u e we e eco ded daily. The ins an aneous mo -
ali y (Z
L
) du ing he la al ea ing pe iod was calcula ed
sepa a ely o each aqua ium, and he lake-speci ic Z
L
was
calcula ed as a mean o aqua ia o a gi en popula ion. The
mean (SD) ea ing empe a u es we e 12.9 0.4,
13.5 0.6 and 15.0 0.4°C in sp ing 2005, 2006, and
2007, espec i ely.
A andom sample o i e la ae om each aqua ium was
aken o a challenge es . Challenge es s we e pe o med
in a low- h ough swimming chambe wi h a olume o
18 ml. The chambe was connec ed by ubbe hoses o a
wa e ci cula ion pump, and he whole sys em was
imme sed in an aqua ium. Wa e eloci y in he chambe
was calib a ed sepa a ely in each ial acco ding o he
a e age L
T
o la ae a a gi en ime. Fi e la ae we e placed
in he swimming chambe , and wa e low was adjus ed o
he le el o 1 L
T
s
1
o 1 min, a e which wa e eloci y
was inc eased o 5 L
T
s
1
(SD =1). Swimming abili y o
la ae agains low was eco ded as he ime (s) un il he
median la a ( hi d o he i e) was exhaus ed and was
unable o keep i s posi ion in he swimming unnel. A e
ha , la ae we e emo ed om he chambe and anaes-
he ized be o e measu emen o indi idual L
T
and W
T
.
Da a analysis
A gene al linea model (GLM) wi h a main e ec model
s uc u e was used o es o he e ec o lake, s udy
yea , and age o spawne s (young s. old spawne s) on
he o al ene gy alloca ed o g ow h and eggs (P
S+R
,
kJg
1
) o o ep oduc ion (P
R
,kJg
1
) o emales in he
summe be o e spawning. We body mass o he emales
was used as a co a ia e in he models.
GLM, wi h P
S+R
as a co a ia e, was used o es o he
e ec o he spawning his o y on he ela i e ecundi y
(eggs g
1
) and we mass o eggs (mg) o emales. In hese
analyses, he P
S+R
o indi idual ish om he s udy lakes
was assumed o e lec he lake- and yea -speci ic s a us
including he he mal e ec s, so lake and yea ac o s
we e no longe included in he models.
GLM, wi h he o al biomass o endace (kgha
1
)in
summe be o e he spawning season as a co a ia e, was
used o es o he e ec o he emale age (young s.
old) on P
S+R.
The di e ence in he e iliza ion ailu e (Z
F
), o al
mo ali y o emb yos du ing he expe imen al incuba ion
pe iod (Z
E
), p opo ion o ha ched la ae ali e (H%),
and L
T
and W
T
o he ha ched la ae we e compa ed
be ween young and old spawne s by he GLMs wi h P
S+R
as a co a ia e.
In la al expe imen s, he ea ing empe a u e di e ed
be ween he s udy yea s due o p oblems wi h he hea ing
sys em. Thus, he empe a u e e ec on he g ow h o he
la ae was co ec ed by a empe a u e-speci ic g ow h
unc ion de i ed om he expe imen al da a o Luczynski
(1991). The L
T
and W
T
o la ae in each aqua ium we e
adjus ed o co espond o g ow h a 13.5°C which was
he mean ea ing empe a u e in 2006. Because he la ae
o all emales om a lake we e pooled in he ea ing
expe imen s (no possible o iden i y mo he s o indi id-
ual la ae), he P
S+R
o he analysis was calcula ed as an
annual mean o all emales in speci ic yea and lake. Da a
we e di ided u he in o wo P
S+R
classes lowe and
highe han he o e all mean o he emales in all yea s
(o e all mean =4.6 kJg
1
). The di e ences in empe a-
u e-co ec ed L
T
and W
T
we e es ed by - es be ween
he wo P
S+R
classes. GLM model wi h he ln- ans o med
ª2016 The Au ho s. Ecology and E olu ion published by John Wiley & Sons L d. 783
J. Ka jalainen e al. Pheno ypic Plas ici y in G ow h o Female Fish

ea ing empe a u e as a co a ia e was used o es he
e ec s o P
S+R
on he Z
L
and swimming pe o mance o
la ae a e he 23-days ea ing expe imen . In his analy-
sis, P
S+R
class was a ixed ac o .
Resul s
Plas ici y in g ow h and ecundi y
The la ge di e ences in he popula ion densi y be ween
lakes caused high a ia ion in he mean size o bo h ju e-
nile and ma u e ish, as well as in he ecundi y o
emales. The in e annual a ia ion in he we mass o 0+
ish a e he i s g owing season was high, and e en a
ou old di e ence be ween successi e yea s has been
obse ed in Lake I (Fig. 2). The majo i y o endace
emales spawned o he i s ime in hei second au umn
(Table 1, % o ma u e indi iduals a age o 1+) and he
p opo ion young spawne s a ied be ween 40 and 84%
o all spawne s. Thus, e e y yea he e we e also olde
and likely epea spawne s (age 2+o olde ) p esen in all
lakes, bu hei p opo ion and o al numbe we e clea ly
lowes in Lake I wi h he lowes popula ion densi y and
highes adul mo ali y due o in ensi e ishing.
To al ene gy (kJ) alloca ed by endace emales o
soma ic g ow h and eggs di e ed conside ably be ween
lakes (Fig. 3A) demons a ing he ex eme a iabili y o
hei g ow h and ecundi y. Young spawne s (age g oup
1+) in es ed signi ican ly mo e (F=659.6, P<0.001,
Fig. 3B) ene gy in o g ow h and eggs (P
S+R
,kJg
1
) han
old spawne s (age g oup ≥2+). The P
S+R
also di e ed
signi ican ly be ween lakes (F=7.2, P<0.001), being la -
ges in he spa ses popula ion wi h ex emely as -g ow-
ing indi iduals in Lake I, and also be ween yea s
(F=28.1, P<0.001). The e ec o he co a ia e we
mass was no signi ican (F=0.01, P>0.05).
The ene gy alloca ed o eggs (P
R
,kJg
1
) also di e ed
signi ican ly be ween young and old spawne s (F=25.3,
P<0.001). The P
R
o young spawne s was highe han
ha o old spawne s (Fig. 3B), bu old spawne s alloca ed
a highe p opo ion (69%) o o al ene gy o eggs han
young emales (49%), and hus, a smalle sha e emained
o soma ic g ow h. Al oge he , he a ia ion in P
R
was
e y low compa ed o ha o P
S
.The P
R
di e ed signi i-
can ly be ween yea s (F=3.2, P<0.05) bu did no di -
e be ween lakes (F=1.0, P>0.05). Again, he e ec o
he co a ia e mass was no signi ican (F=1.1, P>0.05).
The la ge di e ences in he age-speci ic size o emales
be ween lakes yielded la ge be ween-lakes di e ences in
hei absolu e ecundi y (eggs emale
1
, Table 1). A he
same size, he old spawne s had on a e age 10% lowe
Figu e 2. In e annual a ia ion in he mean we mass (g) o 0+
endace in 1973–2013 (Helminen e al. 1992) in Lake I and Lake IV
(P. Valkeaj€
a i, unpublished da a).
Figu e 3. (A) To al ene gy alloca ion o soma ic g ow h (kJ) and eggs
(kJ) by young (1) and old (2) spawne s in Lakes I–IV. (B) Rela i e
ene gy alloca ion o soma ic g ow h (P
S,
kJg
1
o emale we mass)
and egg p oduc ion (P
R
,kJg
1
o emale we mass) by young and old
spawne s in Lakes I-IV. The means o e all lakes and yea s o o al
ene gy (P
S+R
,kJg
1
o emale we mass) used o g ow h and egg
p oduc ion du ing g owing season and o mean ene gy used o
eggs (P
R
) a e shown by dashed and solid lines, espec i ely.
784 ª2016 The Au ho s. Ecology and E olu ion published by John Wiley & Sons L d.
Pheno ypic Plas ici y in G ow h o Female Fish J. Ka jalainen e al.
absolu e ecundi y han he young spawne s. We mass o
eggs (mg) and ela i e ecundi y (eggs g
1
emale we
mass) di e ed signi ican ly be ween hese spawning his-
o y classes (F=3.9, P<0.001; and F=25.9, P<0.001,
Fig. 4). The egg mass o old spawne s was highe bu
hei ela i e ecundi y was lowe han hose o young
spawne s. In he GLM model, he co a ia e P
S+R
signi i-
can ly a ec ed he egg we mass (F=11.5, P<0.01) and
ela i e ecundi y (F=3.6, P=0.06) o emales: In bo h
young and old spawne s, highe P
S+R
(and hus mo e
ene gy a ailable) was associa ed wi h highe egg mass bu
lowe ela i e ecundi y.
E ec s o P
s+
on e iliza ion ailu e and
egg mo ali y
P
S+R
had no e ec on he e iliza ion ailu e Z
F
(F=0.15, P>0.05) o he o al emb yonic mo ali y
om e iliza ion o 100% ha ching Z
T
(F=0.15,
P>0.05). Nei he Z
F
(F=0.15, P>0.05) no Z
T
(F=0.7, P>0.05) di e ed signi ican ly be ween young
and old spawne s. In he incuba ion expe imen s, Z
T
was
gene ally high and a iable be ween yea s and popula-
ions; he ela i e o al mo ali ies (A%, mean SD)
we e 82 9%, 53 23%, 25 16%, and 76 36% in
Lakes I, II, III, and IV, espec i ely. Fe iliza ion ailu e
cons i u ed mos o he o al mo ali y.
E ec s o P
s+
on la al g ow h, mo ali y,
and swimming pe o mance
P
S+R
had a signi ican posi i e e ec on he o al leng h
(L
T
) o ha ched la ae (F=4.3, P<0.05) bu no on he
p opo ion o ha ched li e la ae ali e (H
%,
F=2.7,
P>0.05). L
T
o newly ha ched la ae (F=5.6, P<0.05)
and H
%
(F=7.5, P<0.05) di e ed signi ican ly be ween
young and old spawne s. The mean L
T
was 8.5 mm
(SD =0.7, n=31) and 8.7 mm (SD =0.4, n=48) o
he young and old emales, espec i ely. The mean H
%
was 93% (SD =15, n=38) and 98% (SD =7, n=59)
o he young and old emales, espec i ely.
A e he 23-days ea ing expe imen , he la al pe iod
mo ali y Z
L
(Fig. 5A) di e ed be ween he low and high
P
S+R
classes (F=20.3, P<0.001) and he empe a u e
co a ia e was also signi ican (F=13.8, P<0.01). Mo -
ali y in he low P
S+R
class was highe han in he high
P
S+R
class. The swimming pe o mance (Fig. 5B) o he
la ae did no di e signi ican ly be ween P
S+R
classes
(F=1.3, P>0.05), and he e ec o empe a u e co a i-
a e was insigni ican (F=0.5, P>0.05). The e was no
signi ican di e ence be ween P
S+R
classes (Fig. 5C, D) in
la al L
T
o W
T
( =1.75, P>0.05; and =0.24,
P>0.05, espec i ely).
Implica ions o popula ion le el
In he s udy yea s, he es ima es o mean densi y o
spawne s, egg p oduc ion, and la al p oduc ion di e ed
conside ably be ween he lakes (Fig. 6A–C): The o sp ing
p oduc ion was highes in Lake IV wi h he highes o al
Figu e 4. (A) Rela ionship be ween egg we mass (g) and o al
ene gy alloca ed o g ow h and egg p oduc ion (P
S+R
,kJg
1
o
emale we mass) du ing he g owing season. Reg ession lines
(y=a+bx) o young (a=1.81 0.12 (SE), b=0.039 0.021)
and old spawne s (a=1.83 0.13, b=0.11 0.04) a e gi en
sepa a ely. (B) Rela ionship be ween ela i e ecundi y o emales
(egg g
1
emale we mass) and P
S+R
. Reg ession lines o young
(a=130.3 11.1 (SE), b=2.53 1.93) and old spawne s
(a=121.7 8.52, b=3.31 2.39) a e gi en sepa a ely.
Figu e 5. (A) Mo ali y (Z
L
), (B) swimming pe o mance (seconds), (C)
o al leng h (L
T
, mm), and (D) we mass (W
T
, mg) o endace la ae
a he end o he 23-day ea ing expe imen s in sp ing 2005, 2006,
and 2007. Ba s indica e he mean alues o la ae ha ched om he
eggs o emales wi h low o high P
S+R
. E o ba s ep esen he
s anda d e o o he mean, and ***indica es s a is ically signi ican
di e ence be ween he low and high P
S+R
.
ª2016 The Au ho s. Ecology and E olu ion published by John Wiley & Sons L d. 785
J. Ka jalainen e al. Pheno ypic Plas ici y in G ow h o Female Fish
densi y es ima e, while he lowes egg and la al p oduc-
ion was obse ed in Lake I wi h he lowes popula ion
densi y and he highes annual mo ali y. Ins ead, he
mean annual densi y o 0+ ish in au umn showed low
a ia ion be ween he lakes (Fig. 6D), and he o al
annual biomass o he popula ion showed li le a ia ion
be ween he lakes o e en an opposi e end compa ed o
he densi y, wi h Lake I ha ing he highes mean biomass
among he s udy lakes (Fig. 6E).
Discussion
In ou s udy lakes, endace emales alloca ed a a he con-
s an and high p opo ion o hei ene gy in es men s o
eggs (kJg
1
) despi e e y di e en g ow h pa e ns
depending on he esou ces a ailable in he di e en lakes
(e.g., ange o mean W
T
and ecundi y a age o i s ep o-
duc ion om 5 o 132 g and om 530 o 21,000 eggs e-
male
1
, espec i ely). The in es men s in o eggs hus
dic a ed he sha e emaining o g ow h. Egg p oduc ion by
la ge emales and old spawne s ook a la ge p opo ion o
hei o al ene gy alloca ed o g ow h and eggs (P
S+R
) han
he egg in es men s by smalle and young spawne s, which
led o a end o dec easing g ow h a e a highe size and
age. Such educed g ow h a e ma u a ion is a phe-
nomenon widely obse ed among ishes (Ro 1983; Folk-
o d e al. 2014), and al hough some ish species wi h
limi ed ood supply may pa ly o ully sac i ice egg p o-
duc ion o p ese e body condi ion, mos main ain in es -
men in ep oduc ion a he expense o body ese es
(Sabo ido-Rey and Kjesbu 2005).
The ene gy alloca ion o eggs pe body mass was highe
in young han in old spawne s, and he egg size and con-
sequen ly he ela i e ecundi y also di e ed, wi h young
emales p oducing mo e bu smalle eggs so ha he
newly ha ched la ae o young emales we e smalle han
he la ae o old spawne s. The ecognized high alue o
la ge ma u e ish (high ecundi y, la ge eggs, highe su -
i al o o sp ing) o he popula ions o se e al species
has led o he ecommenda ion in hei ishe ies manage-
men o conse e la ge, ypically old indi iduals (Dua e
and Alca az 1989; Be keley e al. 2004; Sabo ido-Rey and
Kjesbu 2005; Enbe g e al. 2011). Howe e , in ou en-
dace expe imen s, he e iliza ion a e and he su i al o
emb yos we e no a ec ed by he age o spawne s o he
o al ene gy alloca ion o he eggs. This con as s wi h he
esul s o ea lie expe imen s by Kamle e al. (1982) who
epo ed ha endace emales spawning o he i s ime
p oduced he “wo s ” eggs, middle-aged emales p oduced
he bes eggs, and old spawne s laid eggs wi h again lowe
quali y. The emb yonic mo ali y in ou expe imen s was
highes du ing ea ly emb yogenesis un il he eyed s age,
which has also been epo ed in p e ious s udies
(Wilkonska and Zu omska 1982; Kamle 2005; Ka -
jalainen e al. 2014). Ou e iliza ion p ocedu e simula ed
he communal spawning whe eby se e al males elease
hei spe m simul aneously du ing spawning, and he e-
o e, he pa e nal e ec s on emb yonic su i al emain
un esol ed.
In many ish species, he impo an ep oduc i e ai s
o age and size a ma u a ion a y wi h changes in popu-
la ion densi y (Adams 1980; T ippel 1995; Sabo ido-Rey
and Kjesbu 2005; Roos e al. 2006). As he age a ma u a-
ion o endace in Finnish lakes is p ac ically ixed o
hei second au umn (age g oup 1+yea s), he size a
ma u a ion a ies ma kedly wi h he indi idual g ow h
a e o ish, which again depends on popula ion densi y.
In ou s udy lakes, luc ua ion be ween high and low
s ock densi ies a e ypical and caused by in e annual a i-
a ion in en i onmen al condi ions (Ka jalainen e al.
2000; Ma jom€
aki 2003) as well as in e s age e ec s o en-
dace popula ions (Ma jom€
aki e al. 2014). In some Fin-
nish lakes, in ensi e ishing o he endace popula ion
app eciably shapes he spawning s ock s uc u e (Sa ala
and Helminen 1995; Huusko and Hy €
a inen 2005) and
ep oduc i e ai s o he species. Especially in Lake I, a
spa se popula ion ollowing high ishing mo ali y
esponds o high esou ce a ailabili y by high g ow h a e
p io o spawning and subsequen high indi idual ecun-
di y. A simila esponse o g ow h (Fig. 2) and ecundi y
has been seen in many o he lakes, including Lake IV
whe e in he 1990s a long and p obably en i onmen al-
Figu e 6. Densi y o spawning s ock (A, ma u e indi iduals ha
1
),
popula ion ecundi y (B, eggs ha
1
), la al densi y (C, la ae ha
1
),
densi y o 0+ endace in au umn (D, indi iduals ha
1
), and o al
biomass o endace in au umn (E, biomass o 0+and ma u e ish
kgha
1
) in he s udy lakes in 2003–2007. Ba s ep esen annual
means and e ical lines s anda d de ia ions.
786 ª2016 The Au ho s. Ecology and E olu ion published by John Wiley & Sons L d.
Pheno ypic Plas ici y in G ow h o Female Fish J. Ka jalainen e al.
induced phase o low endace s ock p e ailed (Valkeaj€
a i
and Ma jom€
aki 2013).
In e es ingly, he ela i e ecundi y o endace emales
in he spa se popula ion was lowe and egg size la ge
han hose o ish g owing in he dense s ock wi h e y
much lowe ood a io pe capi a. This esponse o egg
size o ood sca ci y was opposi e o he mechanisms
epo ed among pe iodic salmonids, which end o p o-
duce la ge eggs i emales unde go ood sca ci y p io o
spawning (Tho pe e al. 1984; Hu chings 1991; Bu on
e al. 2013). This ade-o o in es ing in highe quali y,
la ge la ae while educing hei quan i y unde ood
limi a ion has been conside ed a bene icial adap a ion in
low esou ce en i onmen al condi ions (Hu chings 1991;
G ege sen e al. 2011; V ilek and Reicha d 2014). How-
e e , s udies ha e e ealed ha he exp ession o ma e nal
e ec s is con ex -dependen and es ic ed ma e nal ood
a ailabili y has been shown o ei he dec ease (Gagliano
and McCo mick 2007) o inc ease (Hu chings 1991; Gui-
sande e al. 1996; Allen e al. 2008) o sp ing size and su -
i al. Plais ow and Ben on (2009) concluded ha
ma e nal e ec s in high compe i ion popula ion (low
ood a ion) impac mo e on ju enile su i al compa ed
wi h low compe i ion popula ions (high ood a ion),
whe e ma e nal e ec s ha e mo e impac on he popula-
ion g ow h a e.
In addi ion o he compensa o y densi y-dependen
inc ease in p e ec ui men su i al o endace along wi h
he dec ease in spawning s ock (Ma jom€
aki 2003), excep-
ionally high compensa o y plas ici y in g ow h and sub-
sequen changes in ecundi y and egg size inc ease he
capaci y o endace popula ions o wi hs and high ishing
mo ali y. In a spa se s ock, emales p oduce pe capi a
mo e and la ge eggs and la ae wi h highe su i al: In
Lake I, he spawning s ock densi y was much lowe han
in he o he lakes, bu he es ima e o su i al om newly
ha ched la ae o 0+ ish in au umn was as high as
32 30% o lake I (mean SD) compa ed o
11 7% o Lakes III and IV. Mo eo e , he ex emely
high g ow h a e o ish in he Lake I p io o spawning
esul ed in o al biomass o endace in au umn as high as
in he o he lakes (Fig. 6E). The longe g owing season
and highe p oduc i i y in Lake I han in he o he lakes
also con ibu e o he high g ow h and egg p oduc ion o
endace emales, al hough he me a-analysis by Viljanen
(1986) showed ha di e ences in he g ow h a e o en-
dace popula ions be ween sou he n and no he n lakes
was much smalle han he in e annual di e ences in
g ow h o ish in same lake and e en in successi e yea s.
Size-selec i e ishing is commonly in e p e ed as one o
he majo causes behind obse ed changes in age a ma u-
a ion by a ec ing g ow h a es and inducing e olu ion-
a y egime shi s (Sabo ido-Rey and Kjesbu 2005; Roos
e al. 2006). In endace popula ions, ishing is e lec ed in
o he ep oduc i e ai s, and in ensi e ha es ing has also
been obse ed o simpli y he spawning popula ion s uc-
u e causing changes in he popula ion dynamics
(Huusko and Hy €
a inen 2005).
Al hough he la ge in e annual di e ences in g ow h o
pa en al ish wi hin a lake we e caused by hei ex eme
pheno ypic plas ici y in esponse o he changes in he
popula ion densi y, we canno o ally o e ule he e ec
o local adap a ion, which has been sugges ed o be com-
mon in salmonids (Taylo 1991; P imme 2011). Local
adap a ion o ish can be apid, p og essi e p ocess d i en
by en i onmen -induced selec ion p ocess (Eizagui e
e al. 2012; Wes ley e al. 2012). Plas ici y i sel “is he i a-
ble and popula ion di e ences in eac ion no ms can
e lec adap i e esponses, by na u al selec ion, o local
en i onmen s” (Hu chings 2011), and hus, locally
adap ed popula ions may a y in hei plas ici y. Ou
s udy species has high in e annual a ia ion in g ow h
ha ing la ge di e ences in mass o 0+ ish e en be ween
successi e yea s, and he po en ial o plas ici y seems o
be simila in he s udy lakes (see Fig. 2). Also s ock ans-
e s o endace by ishe ies manage s om lakes wi h
dense popula ion and slow-g owing indi iduals o
ano he lake wi h spa se popula ion has caused ema k-
able changes in g ow h a e o ans e ed ish ma ching
wi h he ampli ude o a iabili y in ou s udy lakes
(Huuskonen, H., Ma jom€
aki, T. J., unpublished esul s).
In he incuba ion expe imen s, he emb yos o all pop-
ula ions de eloped a simila a es and hei ha ching suc-
cess was high. The newly ha ched la ae o old spawne s
we e sligh ly la ge han hose o young spawne s.
Acco ding o he concep o “ apid g ow h leads o
educed suscep ibili y o size-selec i e mo ali y and
enables high su i al and high i ness” (Mille e al. 1988)
e en small di e ences in he ha ching size may signi i-
can ly a ec he u u e su i al. Al hough U panen e al.
(2005) obse ed no clea size-dependen mo ali y du ing
he ea ly li e o endace in Finnish lakes, Au inen (1995)
and Sa ala and Helminen (1995) ha e epo ed ha he
yea -class s eng h o endace in hei s udy lakes seemed
o be posi i ely associa ed wi h egg size. In ou ea ing
expe imen s, he mean lake-speci ic ins an aneous mo al-
i y a e (Z
L
) anged om 0.10 o 0.34 and mo ali y did
no di e among popula ions bu was signi ican ly di e -
en be ween he o sp ing o emales wi h low and high
P
S+R
. Howe e , he g ow h and swimming pe o mance
o he la ae unde expe imen al condi ions did no di e
be ween P
S+R
classes. Al hough ou expe imen al and ield
da a basically suppo he asymme ic ood compe i ion
hypo hesis o Ham in and Pe sson (1986) as a mechanism
explaining he 2-yea cyclici y o endace popula ions, he
di e ences in la al su i al and p ope ies a e a oo
ª2016 The Au ho s. Ecology and E olu ion published by John Wiley & Sons L d. 787
J. Ka jalainen e al. Pheno ypic Plas ici y in G ow h o Female Fish