Environmental Tolerances and Requirements of Splittail
PACIENCIA S. YOUNG AND JOSEPHJ. CECH, JR.'
Depannrml of ll'ildlijr. Fish. and Consccy~lIioaBiolos?.
Uniwrsiq' of Coli/nn~ia.,Dm.ir. Davis. Gzlfirnio 95616. USA
Ab.wacr.-The range of splionil Pngnrriclrrlr,r ~ c m l c p i d o ~ uhas
r decrused to lcsr than r third
of i t s original range due to loss or alleration of habitats. We measured the critical 1henn.l minima
agement and rcstoralion of this species. Neither thermal acclimrtion nor fish weight affeaed the
but .
,
T
C
(29-33'C) of fish acclimated at 17 and 20.t were higher than
C
T
,
.
(21-22T) of fish acclimated a I 2 T . Mun CWmI.vdua were low (0.6-1.3 mg O2/L)
for a l l age-group. although immature age-2 fish acclimated at 12Y: bad a l o w CWe. than
my group acclimated at IPC. Mean. C
,S
(20-2%) did wc vary with acclimtion tempenlure,
but i n c r u d with inmasing weight for fish acclityted at 17-C. M u n time to loss of equilibrium
a d w u r e n ~ l l lvo w for a n 4 firh
in a l l ape-gmups z e l ~ ~ ldl ye e d as ulinitv inGin
(6.5-7.3W
1%
Inauru in acclimation cempmturr by 3T for small . a 4fish .nd 5'12 for o r - 2 lirh
.a dead-end sloughs. A *ck of wfficient-flooded&gelation for spawning .Idruring, a s n o w
e w . larvae. and adult wwaen). a bimic
envimnmenul tolcnmrr of Mher life rug- (i.~..
factors (rg.. predation. competition) may be limiting splittail lbundracc and disuibution.
The splittail pogonic&hys mncrolepidorus (Ayres 1854) is theonly surviving memberof its genus
and one of the most ancestral North Amuican c y p
rinids endemic to the SacramentoSan Joaquin
drainage o f California (Moyle 1976). I t once was
one of the most abundant estuarine species in the
Sacramento-San Ioaquin estuary and supponed a
small hook-and-line fishery (Caywood 1974). I t
was once widely distributed in lakes and rivers
throughout California's central valley (Runer
1908) but disappeared from much of its native
range becauseof loss or allcration of lowland habitats following dam constntction. water diversion.
and agricultural development. The species is now
largely restricted to the SacnunentoSan ioaquin
estuary (Herbold et d. 1992; Mnyle and Yoshiyama 1W2) ucept during upstrcamspwning migratiom (Moyle
.1. 1995). Acto -Y
spawning areas or upsueam habitas is blocked by
dams on the large rivers. and because splittails
seemingly incapable of negotiating existing fishways, they ur restricted to water below the dams
(Moyle et 1. 1995). I n 1994. the splittail had reportedly declined 62% o v a che previous 13-year
period (Meng and Moyle 1995). Because of the
-
' To whom reprint reguests should he addressed.
rapid population decline, thesplittail waiproporad
for listing as a threatened species under the Enb n g d Species Act by the United States Fish
and Wildlife Svvice (USFWS) in 1993. but listing
was &fund in 1995 (Moyle et a!. 1995). AIthough an unusud reproductive s u m s oecumd
in 1995 that was associated with an exceptionally
wet spring (P. M o y l University
~
o f California. Davis, penond communication). the future of this
species is- far from secure. Continued decline in
freshwater inflows into the estuary will eventually
change both =linity Dmperawre kvels,
pasdecdisbolved oxygen levels. and
wuer flow velocitiu.
rrrponx to fie
decr;rxd
fmhwatvlnlow. H ~ ~
h.+
bi,
u
w
~
till up
'
-
mum into ch.nnelized
thu
hve
the appropriate fubitau for
Such an u p
smm
rplitui,s
the
rhifi
MY
vulclenble
divcnion
make eggr.
young
rybtem
via
south delta(Meng
upon. from
and Moyle 1995). I n addition. electrical power
generating plants discharge wum water into the
estuary. I n spite of information on the splituil's
age and growth. condition. reproductive biology.
yurslass shmgth. and distribution (Caywood
1974; Daniels and Moyle 1983: Meng and Moyle
1995). the species' environmental requirements
664
ENVIRONMENTAL TOLERANCES OF SPLITTAIL
and tolerances are relatively unknown. Thereeffects of these environmental
fore, the
on splittail abundance are unclear.
o u r study was designed to define the splittail's
environmental requirements and tolerances to assist in effective water and habitat management and
restoration of this species. We addressed swimming performance (associated with effects of flow
fishway negotiationsj along with limits of tolerance to environmental conditions (associated
with habitat requirements). Specifically, the study
aimed to determine the critical thermal minima
(CT,,)
and maxima (CT,.,),
critical dissolved
oxygen minima (CDOmi,), critical salinity maxima
(cS,,,),
and critical swimming velocity (UCrit)of
age-O, age-I, and immature age-2 splittails.
Methods
~ i s hcollection and maintenance.-Zlassification of splittails by age-group was based on fish
wet weight and standard length (SL) according to
Daniels and Moyle (1983). Small (0.1-0.5 g; 2-3
cm SL) age-0 fish were collected at Georgiana
Slough (in the northeastern .part of the estuary);
large age-0 (1-4 g: 4-7 cm), age-l (10-42 g; 913 cm), and immature age-2 (80-200 g; 18-23 cm)
fish were collected from Suisun Marsh (in the
western part of the;estuary) and at the state and
federal pumping and fish salvage facilities in the
southern pan of the estuary. Fish were transported
to laboratories at tlie University of California, Davis, in insulated coolers or fiberglass tanks with
aerated water at ambient (collection) temperature;
rock salt (NaCI) was added (4%0) to minimize osmotic stress on the fish. Age-0 fish were collected
during spring and summer at 17-20°C and 0-1%
salinity and were acclimated to 17 or 20°C; most
age-1 and age-2 fish were collected during the fall,
winter, and spring at 9-18°C and 0-5%0 salinity
and were acclimated to 12 o r 17°C. A few age-l
and age-2 fish, collected in late spring at 19-21°C
and 1-4% salinity, w e n originally acclimated at
20°C but were later reacclimated to 17°C because
the number of fish was smaller than the required
sample size for the experiments. Fish were held in
aerated flow-through aquaria (age-0 fish) or fiberglass tanks (age-l and age-2 fish) with air-equilibrated well water. Thermal acclimation was conducted at IoC/d from the collection temperature.
Age-0 fish were fed Arternia sp. nauplii and fish
crumbles; age-1 and age-2 fish were fed trout pellets. Fish were subjected to simulated natural photoperiod.
665
Tolerance Tests
Determinations of thermal, dissolved oxyge.
(DO), and salinity tolerance limits were conducte~
following modifications to the methods of Cox
(1974) and Becker and Genoway (1979). Loss of
equilibrium was used as the end point for the tolerance tests. Fish were maintained at acclimation
temperature for at least 7 d and were not fed for
24 h before the start of an experiment. Fish were
placed in test vessels or containers with flowthrough water at acclimation temperature 15-18 h
before the start of experiments to minimize transfer-related stress. Fish were weighed after each
experiment and measured (SL) after swimming experiments. Some of the fish used for one test were
also used for, at most, two different tests after at
least 1 week of recovery after each test. None of
the fish were used twice for the same experiment.
In all tests. each fish was isolated. In the temperature and DO tolerance apparatus, fish were not
visually isolated, but there was no. indication that
the behavior of one fish affected the behavior of
others. Furthermore, there was a random placement of controls among the test fish.
Temperature.-Fish
were held in individual
Plexiglas vessels of a flow-through design (Cech
et al. 1979) and were subjected to decreasing
(O.O8'C/min for CT,in) or increasing (O.laC/min
for CT,,,)
temperatures, starting from the acclimation temperature. Control fish were subjectec
to the same protocol but without the temperature
changes. Inflow water was continuously aerated to
ensure a high level of DO. Volumes of test vessels
were 1.4 L (age-0 and age-1 fish) or 4.0 L (age-2
fish), and mean test water flow rates were 170 or
250 mL/miu, respectively. Each vessel was
equipped with a calibrated Yellow Springs I n s m ments thermister probe (YSI model 401), and temperature was monitored with a YSI telethermometer (model 44TD) every 10 min and at the end
point. Immediately after recording an end point
temperature, test water inflow to that vessel was
stopped, and an acclimation temperature inflow
was started.
Final thermal preferences and optimum temperdata
atures for growth were estimated from CT,,,
with regressions modified from Jobling (1981): final thermal preference = (CT,,,
- 16.43)/0.66;
optimum temperature for growth = (CT,,,
13.81)/0.76. The Jobliug (1981) equations were
based on 49 fish species in 16 families. Estimates
derived from these equations were only applied to
fish acclimated to the higher temperature because
',
666
YOUNG AND CECH
these equations were based on the upper incipient tem to that container Hras stopped, and a freshwater
lethal temperatures (WILT) and CT,,
for fish ac- inflow was started.
climated to the highest temperature.
Dissolved orv~en-Fish
were held at ambient
- ,-Salinity endurance experiments w e n conducted
temperature in a temperature-controlled water bath
in individual Plexiglas test vessels of a flow- in the same system as thc salinity tolerance tests.
through design similar (age 0) o r identical (age k Fish were not fed for 24 h before or during the
and age 2) to those used in the thermal tolerance experiments. After 15-18 h habituation. all freshtests. Volumes of test vessels were 0.8 L (age 0). water inflows w a c stopped and a concentrated
1.4 L (age 1) or 4.0 L (age 2). and the mean test rock salt brine solution was slowly (5-6 min) inwater flow rates were 140, 170 or 250 mUmln. voducul above the constantly bubbling airstone
respectively. A 3 0 c m polyethylene tubing (1.67- (for rapid mixing) until the desirui salinity level
mm internal diameter) was insexled into each of (12 (age 0 only]. 14 (age 0 only]. 16, 20, 24. o r
the test vessels for w a t a sampling. Fish w e n sub- 28%) was reached. Behavior and status of fish
jected to decreasing levels of DO by passing in- werc constantly monitored. For fish with end
flowing water through a polyvinyl chloride ship- points grater than 24 h. at i&t two-thirds of the
ping column ((%h & al. 1979) in which a wun- water volume was replaced by w a t u of the same
tallow of nitrogen gas (regulated through a y test salinity every 24 h I m m o d i l y lfter the end
flowmeta) altcrad DO content Dissolved oxygen poinL the time to loss of equilibrium CIZB) was
flow was surtcd If TLE
partial p ~ s u r e
(Pq)in the inflow column was rccorded md a hrrhwas
not
observed within 120 4 thc expcriwat was
daxasea at 1 tomImio (1 tom = 1333 Pa: 14 tom
mded. No Srh d iat 2OT wen available
% 1 mg
from approximately 150 tom
for salinity urdurrncc expaimurts.
Pq (appmximating
-- air s a m t i o n levels) to about
40 ton Pq. At this point. the rate of decrease was s w i m perfon
slowed to 0 5 wnJmin until the end point was
wcrc ds
aitiul
rrachd Tbc Pq was monitored (Cametun Inal
'on lcmp~fupcwith recir(Bm 1964) .
shumwt Co, model 100 DO meter) every 10 min
'ng
and at the end point Immediately afta a 6sh.s end
a uiable- speed
Flumes
pointrecordsd test water
to mat
and age 1) a d 102 L (age 2) in volume. p u t l y
was stopped, and an aerated water inflow was be- immasod in a -nmued
bath
gun Control fish wen subjected to the same pro- md dibntcd
with a digital MarshMarshMcBiracy
tow1 but without changes in DO. No fish tccli20
oruble
mcra. kh
musd u 2OT and no fish less than 1 g werc avail- hhwas pswimming
chamberllld
i.
able for the DO tolerana tests.
1 h habituation with wakx flow at 3 cmls (~ge
0
2), critical
Soliniry.4plittails were held in 10-L plastic md age I) or cmls
b u c b (age 0 and age 1) or 20-L glass aquaria velocity ( U ~ was
J mmud
by
increases of
(age 2)
the - h a t i o n
temperatun with -010 .dsin water veldtyat 10-min intervals, Stanstant lfntion
in
t c ~ m r r c o n m l l e d ing at LO cm/s, until thc 6sh was fatigued (Beamish
each 1978). A fish was -id&
wuer bdkscmXned
in the walk
fatigued whca it was
bucket and a standpipe in each aquarium main- impiu& three timer at the &-end of the
tlincd the 5-L (bucket) Or l>L ((squarium) ~ 0 1 ~
b=
~
I(+,, 1(dS)
daM
llmc Each container was oquippcd with a @tic
(BM 1964) BS fdlovr:
U .
U,
(10
top to Pn6sh from w i n g - E x ~ d m ManhXT/10 min), wbac U, = highest velocity
hr6 were subjected to increasing Icvels of salinity (a&)
maintained for 10 min .nd Q = time (min)
W % X r t a r t i ~ gat 0%. by
Of a
salt elapsed at fatigue velocity. Relative Usdl @ody
(NaCl. (hc dominant solute in seawater) brinedrip 1 ~ s ) &htd by dividing absolute (Idc
fraluetlcies(TBF)wcre measystem Salinity was monitorcd (YSI model 33 a- by SL (cm).T.il
linity-~~nduaivity-tcmptnnrrcmeter calibrated
for two igo-2 6sh by counting the number
with a Rkdiomacr -10
chloride titrator) e v a y of tail buts o v a a 1-min paid
20 min and at the end point Conlrol fish w u e
subjcdfd to me same pmtocol but with a k h - SM&iCcJAMbsa
Analyses of variana (ANOVA). Bonfmni's
water drip system Immediately after an end point.
container d i n i t y was recorded, the brine drip sys- tests. and Dunn's n o n p m C t r i c tests Were Con-
-
w)
zw-z
wercT
-
.
-
-
+
667
ENVIRONMENTAL TOLERANCES OF SPLITTAIL
TABLE 1.-Mean critical thermal minima (CT,,) and maxima (CT,,,.,), estimated upper limits of safe temperature
(uLST), final tmp=tUre preferences, and thermal growth optima for age-0, age-I, and age-2 splittails acclimated to
different temperatures. There were no significant differences in CT,, values; within an age-group, an asterisk denote
significantlyhigher C
T
,
value (P < 0.05).
,
Acch-
Temperatun CC) ot
mation
temperaIuR (C!
N
Mean
(SE)
N
M a
small age 0
20
17
8
7.0
(0.15)
9
10
m e age 0
20
17
32.0
30.8
33.0
30.0
~ge-gmup
a- CCI
5
6.5
7.3
4
6.8
CT-
(0.10)
(0.14)
(0.10)
ducted to quantitatively compare values among
different tests (e.g.. thermal tolerance tests at different acclimation temperatures for different agegroups). Student's f-tests or Mann-Whitney nonparametnc tests were used to compare data for fish
acclimated at two different temperatures. Regression analyses were applied to show relationships
CS,,,,
and U,,,,
between fish weight and CT,,,,
and between TLE and salinity. Aptness for the
linear or the polynomial regression model was
based on the least mean squared residual and prohability values. All of the above statistical analyses
were conducted with SIGMASTAT software.
Analyses of covariance were conducted with SYSTAT software to determine significant interaction
effects of acclimation temperature and fish weight
CS,,
TLE, and U,,. Statison CT, CT,,,,
tical differences were considered significant at P
< 0.05.
Results
Tolerance Tests
Temperature.-As the temperature approached
the critical minimum or maximum, most of the
splittails were observed darting or turning around
(presumably an escape behavior), increasing ventilatory frequency, and gasping (mostly in CT,,,
measurements). Posttest recovery (restoration of
equilibrium) took 1-10 min. Four small and one
large age-0 fish did not recover from the test; data
from these fish were not included in the statistical
analyses. None of the control fish died.
Whereas fish weight and acclimation history had
no effect on CTmi, (6.5-7.3T), they had important
influences on CT,,,
(Table 1). Mean CT,,,
increased with acclimation temperature, decreased
with loglo(weight), and had a combined effect ex-
8
6
4
rc1
(SE)
Final
Growth
LLST preference optimum
(0.37)
27
26
24
(0.21)*
(0.41)
28
25
25
(0.33)-
22
21
24
22
25
21
= 12.017 + 1.036(acpressed as follows: CT,,,
climation temperature) - 4.405.loglo(wet weight)
0.24l(acclimation temperature X loglo[wet
weight]); 9 = 0.924; P < 0.001; N = 49. For the
small and large age-0 fish, an increase of 3'C in
acclimation temperature resulted in significant 1.2
and 3.0°C increases in CT,,,,
respectively. For
age-l and age-2 fish, a 5°C increase in acclimation
temperature resulted in significant 8 and 7 T increases, respectively. Table 1 also provides the estimated temperatures for final thermal preferences
and growth optima of different age-groups of splittail (data derived from equations in Jobling 1981).
Based on the safety factor of 5°C (Bridges 1971)
upper safe thermal limits were estimated from
CT,,,
(rounded to the nearest "C) for different
age-groups acclimated at different temperatures
(Table 1).
Dissolved oxygen.--As DO level decreased to
the end point, splittails increased activity (turning,
swimming, or darting around), then decreased activity but increased ventilatory frequency and
gasping. Posttest recovery generally took 3 minor ,
less; none of the fish died.
Mean CDO,,,,, values were low (9-18 tort Po2
o r 0.6-1.3 mg 0 2 L ) for all age-groups (Figure 1).
They were not affected by weight (1-187 g) or by
the interaction of weight with acclimation temperature (12 and 17"C), but age-2 fish acclimated
at 1 2 T had a significantly lower mean CDOmi, (9
tom Po2 or 0.6 mg OzlL) than any age-group acclimated at 1 7 T (15-18 torr Poz or 1.1-1.3 mg
02n).
Salinity-As
salinity level increased to end
points, splittails increased activity (turning, swimming, darting around, or trying to jump out of the
container), then decreased activity before losing
+
Y O U N G A N D CECH
k
25
0
-
acclimated a 1 1 7 1 ~
a c c l i m a t e d at 12 C
4
WET
FMVRE I.-MU.
W E I G H T
tg)
(+SE) aitical d i i l v d oxygen minima (tom) of age-2 spLiItail8 1~climatedat 12 and 17%
range from 4 to 10. Asluirk indicates a critical o x y p pruruns
in rrltio. to mua (ZSE) might. Sample sizes
dgaitiumtly lower tb.n 111 othm (P C 0.05).
'
equilibrium. Posttest recovery generally took 6
mitt or less. S
i
x smdl and three large a g e 4 fish
died during the experimmt. and data from these
fish were not included in the statistical analyses.
None of the control fish died.
Although fish were acclimated to freshwater.
mu. CS,
values w e e high (20-29% Figure
2). M a n CS,
(22-27s) for fish acclimated to
1 X inacased with an increase in fish weight
(0.2-192 g; 9 = 0.40. P < 0.001; N = 27) and
was described by the following: CS,
= 21.89
+ O.OS(wet weight). Inin acclimation teapcnatn did not significantly affix3 the CS,
for
age0 ad a g e 2 fish. This could not be tcrted for
age-1 6sh,which w c n acclimated to only onetunparnvc Them was no i n t d o n effect of aalid o n GMpenture and weight on &I CS-.
.win@ Endvmnce Text
Splituils at high d i n i t y levels (24 and 28%)
behaved similarly to h s c in salinity tolerance
tests. whcrus thore at Iowa salinity levels inr
cnrxd cbeir activity les before the a d point
Mort 6sh acclimated m 1% recovered from the
wrpaiment in I min or less. whereas fish acclimated to I2'C generally took 5 min to recover.
Control, age4 fish at 12 and 14% and -1
and
a g e 2 licb at 16% maintained their equilibria and
survived for the duration of the cxpdmmf
Mean time to Lars of equilibrium 0 in all
age-groups gencnlly daxkced as salinity increased (Figure 3. regnosion equafiom in Table
2). Man TLE at 16 and 20% w c n significantly
lower for age4 fish than for those of ocher agegroups. From the regressions (Table 2). salinity
tollevels aruc estimated for diffaent TLE
periods for different splittail age-groups @ble 3).
The age-0 fish had the lowest CS,
ad also the
lowen 4 n W d d i t y tolerance levels for diffucatTLEpuiods. Intcnaionofweight@9-121
g) and rclirmtion tanpenatrc (I2 and 1had
no sigaihant effect on Uw TLE
Swimming Pe&nnance
SpIituilr in dl agegroups swam d l in the
water Uumq dWgh most age1 and -2
fish
(eapbc*lly U 12T)were gcaenlly i d v c in the
holding tanks. We obremd that uil beat
cy mF)
inas w r t c r a u M t iadthough it wasquantified for only a few individuals.
For example, u 1% lwo ago2 fish (99 a d
g wet weighk 19.1 and 18.7 cm SL. n s p e a i ~ e l y )
ma-
ENVIRONMENTAL TOLERANCES OF SPLITTAIL
16
0
25
W E T
50
75
WEIGHT
100
125
(g)
Floune 2.-Mean (2SE)critical salinity maxima of splittails in relation to mean (+SE) weight at different
acclimation temoeratures. Reeression line is olotted for fish acclimated at 17°C only; N = 4-8; symbols lacking
a common 1ette;are significantlydifferent ( P < 0.05).
increased TBF from 1.I 8 Hz at 10 cmls to 3.22
Hz at 70 cmls. Interestingly, 9 of 28 small age-0
fish, and 2 of 21 large age-0 fish held onto the
upstream screen with their mouths when the water
current was greater than 30 cmls. Some of the
age-1 and age-2 fish also attempted this behavior
when the current was greater than 40 cmls, but
they were uusuccessful because of the fine screen
mesh. None of the fish died during the experiments.
Mean Ucrit was significantly affected by both
standard length and water temperature (small
age-0 and age-2 fish only). Mean absolute U,,it
(19.5-66.3 cmts) increased (9= 0.74, P < 0.001;
N = 43) with standard length (SL, 2.3-20.7 cm)
for fish acclimated at 17°C (Figure 4) and was
described by the following: U,,i, = 14.441 +
2.604(SL). Howevez mean relative UCri,(3.4-6.8
body lengthsls) decreased (r2 = 0.41, P .C 0.001;
N = 43) with standard length (SL, 2.3-20.7 cm)
(Figure 5) and was described by the following:
Uc,it = 7.296 - 0.223(SL). A 3°C increase in acclimation temperature in small age-0 fish significantly increased the absolute U,,i, by 11 cm/s, but
not the relative UCrit.A S T iucrease in acclimation
temperature in age-2 fish significantly increased
the absolute U,, by 25 cm/s and the relative U,,i,
by 1.26 body lengthsls.
Discussion
Overall, our studies show that splittails are higbly tolerant of thermal changes, salinity increases,
dissolved oxygen decreases, and strong water currents. All of these measures compare well with
those reported for other native and introduced California cyprinids; the splittail salinity tolerances
were noteworthy.
Temperature
The thermal tolerance of fish is generally estimated either as the incipient lethal temperature
(ILT) or as critical thermal maxima or minima
(CTM). For the splittail, thermal tolerance was determined by measuring CTM, which involves a
rapid increase or decrease in temperature, with loss
of equilibrium as the end point. The CTM is considered the ecological lethal index because animals
in nature may encounter such temperatures as
acute fluctuations above their tolerance limits
(Hutchison 1976). This method is particularly useful in assessing temperature tolerances of fishes
subjected to periodic thermal discharge (Bridges
YOUNG AND CECH
I o3
*
-
0
L:
lo2 LT
m
g
a
7 10'
Is
0
I
rn
rn
0
-)
0
loo
W
E-
2
r
lo-'
t
i
19 01 81 1
4 g (17:~)
42 g (17-C)
121 g
(17-C)
170 g (12 C)
-
.
-
-
i, :%,[
, .
12
14
16
18 20 22 24 26
S A L I N I T Y (2.)
28
30
Fbaw.6 3.--him (SB)tima m Lors d equilibrium (TLS loglo w e ) in duio. lo salinity level in diffawt
.ypmupr of rplituil. Sample sizes range from &me to four. .rrruirk indiulco r sigui-y
I o w a TLE d u e
u hm e nlinity lev* (P< 0.05): u m w indiclur rlvvivd for mac than I20 b
1971; Jobling 1981) and is also more economical
with respect to materids and hllman c f f m (Hutchiros 1976: Kilgour and McCauley 1986). In the
LT muhod. fish are abruptly hausfared to diffcrcn( tempMtures: this procedure not only subj e t s the fish to heat o r cold shock but also incorpontes thc effurr of transfer suers. Although at
some tempaamrcs the theimal shock md transfer
stress might be sublethal, the combined effect is
believed to compound the effect of s w a t i o n and
quickly lud to death (Itzkowitz u al. 1983).
The thermal limit values obtained hcn rre the
amst collde~~alivc
estimate of
kuusc the
ntc of i(O.1Wmin) or dcaurc (0.08.CI
min) p d u d c c m U m d d i o a If the rite is
too slow (c& I*C/h) a significant partial mcrmal
acclimation wouId occur. if tho rate is too fast
(e.g.. L%/min) UIC lag a g e a bath tunpuaNre
and fish body tcmperarure would lengthea Both
rated would result in decreased CX~.
valuer or
inacarcd CXvalues (Kilgour and MfCauley
1986). Fwthamorc B&kcr and Genoway (1979)
observed that at thc rate of O.l%/mia the C
T
,
,
values dearly equal the upper LT valuer.
The splittail's high mermal tolaance (mean
am 9 4 4 T above acclimation tunperatures)
fiI3 well within wme of the widely distributed
freshwater Cdifomia cyprinids. which have
CT,,
6-WC above .oclimation tunpauure
(c.g.. Saauncrrto bkk6rh ~nhodond ~ k p i dotus, California m d H~~pcmlumu
~
cur hitch Lad& dlkan& and Saauncuto
qauw6sb &dwcheUus pnndir [Knigbt 19851:
tWad miosowPinuphrrlupmrnelus, Klunuhtui
-
--
ENVIRONMENTAL TOLERANCES OF SPLITTAIL
TABLE 3.-Mean
critical salinity maxima (CS,.
t
SEM) and estimated salinity tolerance levels (%o) for different time to loss of equilibrium (TLE) periods of differ,t splinail age-groups. Salinity tolerance levels were es"mated based on TLE regression equations from Table 2.
Criterion
salinity
Age 0 Age 1 Age 2
Age 2
($4 for
6-h TLE
12-h TLE
24-h TLE
48-h TLE
72-h TLE
96-h TLE
20
19
18
17
16
16
chub Gila bicolor bicolor, speckled dace Rhinichthys osculus, and blue chub Gila coerulea [Castleberry and Cech 19921). As estuarine fish, splittails
are subject to thermal fluctuations associated with
tidal cycles as well as die1 and seasonal fluctuations (Moyle 1976; Moyle et al. 1982; Daniels and
Moyle 1983). Their high thermal tolerance might
partly explain their survival in dead-end slough
and marsh environments.
Of concern, however, are thermal discharges
.
A
671
from electrical power generating plants such as
those in the Sacramento-San Joaquin Delta, whick
sometimes discharge water 13-15°C warmer tha,
the intake water (Finlayson and Stevens 1977; Pacific Gas and Electric 1992). In the vicinity of the
power plants, splittails make up 4-12% of the total
fish composition (Pacific Gas and Electric 1992).
and larvae are common (Wang 1986). If a wannwater discharge suddenly increases the ambient
temperature by 9-14T, all splittails in the vicinity
will die if they do not swim away. Although adult
fish might he able to escape, young fish probably
cannot. In addition, even if CT,,
is not exceeded,
temperature just below the CT,,
may cause structural anomalies (review by Reynolds and Casterlin
1980) that would increase the vulnerability of
young splittails to predation (Elliot 1981).
Power plant operations during winter might pose
a greater problem. Our results showed that in
spring, summer, and fall, a lZ°C increase would
be lethal, but in winter, an increase of only 9'C
would he lethal. However, in some cases, lower
ambient temperature may mitigate impact. For example, Bridges (1971) found that juvenile spot
Leiosfomus xanthurus were not killed by the increased temperature from power plant discharges
a c c l i m a t e d a t ZO:C
a c c l i m a t e d at 170C
a c c l i m a t e d at 12 C
S T A N D A R D
L E N G T H (cm)
FIGURE
4.-Mean (?SE) absolute critical swimming velocities of splittails in relation to mean ( t S E ) standard
lengths. Regression line is plotted for fish acclimated at 17°C only; N = 8-14: velocities lacking a common letter
are significantly different (P < 0.05).
YOUNG AND CECH
acclimated a t 2 0 1 ~
acclimated a t 170C
= acclimated a t 12 C
a
T
A
STANDA.RD
-
daring w i n e bccause the ambient water t a p e r was lower and muimum t e q m a t u m never
racbed a-.
An additional potential for mortality can OCCIU
during w i n e if power plant o p t i o n s am Shut
down. Many fish kills in winter art associated with
such shutdowns bccause exposure to cold after acclimation to w m water ir lethal to temperate fisha (SPuffcr 1980). If the watcr tunpenlure in the
vicinity of p o w e r p h t s Rlddenly dmpr to PC due
u, power plant shutdoam. it could be l a h d to the
rplimilr in the ama because, nglrdlcu of t h d
rdimation, the lowermcraul limitof any splitmil
yodmuptcrtcdisfc.
Although vflimrtion history M no iDdueaa
on the lower t h e d l i t of thc splittail, it M
significant effecton the u p p a t o l u a a a limit Inactse in mermrl8cclimrtion in .~companicdby
80 in-in
uppcrthtrnul limit. amponsecommom in o&wcyprini& (cg, S w t o bl-h
Caliiornia mach h&
ti .
Sacramento squawfish
[Knight 19851: fathead minnow, Mamath tui Chub.
speckled dace, blue chub [Casdebary lad M
19921) and many other fish species (Jobling 1981).
In addition to thermal acclimation. fish size
L E ' N G T H (cm)
(weight)also hsd an influenceon the splittail upper
thermal limit but not on the Iowa mcrmal limit.
As a splittail grows. its upper thennal limit de-
creases. Bcause splittails ue spawned in flooded
vegetation during late spring and d y summer
and ago0 fish habitats have peak water tunparives that am presumably wanner. these young fish
might be more adapted to higlsvampauunr than
age4 and age2 fish.
Sasonat upper ufe thumal limits for splituil
aabeinfdfmmthertimuedupperufemCrmal limits of differcat s p W agog~wprdmucd.tdi&nattcmparancsCruac l).POrwr.mplc ramma u p p a u f c thermal limit w ~ l l l dbe
based on 2o.c rcclimatiop spring-hlt upper i i t
orouldkbasedon I 7 Y : d i r m t i o a . u d ~ i m t ~
u p p a limit W on 1232 acclimation. Until a
mondetailcdrtudyiscwdudodoPmcthamal
cfiedr on survival. grow&. reproduction. and othcr splittail dyolmia, UMC u p p r ufe mamrllimi a c a n w v c i s the barez f o r c d m a i i n g d
uppa (henrul l a q u . m o of .gob.-1.
.nd
age-2 fish.
Estimated find r u n p e r a ~ r eprefcrenaes and
thermal growth optima based on Jobling (1981)
ENVIRONMENTAL TOLERANCES OF SPLITTAIL
equations were all higher than the acclimation temperatures and very much lower than the upper limits (Table 1). Under certain conditions, physiological processes may have different thermal optima
and these may result in changes in the preferred
temperature (Crawshaw 1977). For example, Brett
(1971) observed that sockeye salmon Oncorhyn&us nerka normally select 15°C. a temperature at
which active metabolism, sustained swimming
speed, and cardiac work are maximal. With unlimited food rations, young salmon sustain optimum
growth at this temperature. However, if rations are
limited, growth optima occur at a lower temperature (Brett et al. 1969; Brett and Higgs 1970), a
pattern also found in bluegill Lepomis macrochirus
(Stuntz and Magnuson 1976). western mosquitofish Gambusia offinis (Wurtsbaugh and Cech
1983), and lake trout Salvelinus namaycush (Mac
1985). Other nonthermal influences (e.g., season,
photoperiod, age, sex, maturity, light intensity, nutrition, health, salinity, disease, pollutants, biotic
interactions) can also affect thermal preference
(reviews by Reynolds and Casterlin 1980 and
Stauffer 1980).
Dissolved Oxygen
California cyprinids that live in warm lentic waters or intermittent, slow-flowing streams are tolerant of low DO levels (0.2-1.5 mg OzL; e&.
goldfish Carassius aurafus [Fry and Hart 19481:
fathead minnow, Klamath tui chub, speckled dace,
blue chub [Castleberry and Cech 19921). The splittail's preferred habitats (slow-moving sections of
rivers and sloughs) can have very low DO levels.
For example, in Buckley Cove (located in the section of the San Joaquin River known as the Stockton Ship Channel), the DO level can drop to 0.4
mg 02L at midday, 92.3 cm below the surface
(California Depmment of Water Resources 1994).
Fish generally avoid hypoxic conditions by moving away from them. However, when food ahundance is low, fish (especially benthic foragers)
readily forage in hypoxic waters (Rahel and Nutzman 1994). Splittails are benthic foragers (Caywood 1974: Daniels and Moyle 1983) and their
short-term low DO tolerancemay increase survival
by permitting foraging for invertebrates with low
DO requirements or foraging in hypoxic benthic
areas at times of low food availability. This low
DO tolerance is enhanced during winter because
the lower acclimation temperature results in lower
CDO,,,i, values (Figure 1). This is probably hecause at colder temperatures, fish have lower oxygen consumption rates (review by Fry 1970) and
673
thus can tolerate lower DO levels in the water.
Davis (1975) explained that at lower temperature,
fish hlood oxygen dissociation curves, w h ~ c hre
late blood percentage saturation to the PO2. typically shift to the left (indicating a lower oxygen
requirement to fully saturate the blood), decreasing
the Po2 threshold for hypoxia responses.
We cautioned against using the CDO,i, for establishing DO criteria. These values should be considered as extreme end points, approximating lethal limits. Complete loss of equilibrium by fish
(end point) indicates the point that experimental
conditions become detrimental to the fish. At this
point, the fish becomes disoriented and physically
unable to escape the harmful conditions which
could lead to its death (Becker and Genoway
1979). It has been recommended that studies on
the effects of low DO levels on growth be conducted to determine DO minimum criteria (Tarzwell 1958; Doudoroff and Shumway 1967, 1970:
Davis 1975: International Joint Commission 1979;
U S . Environmental Protection Agency 1986).
Salinity
Cyprinids are typically stenohaline freshwater
fishes, although a few California species have been
reported to tolerate salinity levels of 12-16%0 (e.g.,
common carp Cyprinus carpio [Geddes 19791,
goldfish [Threader and Houston 19831, Mojave tui
chub Gilo bicolor mohavensis [McClanahan et al.
19861). However, the splittail has an unusually
high salinity tolerance even when acclimated to
freshwater. Native California cyprinids that have
refuges in streams are rarely found at salinities
greater than 3%0 (P. Moyle, personal communication). It is not known if the remaining splittails
represent a more euryhaline genetic subset of the
splittail populations that once had a much broader
geographic range in California. It is suspected that
the salinity tolerance of this species comes from
having to survive in alkaline lakes on the valley
floor during long periods of drought (l? Moyle,
personal communication). Splittails are now mostly found in the estuary, living in environments
where salinity fluctuates due to flooding, drought,
and tidal and seasonal cycles. Forexample, salinity
levels in Suisun Marsh (where most of the age-1
and age-2 fish were collected) seasonally range
over 0-17%~ (Baracco 1980) and can increase
I%& over a 6-h tidal change (L.Millet, California
Department of Water Resources, personal communication). Splittails reportedly have been captured in waters with salinities as high as 18%0
(Meng and Moyle 1995).
i
674
YOUNG AND CECH
As a splittail grows, its salinity tolerance in- havior. Aleev (1969) analyzed the relationship becreases with age (Figures 2. 3). Many other fish tween & x i m u m body height ( H ) and standard
species have been found to have better salinity length (SL). and the ratio (Y) of anterior-H distolerances at more advanced stages of develop- tance (axial distance fmm the anterior end of the
ment (e.g.. channel catfish Ictalunupuncrarus [Al- fish to the level of H ) to the S L of '156 fish species.
Icn and Avault 19701, mach Rurilus rutifus (Scho- He concluded that for the most efficient swimmers
fer 19791. sharptooth catfish CInrias garicpinus (e.g., Atlantic huring CIupea hrengnr. bluefish
[Brim and Hecht 19891. chinook salmon ONO- Ponurfomur dtaNiX). H is 30% o r less of S L and
diynchus~shawytcha[Clarke et al. 19811. rainbow Y is between 0.40 and 0.55. The splittail's H of
trout Oncorhynchus mykiss [Johnsson and Clarke 19% of SL and Y of 0.48 categorize it as an effi19881). This phenomenon is probably related to cient swimmer. Swimming is very important for
body surface :volume ratio (Parry 1960). to func- splittails' survival becruse the fish migrateduring
tional development of the osmorcgulatory system high wintcr-spring runoff to flooded vegetation for
(Hoar 1988). o r to ontogenic changcs in hemoglo- spawning and forage in these periodidly flooded
bin (Perez and Maclean 1976). Given the great habitats as young (Caywood 1974). Daniels and
differences in size between a g e 4 to age-2 sptit- Moyle (1983) obrerved thatthe spawning success
tails, the rcduced body surface: volume d o in of rplitUils was positively correlated with river
larger fish may significantly contribute to its in- outflows; Caywood (1974) also observed Cbat a
a a s d salinity tolennct. In salmonid specks. rtloccsrful year-class was ryociatcd with winter
growth is accompanied by functional development runoff utffciently high to flood tbc paipbcnl arof ~ b n ~ ~ r e g u l a t organs
o r y such as gill% kidneys. eas of the cs-.
In w swimming tats.many
urinary bladder, and intestinexnd development of splitullr held (or tried to hold) onto the nprtreMl
osmorcgulatory hormones ( r e v i e d by Hoar raeen of fJ~swimmingchamber with thcirmoutbs
1988). We did not examine the development of when'velocity appmachcd meir Ud, and it is psplimil osmorcgulatory organs that prertunably sible that splittails hold on to vegetation or&
.ccompanied their growth The development of subfcaatrcs to maintain station againa
W organs may not be as dramatic as those in amng cumnts.
anadmmous salmonids. In the Mozambiquetildpia
Mean absolute Ud,( d s ) increased with splitOruxhromis mosambicus, a second hemoglobin tail length, which is typical for many fishes beappears a t 47 d that has a higher afiinity for & at cause of the improved efficiency of the caudal' fin
1977). Similarly. mean relative U* (body
hiber osmotic pressure and t c q c r a N r e and may
u d in toleranm to higher salinity and tcmpcnNre length&) davcrrod with splittail length. M is the
(Puczand Maclean 1976). This may not be the cd.sc for many other fish&. Thc decrease in relative
case for the splittail because splittail growrh is not Ud with length is probably becruse the power
accompanied by an increase in its qpper thamal ncedcd to overcome drag itmenses exponentially
toluance.
with body length (Weihs 1977); also. the maximum
In nature, adult splittails migrate upstream into stride frequency is rcduced in larger fish due to
freshwater to spawn in flooded veguation. The increavd contraction times of swimming muscles
larvae remain in shallow, weedy areas, and a g e d with the lengib of the fish (Wtrdle 1977).
ftsh @iobably larger than our a g e 4 fish) migrate
Inin tunpcnturr resulted in gnxter
do war^ with river flows into shallow. pm- swimming performance by small age4 and We-2
ductive warvf of the ertuary (Wang 19%; Meng rplituilr. Inin acclimation tunof
and Moyle 1995). Results of the salinity etdunncc . 3.C for small .ge-O fish and 5.C for qe-2 fi,&
tests confirmed that our a g e d fish w u e much wm increased absolute U& by 11 and 25 cml& nd t i v c to i n d salinity levels than the a g e 1 ipcuively, and iaacaxdrelative U d in age-2 fish
and age-2 6sh. 'Ihc longer-term TLE results (Table by ,126 body lcngthsls. Similar observatioqs of
3) arc rsoomrnended for detumining splituil sa- i n d U* with i
d rempenavc have
ban reported for other fish species. For w r a m p l ~
linity rcquinments.
for the fry of four salmonid specks, an inS W g Pcrfomf(u~cc
of X ~ r e s u l t e din a 5 - c d s (-2-body kngthls)
Splittail swimming performance is conriaart iaaease in Ud (Heggcnes and Traaen 1988): for
with the species' streamlined body form and deep- Largunouth bass Microprenu salnwidu. an inIv forked caudal fin hence the common name) and aease of I I T resulted in an increase of 0.61-1.47
(We
ENVIRONMENTAL TOLERANCES OF SPLITTAIL
tuna Thunnus albacares, swimming speed was positively correlated with red muscle temperature (DiZen et al. 1977). Low temperature generally results
in decreased swimming performance, probably as
a result of biochemical (e.g., enzymatic) and physiological changes (Wardle 1980). The general increase in fish swimming performance with thermal
increase reportedly derives from decreases in
swimming muscle contraction times (Wardle 1980)
and increased aerobic power output available from
red muscle fibers at higher environmental temperatures (Heap and Goldspink 1986). Decreased
muscle contraction time at higher temperature increases tail heat frequency, resulting in better
swimming performance (Batty et al. 1991). Increase in aerobic power output from red muscles
at higher temperatures results in white muscle recruitment at higher speed (Rome et al. 1984; Heap
and Goldspink 1986). For example, in common
carp at lo", white muscle fibers were recruited
at 1.25-1.56 body lengthds, but at 20°C they were
recruited at higher speed of 2.0-2.5 body lengthsls
before getting fatigued (Rome et al. 1984). As
swimming velocity increases, there is a gradual
recruitment of red (aerobic) muscle fibers until
they are all utilized, after which white (anaerobic)
muscle fibers are recmited in proportion to the
swimming velocity. At lower temperature, fish will
have recruited all their red muscle fibers at lower
swimming speed, and the recruitment of white
muscle will occur earlier, resulting in the fish
reaching fatigue at lower swimming velocity
(Randall and Brauner 1991).
Although splittails were shown to be good
swimmers by their high UCritvalues, no swimming
endurance tests were conducted. If the criterion
for water diversion screen approach velocity is
based solely on Uctitresults, as in the case of other
fish species (Clay 1995), then the recommended
approach velocities of 6 cm/s and 10 cm/s by the
USFWS (1994) for delta smelt Hypomesus tmnspacificus (a threatened native species of the Sacramento-San Joaquin estuary) and 12 cmfs for salmonid fry would pose no problem for splittails
more than 2 cm in SL.
Available data on California cyprinids show an
overall pattern of similar environmental tolerances, perhaps reflecting genealogy. Like other native California cyprinids, especially those in rivers
and lakes, splittails are well adapted to wet and
dry climatic cycles (Meng and Moyle 1995), as
reflected in their wide tolerances to thermal
changes and low dissolved oxygen. Their exceptionally high salinity tolerance probably enhanced
675
survival in the estuary. Many of the state's native
cyprinid populations have declined (e.g., Mojave
tui chub), have become extinct (e.g., Clear Lake
splittail Pogonichthys ciscoides) or have been extirpated from state waters (bonytail Gila elegans)
due to habitat loss or pressure from introduced
species, sucb as the common carp (Moyle 1976).
Abiotic environmental factors including temperature, dissolved oxygen, salinity, and water current
do not appear to limit the splittail's distribution
and survival during years of high precipitation.
However, California's highly regulated river and
reservoir system restricts the occurrence and duration of floods. The splittail's high tolerance to
thermal change, low dissolved oxygen, and high
salinity presumably permit extended occupancy,
especially by age-l and older fish, of the dead-end
sloughs that may be an overly harsh habitat for
potential predators or competitors. Although their
general hardiness probably contributes to their survival, splittails have been found mostly in the estuary, which is less than a third of the species'
former range (Meng and Kanim 1994). This indicates that the conditions contributing to their
habitat restriction (e.g., extended drought, water
diversion, inadequate seasonal flooding, habitat alteration, water pollution, and biotic factors such
as predation or competition) are extremely serious
or that other life stages (i.e.. egg, larvae, and adult
spawners) are significantly less hardy. These alternatives deserve additional study.
Acknowledgments
This study was supported by the Interagency
Ecological Program for the San Francisco
BayDelta. This cooperative program includes
the California Department of Fish and Game
(CDFG), California Department of Water Resources (CDWR), State Water Resources Control
Board, the USFWS, the U S . Bureau of Reclamation, the U S . Geological Survey, the National
Marine Fisheries Service, the U S . Environmental
Protection Agency, and the U S . Army Corps of
Engineers. P. Herrgesell (CDFG) and R. Brown
(CDWR) facilitated this support. Splittails were
collected by S. Matern, L. Hess, S. Siegfried, G.
Weis, J. Morinaka, L. Grimaldo, R. Baxter, H. Bailey, T. Hampson, and the CDFG Fall Midwater
Trawl Survey and Delta OutEowfSan Francisco
Bay Survey groups headed by K. Hieb and J. Arnold. We thank P. Lutes and B. Bentley of the
University of California, Davis, Aquaculture and
Fisheries Program for assistance in the fish maintenance system; L. Grimaldo for identifying and
.,
1"
,,
676
Y O U N G A N D CECH
1. Wang for confirming identifications of the small
agc-0 fish; H. Zhou for statistical advice; A. Farrcll
for advice regarding Figure 3; K. Jacobs and H.
Proctor (CDWR) for the water quality monitoring
data; and P. Moyle. R. B u t - L. Holland-Bartels.
L. Brown. B. H h l d . I. Stauffcr. and o n e anonymous reviewer for their valuable comments and
suggestions on the manuscript. We also thank D.
Shigematsu, D. Irwin. M. Thibodcau. S. Cummings. C. Porter. I. Lorcnzo. I. Heublcin. I. Khoo.
G. Cech. L. Brink. and.'F Moberg for technical
assistance.
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Acaplcd April 24. 1996