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Marine and Freshwater Behaviour and
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Osmoregulatory capabilities of the
gray snapper, Lutjanus griseus: salinity
challenges and field observations
Xaymara Serrano a , Joseph Serafy a b & Martin Grosell a
a Division of Marine Biology and Fisheries, University of Miami,
Rosenstiel School of Marine and Atmospheric Science, 4600
Rickenbacker Causeway, Miami, FL 33149, USA
b Southeast Fisheries Science Center, National Marine Fisheries
Service, 75 Virginia Beach Drive, Miami, FL 33149, USA
Available online: 15 Jun 2011
To cite this article: Xaymara Serrano, Joseph Serafy & Martin Grosell (2011): Osmoregulatory
capabilities of the gray snapper, Lutjanus griseus: salinity challenges and field observations, Marine
and Freshwater Behaviour and Physiology, 44:3, 185-196
To link to this article: http://dx.doi.org/10.1080/10236244.2011.585745
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Marine and Freshwater Behaviour and Physiology
Vol. 44, No. 3, May 2011, 185–196
Osmoregulatory capabilities of the gray snapper, Lutjanus griseus:
salinity challenges and field observations
Xaymara Serrano
a
*, Joseph Serafy
a,b
and Martin Grosell
a
a
Division of Marine Biology and Fisheries, University of Miami, Rosenstiel School of Marine
and Atmospheric Science, 4600 Rickenbacker Causeway, Miami, FL 33149, USA;
b
Southeast Fisheries Science Center, National Marine Fisheries Service,
75 Virginia Beach Drive, Miami, FL 33149, USA
(Received 30 January 2011; final version received 25 April 2011)
We investigated the osmoregulatory responses (plasma osmolality and
blood hematocrit) displayed by the gray snapper 6–192 h after abrupt
changes in ambient salinity. Fish were challenged with six different salinity
treatments including a control (0, 5, 30, 50, 60, and 70 ppt) and blood
samples were collected at various time points post-transfer. Gray snapper
across all size classes tested (13.5–24.5 cm total length) acclimated
successfully to hypo- and hyper-saline environments (0–60 ppt) after an
adjustment period of 96 h. However, abrupt transfers to 70 ppt resulted in
100% mortality within 48 h. Laboratory results were then compared with
field measurements obtained after fish were captured in low salinity
(0–4 ppt) or marine (30 ppt) habitats, suggesting that osmoregulatory
processes occurred similarly in both settings. Overall, findings suggest that
gray snapper possess similar or higher osmoregulatory capabilities
compared to many euryhaline species examined to date, and thus should
be considered a euryhaline species.
Keywords: tolerance; osmoregulation; gray snapper; Lutjanus griseus;
acclimation; euryhalinity; Everglades restoration
Introduction
Salinity acclimation is a complex process that involves a set of physiological
responses in multiple osmoregulatory organs (i.e. gills, intestine, and kidneys; Lin
et al. 2004; Marshall and Grosell 2005), and is known to induce changes in
parameters such as plasma osmolality (e.g. Crocker et al. 1983; Nonnotte and
Truchot 1990; Varsamos et al. 2002), Na
þ
/K
þ
-ATPase activity (e.g. Jensen et al.
1998; Arjona et al. 2007), and blood hematocrit (e.g. Leray et al. 1981; Brown et al.
2001; Denson et al. 2003), among others. To date, much of the work on acute
osmoregulatory responses of fish to salinity change has been conducted on
euryhaline species that either encounter different salinity levels in their habitat or
move among distinct habitats throughout their life history (e.g. salmonids).
Typically, these responses begin with a ‘‘crisis’’ period characterized by an increase
or decrease in plasma osmolality, followed by a ‘‘regulatory’’ phase as ions reach
*Corresponding author. Email: xserrano@rsmas.miami.edu
ISSN 1023–6244 print/ISSN 1029–0362 online
ß2011 Taylor & Francis
DOI: 10.1080/10236244.2011.585745
http://www.informaworld.com
Downloaded by [University of Miami] at 13:40 13 December 2011
steady-state levels, usually within 2 weeks post-transfer (e.g. Ferraris et al. 1988;
Mancera et al. 1993; Arjona et al. 2007); unless acclimation to the new salinity level is
unsuccessful. These phases occur because to counteract the large passive forces that
dominate ion and water movement in the ‘‘crisis’’ period, the permeability of plasma
membranes and tight junctions must be altered, and ion uptake (or extrusion)
systems must be activated during the ‘‘regulatory’’ phase (Ferraris et al. 1988).
Estuaries are generally characterized by wide salinity fluctuations over short time
scales that may vary seasonally with rainfall, river discharge, tidal fluctuations,
evaporation (Tabb and Manning 1961) and/or anthropogenically-driven alterations
of freshwater flow (Wakeman and Wohlschlag 1983; Serafy et al. 1997). As a result,
the success of many species that are either facultative or obligate users of estuaries
may depend on the species-specific capacity to tolerate changes in body fluid
osmolality, osmoregulate and/or engage in more immediate behavioural responses
(Serafy et al. 1997; Serrano et al. 2010). The expectation is that species with juvenile
stages that inhabit estuaries (e.g. Sciaenidae) will be efficient osmoregulators
(Varsamos et al. 2005). In contrast, species with juvenile stages that prefer more
stable salinity regimes are expected to show more limited osmoregulatory abilities
(Dall 1981). Further, while working in Louisiana estuaries, Yokel (1966) contended
that young individuals from different species tended to be more tolerant of low
salinities, whereas adults were less dependent on estuarine areas (spent more time at
sea), and therefore, were expected to be more tolerant of high salinities.
Gray snapper Lutjanus griseus, a species of high economic and ecological
importance in South Florida, USA (Tilmant 1989; Burton 2001; Denit and
Sponaugle 2004; Serafy et al. 2007), is characterized as an estuarine transient
(Ley et al. 1999), but has been included in a list of species that are marine as adults,
but euryhaline as larvae and juveniles (Tabb et al. 1962; Beck et al. 2001). While
juveniles occupy a variety of nearshore habitats with relatively low salinities
(down to freshwater), adults are predominantly marine, but also frequent estuaries
and nearshore habitats, particularly to feed (Starck and Schroeder 1970; Chester and
Thayer 1990; Serafy et al. 2003; Wuenschel and Martin 2006). It is then expected that
as the gray snapper performs inshore–offshore migrations throughout its life span,
the change in external salinity results in physiological (osmotic) stress. Ley et al.
(1999) reported the most extensive salinity range for gray snapper across all sizes
(0–60 ppt) and Rutherford et al. (1989) the highest salinity (66.6 ppt); however, these
values were based strictly on field observations. Serafy et al. (1997), however,
reported that juvenile gray snapper (7.3–8.2 cm total length, TL) survived a brief
(24 h) exposure to freshwater with 0% mortality in the laboratory, but this study
only examined survival and did not target larger size classes, especially those that are
vulnerable to hook-and-line fishing. This information is relevant for gauging
downstream effects of Florida Everglades Restoration (focused on changing the
quantity, quality and timing of freshwater flow in the region; Serafy et al. 2007),
since adults have been suggested to be less tolerant of salinity fluctuations than
younger fish (Starck 1964; Starck and Schroeder 1970).
The main objective of this study was to advance the current understanding of the
basis and limits of the gray snapper euryhalinity. This constitutes the first assessment
of the acute osmoregulatory responses following salinity change of a reef fish, using
size classes that are directly vulnerable to hook-and-line fishing. Overall, we used a
combination of laboratory and field observations on gray snapper to: (1) characterize
the osmoregulatory responses following changes in environmental salinity;
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(2) determine its limits of salinity tolerance; and (3) assess potential differences
associated with the size class of fish tested. For gray snapper to be considered a truly
euryhaline species, we expected transient or no osmoregulatory disturbances in plasma
osmolality and/or blood hematocrit after transferring fish from seawater to various
hypo- and hyper-saline media. In addition, we expected responses to be unrelated to
fish size. Finally, fish collected in the field were expected to display plasma osmolalities
not significantly different from fish in the laboratory at similar salinities. As such, this
is the first ever attempt to compare osmoregulatory laboratory measurements with
field results obtained directly after fish capture.
Materials and methods
Experimental animals
Subadult and adult gray snapper ranging from 13.5 to 24.5 cm TL were collected
from nearshore marine (30–34 ppt) habitats within Biscayne and Florida Bays using
hook-and-line fishing gear. Upon collection, fish were transported to the laboratory
in coolers and held in outdoor tanks with flowing, aerated seawater for a period of
2–3 weeks prior to experiments. Water temperature and salinity in the tanks
averaged 27.8C and 31.5 ppt. Live juvenile pink shrimp Farfantepenaeus duorarum
were provided as food, three times per week (3% body weight per feeding).
Experimental protocol
Five different salinity treatments were chosen to encompass the widest known range
reported for this species. The treatments were 0, 5, 30 (full-strength seawater), 50,
and 60 ppt. A sixth treatment was selected (70 ppt) outside the range reported for this
species to test for an upper lethal salinity limit. Individuals maintained in full-
strength seawater (30 ppt) throughout the duration of the experiment were
considered the control group. Elevated salinities were achieved by addition of
natural sea salts (Instant Ocean mix) to seawater, while lower salinities were
established by adjusting a mix of seawater and dechlorinated Miami city tap water to
the desired salinity. In all cases, transfer of fish to various salinities was completed
within 10 min. To avoid crowding stress, disease or mortality associated with high
ammonia levels, fish were randomly sorted and transferred individually into 30 L
aquaria equipped with biofilters and aeration. Fish were starved for 24 h before and
after transfers, after which feeding was resumed according to the schedule described
above. Fecal matter and other debris were siphoned from tanks 1 day after feeding
and a 25% volume water change was performed at 48, 96, and 144 h. Prior attempts
to draw multiple blood samples from the same individuals over time resulted in
excessive mortalities, especially at extreme salinities. Therefore, individual fish were
sampled only once per salinity treatment as described below. Table 1 presents the
number and size range of fish sampled at each time point within each salinity
treatment.
Sample collection from abrupt transfers
Fish were lightly anesthetized with a 0.1 gL
1
MS-222 (3-aminobenzoic acid ethyl
ester, Argent Labs) prior to blood sampling. One fish from each salinity treatment
Marine and Freshwater Behaviour and Physiology 187
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was sampled at 6, 24, 48, 96, and 192 h post-treatment by caudal puncture using a
1 mL heparinized syringe fitted with a 21 gauge needle. Approximately 200–400 mL
of blood was obtained from each fish, a portion of which was extracted into 75 mL
capillary tubes for hematocrit determination. The capillary tubes were centrifuged
for 3 min and the volume of red blood cells was then measured as a percentage. The
rest of the sample was then centrifuged at 16,000gto separate plasma and stored at
20C until analysis. Plasma osmolality was measured using a Wescor Vapro 5520
vapor pressure osmometer (Wescor Inc., Logan, UT). Treatment water osmolality
was also determined as reference values (Table 1).
Sample collection in the field
Using the same methods described above, additional fish were sampled in the field
within 15 min of capture by hook-and-line. Salinity at each capture site was recorded
Table 1. Number and size ranges (TL) of fish sampled at each time point within each salinity
treatment.
Salinity
treatment (ppt)
Water
osmolality
(mOsm kg
1
)
Sample time
point (h) N
Fish size
range (cm)
0 25 6 7 13.5–20.5
24 7 14.5–24.5
48 6 14.0–21.0
96 5 14.5–22.5
192 6 13.5–21.0
5 143 6 6 14.0–20.5
24 6 14.5–21.0
48 6 14.0–20.0
96 6 14.3–21.0
192 6 14.0–22.0
30 (control) 934 6 6 14.3–22.5
24 8 16.0–21.5
48 8 16.0–24.0
96 7 15.5–19.0
192 6 16.0–24.0
50 1522 6 6 14.7–21.5
24 6 14.5–22.5
48 6 15.5–21.5
96 6 17.5–21.0
192 6 17.5–20.5
60 1857 6 6 13.5–23.0
24 6 14.3–16.7
48 6 19.0–21.5
96 6 13.5–15.5
192 5 15.5–22.5
70 2150 6 6 16.5–22.0
24 6 15.0–23.0
Notes: Individual fish were sampled only once at any given time point.
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using a calibrated refractometer. This approach was used to compare plasma
osmolalities obtained in the laboratory after abrupt transfer with values observed in
fish in low salinity (0–4 ppt) versus marine (30 ppt) habitats.
Data analysis
Examination of data indicated normality and homogeneity of variances; thus
laboratory and field values were reported as means 1 standard error. The
significance of differences among salinities was determined using one-way
ANOVA, with salinity as the main factor. When statistical significance was revealed
(i.e. P50.05), a Dunnet’s post hoc test was used for multiple comparisons of the
means. Finally, backward stepwise regression was used to evaluate the possible effect
of fish size in relation to plasma osmolality and salinity treatment.
Results
Abrupt transfers
Overall, no mortalities occurred in fish from salinity treatments ranging from 0 to
60 ppt; however, all fish exposed to 70 ppt died within 48 h of transfer. Mean plasma
osmolalities (Figure 1) ranged from 269 to 475 mOsm kg
1
for fish transferred to
salinities from 0 to 60 ppt, consistent with ranges observed in many other fresh,
estuarine and marine teleosts (260–400 mOsm kg
1
; Varsamos et al. 2005).
Figure 1. Changes in plasma osmolality for gray snapper Lutjanus griseus following abrupt
transfer to different experimental salinities. All fish exposed to 70 ppt died within 24–48 h
post-transfer. Asterisks correspond to significant statistical differences with respect to controls
(P50.05; analysis of variance and Dunnet’s post hoc comparison test).
Marine and Freshwater Behaviour and Physiology 189
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In control fish (30 ppt), osmolality was maintained at 367 1.32 mOsm kg
1
(n¼35). In transfers to treatments between 5 and 50 ppt, plasma osmolality was
maintained at levels very similar to controls throughout the duration of the
experiment. Transfers to 0 ppt, however, significantly decreased plasma osmolality
to 310 7.53 mOsm kg
1
(n¼7) by 6 h post-transfer, followed by a further
decrease to 269 12.75 mOsm kg
1
(n¼7) at 24 h. By 48 h, values increased to
271 11.46 mOsm kg
1
(n¼6), and were no longer different from the controls at
192 h, with a value of 359 13.73 mOsm kg
1
(n¼6). In contrast, transfer to 60 ppt
significantly increased plasma osmolality to 445 13.39 mOsm kg
1
(n¼6) at 24 h
post-transfer, with a further increase to 475 5.45 mOsm kg
1
(n¼6) at 48 h. Mean
osmolality had decreased by 96 h to 436 10.09 mOsm kg
1
(n¼6), and was no
longer different from the control at 192 h (439 7.71 mOsm kg
1
;n¼5), despite
water osmolality being around 1850 mOsm kg
1
(Table 1). Finally, fish transferred to
70 ppt significantly increased plasma osmolality to 437 15.64 mOsm kg
1
(n¼6) at
6 h post-transfer, a value that increased to 561 41.29 mOsm kg
1
(n¼6) by 24 h,
and resulted in death for all fish before 48 h. Overall, for all six salinity treatments,
backwards stepwise regression analysis suggested that plasma osmolality was only
related to salinity treatment, was unrelated to fish size and that there was no salinity
treatment by size interaction effect.
Mean hematocrit measurements (Figure 2) ranged from 31% to 43% for fish
transferred to salinities from 0 to 60 ppt, consistent with normal ranges observed in
many other species (32–43%). In control fish (30 ppt), hematocrit was maintained at
35 1.32% (n¼35). In transfers to 5, 50 or 60 ppt, blood hematocrit was maintained
Figure 2. Changes in blood hematocrit for the gray snapper L. griseus following abrupt
transfer to different experimental salinities. All fish exposed to 70 ppt died within 24–48h post-
transfer. Asterisks correspond to significant statistical differences with respect to controls
(P50.05; analysis of variance and Dunnet’s post hoc comparison test).
190 X. Serrano et al.
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at levels very similar to controls throughout the duration of the experiment, and no
significant differences among treatments were observed. Although transfers to 0 ppt
significantly increased blood hematocrit to 43 4.1% (n¼7) at 6 h post-transfer,
values had returned to control levels by 24 h (41 1.53%; n¼7). The opposite
occurred upon transfer to 70 ppt – a significantly reduced blood hematocrit
(274.5%; n¼6) was observed at 6 h post-transfer. However, by 24 h post-transfer,
hematocrit levels had returned to control levels (35 1.16%; n¼6) even though all
fish died. Because post-mortem blood sampling was not possible hematocrit values
after 24 h are unknown.
Field collections
Overall, fish collected in low salinity habitats (0–4 ppt) displayed a high variability in
plasma osmolality values, but these values were not significantly different from those
observed in the laboratory after transfer to freshwater (Figure 3). On the other hand,
fish collected in marine habitats displayed low variability in plasma osmolality values
that were significantly higher than those observed in the laboratory controls.
Discussion
Abrupt transfers
This study investigated the osmoregulatory responses in plasma osmolality and
blood hematocrit displayed by the gray snapper after abrupt changes in ambient
salinity. Fish were challenged with six different salinity treatments including a
200
250
300
350
400
)tpp 03~( retawaeS)tpp 4-0( ytinilas woL
Plasma osmolality (mOsmKg
-1
)
Lab Field
(26) (11) (35) (42)
*
200
250
300
350
400
)tpp 03~( retawaeS)tpp 4-0( ytinilas woL
Plasma osmolality (mOsmKg
-1
)
Lab Field
(26) (11) (35) (42)
*
(26) (11) (35) (42)
*
Figure 3. Comparison of plasma osmolalities from gray snapper L. griseus in the
laboratory after transfer to either low salinity (0 ppt) or seawater (30 ppt, control) with gray
snapper after capture in the field at low salinities (0–4 ppt) and full-strength seawater
(30 ppt). Asterisks correspond to significant statistical differences between field and
laboratory results within each salinity ( P50.05; analysis of variance and Dunnet’s post hoc
comparison test).
Marine and Freshwater Behaviour and Physiology 191
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control (0, 5, 30, 50, 60, and 70 ppt) and blood samples were collected at various time
points post-transfer. Overall, results indicated no significant osmoregulatory
disturbances in the salinity range of 5–50 ppt. In contrast, at extreme salinities of
0 and 60 ppt, significant but transient changes in osmolality and/or hematocrit were
observed. However, by the end of the 192 h experimental period, both parameters
showed no significant differences with respect to control values, suggesting a
successful adaptation to these new salinity levels despite the large changes in
environmental salinity. Finally, the lethal salinity, defined by the concentrations
where a constant osmolality cannot be maintained (Foss et al. 2001), was observed at
70 ppt. However, the ability of the gray snapper to recover hematocrit to control
values within 24 h post-transfer to 70 ppt, even preceding 100% mortality, suggests
that fish were able to regain water balance even when they were unable to recover
salt balance.
From the few studies that have examined the effect of body size in euryhalinity,
the effect appears to be species-dependent. For example, after transfers from
seawater to both hypo- and hyper-saline media, Ferraris et al. (1988) found that
smaller milkfish Chanos chanos, not only had longer recovery times, but larger
deviations from control osmolality than larger fish (260 g) compared to milkfish (120
and 40 g). In contrast, Jensen et al. (1998) found no difference in parameters
observed during salinity acclimation when comparing large versus small European
sea bass Dicentrarchus labrax (89 g compared to 6.2 g sea bass), suggesting that this
species is euryhaline at all developmental stages. In this study, the range of sizes of
gray snapper tested varied greatly in every treatment (mean length in each ranged
from 14.1 to 23 cm TL, thus comprising both sub-adults and adults), but results
indicated no significant relationships between size and osmolality of fish tested in
any of the salinity treatments. Overall, these findings contradict previous field-based
observations (i.e. Starck 1964; Starck and Schroeder 1970), and suggest that larger
size classes of gray snapper may be equipped with the same efficient osmoregulatory
capabilities that juveniles possess. Thus, based on the results from this study, we
contend that gray snapper is a truly euryhaline species.
There is a paucity of literature on the immediate osmoregulatory responses for a
single species when abruptly transferred from seawater to both hypo- and hyper-
saline experimental media. Such information is available for more commonly studied
species including the European sea bass (Jensen et al. 1998; Varsamos et al. 2002),
red drum Sciaenops ocellatus (Crocker et al. 1983; Wakeman and Wohlschlag 1983),
milkfish (Ferraris et al. 1988) and Gulf toadfish Opsanus beta (Serafy et al. 1997;
Genz et al. 2008), among others. From these studies, it appears that the salinity range
to which gray snapper was able to acclimate during this study exceeded
corresponding ranges for the species listed above, particularly at the lower end of
salinity. For example, the Gulf toadfish, which is an important component of gray
snapper diet (Starck and Schroeder 1970), can successfully acclimate to hyperosmotic
salinities of up to 60 ppt with a slightly faster recovery time than the gray snapper
(596 h; Genz et al. 2008), but cannot survive in salinities of or lower than 0.5 ppt for
more than a week even after gradual acclimation (McDonald and Grosell 2006).
Similarly, the European sea bass can osmoregulate well over the same wide range of
salinities used in this study (0 to 60 ppt; Jensen et al. 1998). However, the few deaths
recorded in the initial adjustive phase of sea bass after transfer to freshwater also
suggest that the lower salinity threshold may fall between 5 and 0 ppt; contrasting
with the ability of gray snapper to osmoregulate well in freshwater.
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Field collections
To the best of our knowledge, this is the first study to compare measured plasma
osmolalities directly from fish captured in the field with laboratory-measured
osmoregulatory data. Overall, results showed that all size classes of gray snapper
captured within the same salinity in the field (15.5–31 cm TL in freshwater
collections, 9–30 cm TL in marine collections, respectively) displayed similar
osmoregulatory profiles. In addition, fish collected in low salinity habitats (salinities
ranging from 0–4 ppt) displayed osmolalities not significantly different from fish in
the laboratory transferred to freshwater. The high variability in the osmolalities
displayed in field-captured fish at these low salinities likely reflect differences in the
time that each fish had spent at the salinity of capture (i.e. indicative of migration
among habitats). In contrast, field-collected fish in full-strength seawater not only
displayed a smaller variability in osmolality values (consistent with the fact that these
areas tend to have stable salinities), but also unexpectedly displayed significantly
higher osmolality values compared to those in the laboratory at similar salinities.
These unexpected results may be explained by feeding differences in field versus
laboratory fish. While in the laboratory fish were fed solely with shrimp, in the field,
fish is the most prominent dietary component, particularly in larger size classes
(Starck and Schroeder 1970). Supporting this idea, Taylor and Grosell (2006) found
that a large meal of fish fed to the Gulf toadfish provided a substantial K
þ
and Ca
2þ
load that significantly increased the osmolality measured when compared to a squid-
based diet. Alternatively, these higher than expected osmolality values in field-
captured fish at high salinities could have resulted from capture and/or handling
stress, albeit unmeasured. Further, osmolality has been shown to be affected by
handling and/or transporting stress (Redding and Schreck 1983; Denson et al. 2003),
which may explain why most osmoregulatory studies have an acclimation period
after fish capture and/or rearing. Whichever the case, it is important to emphasize
that field-measured osmoregulatory data are only suggestive of the conditions under
which this species is found in nature.
Ecological implications
In South Florida, alteration of freshwater flow has changed the salinity regimes and
degraded estuarine and nearshore habitats occupied by the gray snapper (Serafy
et al. 1997). Further, salinity is expected to undergo more significant changes with
the implementation of the Florida Everglades restoration, which aims at restoring
more natural, mesohaline salinity regimes within many of the South Florida’s coastal
bays (Walters et al. 1992; Harwell et al. 1996; Serafy et al. 1997). Gray snapper and
other species that are subjected to pulses of freshwater flow can either remain in these
areas, if physiologically capable, or leave and risk predation and/or food scarcity
while seeking a more benign habitat (Serafy et al. 1997). This study suggests that
even though freshwater pulses may represent a significant osmoregulatory challenge
to the gray snapper, this in itself will not lead to death. Gray snapper faced with a
freshwater pulse in their natural habitat are capable of remaining in such an area,
although their preferred food items may not. Early observations that multiple blood
drawings from the same individuals resulted in high mortalities (especially at
salinities of 0 and 60 ppt) suggest that while this species is highly tolerant of salinity
changes, when combined with other stressors (e.g. capture on hook-and-line), lesser
Marine and Freshwater Behaviour and Physiology 193
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salinity challenges than those tested may be lethal. Thus, research on the effects of
multiple stressors on the osmoregulatory capabilities of this species is warranted.
Acknowledgements
This work was conducted under Special Activity License no. 07SR-1015 (Florida Fish and
Wildlife Conservation Commission) and UM Institutional Animal Care and Use (IACUC)
protocol No. 07-017 (2007–2009). Financial support was provided through a fellowship from
NOAA’s Living Marine Resources Cooperative Science Center, the Cooperative Unit for
Fisheries and Education Research, RECOVER (US Army Corps of Engineers and South
Florida Water Management District) funds awarded to J. Serafy and NSF (IAB 0714024 and
0743903) funds awarded to M. Grosell. We are indebted to the technical support provided in
the lab and field by B. Teare, N. Hammerschlag (South Florida Student Shark Program),
D. Snodgrass, J. Stieglitz, the Audubon of Florida and members of the Grosell laboratory at
the University of Miami. D. Die and J. Lorenz contributed substantial guidance and supplies
facilitating this research.
References
Arjona F, Vargas-Chacoff L, Ruiz-Jarabo I, Martı
´n del Rı
´o M, Mancera M. 2007.
Osmoregulatory response of Senegalese sole (Solea senegalensis) to changes in environ-
mental salinity. Comp Biochem Physiol A. 148:413–421.
Beck M, Heck K, Able K, Childers D, Eggleston D, Gillanders B, Halpern B, Hays C,
Hoshino K, Minello T, et al. 2001. The identification, conservation, and management of
estuarine and marine nurseries for fish and invertebrates. Bioscience. 51(8):633–641.
Brown J, Moore W, Quabius S. 2001. Physiological effects of saline waters on zander. J Fish
Biol. 59:1544–1555.
Burton M. 2001. Age, growth, and mortality of gray snapper, Lutjanus griseus, from the east
coast of Florida. Fish Bull. 99:254–265.
Chester A, Thayer G. 1990. Distribution of spotted seatrout (Cynoscion nebulosus) and gray
snapper (Lutjanus griseus) juveniles in seagrass habitats of western Florida bay. Bull Mar
Sci. 46:345–357.
Crocker P, Arnold C, DeBoer J, Holt G. 1983. Blood osmolality shift in juvenile red drum,
Sciaenops ocellatus L. exposed to freshwater. J Fish Biol. 23:315–319.
Dall W. 1981. Osmoregulatory ability and juvenile habitat preference in some penaeid prawns.
J Exp Mar Biol Ecol. 54(1):55–64.
Denit K, Sponaugle S. 2004. Growth variation, settlement, and spawning of gray snapper
across a latitudinal gradient. Trans Am Fish Soc. 133:1339–1355.
Denson M, Evin R, Stuart K, Smith T. 2003. Effects of salinity on growth, survival, and
selected hematological parameters of juvenile cobia Rachycentron canadum. J World
Aquacult Soc. 34(4):496–504.
Ferraris R, Almendras J, Jazul A. 1988. Changes in plasma osmolality and chloride
concentration during abrupt transfer of milkfish (Chanos chanos) from seawater to
different test salinities. Aquaculture. 70:145–157.
Foss A, Evensen T, Imsland A, Oiestad V. 2001. Effects of reduced salinities on growth, food
conversion efficiency and osmoregulatory status in the spotted wolfish. J Fish Biol.
59:416–426.
Genz J, Taylor J, Grosell M. 2008. Effects of salinity on intestinal bicarbonate secretion and
compensatory regulation of acid–base balance in Opsanus beta. J Exp Biol.
211:2327–2335.
194 X. Serrano et al.
Downloaded by [University of Miami] at 13:40 13 December 2011
Harwell M, Long J, Bartuska A, Gentile J, Harwell C, Myers V, Ogden J. 1996. Ecosystem
management to achieve ecological sustainability, the case of South Florida. Environ
Manage. 20:497–521.
Jensen M, Madsen S, Kristiansen K. 1998. Osmoregulation and salinity effects on the
expression and activity of Naþ,Kþ-ATPase in the gills of European sea bass,
Dicentrarchus labrax. J Exp Zool. 282:290–300.
Leray C, Colin D, Florentz A. 1981. Time course of osmotic adaptation and gill energetics of
rainbow trout, Salmo gairdneri following abrupt changes in external salinity. J Comp
Physiol. 144:175–181.
Ley J, McIvor C, Montague C. 1999. Fishes in mangrove prop-root habitats of northeastern
Florida Bay, distinct assemblages across an estuarine gradient. Estuar Coast Shelf Sci.
48:701–723.
Lin C, Tsai R, Lee T. 2004. Expression and distribution of Na, K-ATPase in gill and kidney of
the spotted green pufferfish, Tetraodon nigroviridis, in response to salinity challenge.
Comp Biochem Physiol A. 138:287–295.
Mancera J, Pe
´rez-Fı
´gares J, Ferna
´ndez-Llebrez P. 1993. Osmoregulatory responses to abrupt
salinity changes in the euryhaline gilthead seabream (Sparus auratus). Comp Biochem
Physiol A. 106:245–250.
Marshall W, Grosell M. 2005. Physiology of fishes. 3rd ed. Boca Raton (FL): CRC Press.
McDonald M, Grosell M. 2006. Maintaining osmotic balance with an aglomerular kidney.
Comp Biochem Physiol A. 143:447–458.
Nonnotte G, Truchot D. 1990. Time course of extracellular acid–base adjustments under
hypo- or hyperosmotic conditions in the euryhaline fish Platichthys flesus. J Fish Biol.
36:181–190.
Redding J, Schreck C. 1983. Influence of ambient salinity on osmoregulation and cortisol
concentration in yearling coho salmon during stress. Trans Am Fish Soc. 112:800–807.
Rutherford E, Tilmant J, Thue E, Schmidt T. 1989. Fishery harvest and population dynamics
of gray snapper, Lutjanus griseus in Florida Bay and adjacent waters. Bull Mar Sci.
44(1):139–154.
Serafy J, Faunce C, Lorenz J. 2003. Mangrove shoreline fishes of Biscayne Bay, Florida. Bull
Mar Sci. 72:161–180.
Serafy J, Lindeman K, Hopkins T, Ault J. 1997. Effects of freshwater canal discharge on fish
assemblages in a subtropical bay, field and laboratory observations. Mar Ecol Prog Ser.
160:161–172.
Serafy J, Valle M, Faunce C, Luo J. 2007. Species-specific patterns of fish abundance and size
along a subtropical mangrove shoreline: an application of the delta approach. Bull Mar
Sci. 80:609–624.
Serrano X, Grosell M, Serafy J. 2010. Salinity selection and preference of the grey snapper
Lutjanus griseus: field and laboratory observations. J Fish Biol. 76:1592–1608.
Starck W. 1964. A contribution to the biology of the gray snapper, Lutjanus griseus
(Linnaeus), in the vicinity of lower Matecumbe Key, Florida [PhD Dissertation]. [Coral
Gables (FL)]: University of Miami.
Starck W, Schroeder R. 1970. Investigations on the gray snapper, Lutjanus griseus. Coral
Gables (FL): University of Miami Press.
Tabb D, Dubrow D, Manning R. 1962. The ecology of northern Florida Bay and adjacent
estuaries. FL Bd Conserv Tech Ser. 39:1–81.
Tabb D, Manning R. 1961. A checklist of the flora and fauna of northern Florida Bay and
adjacent brackish waters of the Florida mainland collected during the period July, 1957
through September, 1960. Bull Mar Sci Gulf Carib. 11(4):552–649.
Taylor T, Grosell M. 2006. Feeding and osmoregulation: dual function of the marine teleost
intestine. J Exp Biol. 209:2939–2951.
Tilmant J. 1989. A history and an overview of recent trends in the fisheries of Florida Bay.
Bull Mar Sci. 44:3–22.
Marine and Freshwater Behaviour and Physiology 195
Downloaded by [University of Miami] at 13:40 13 December 2011
Varsamos S, Diaz J, Charmantier G, Flik G, Blasco C, Connes R. 2002. Branchial chloride
cells in seabass (Dicentrarchus labrax) adapted to freshwater, seawater and doubly
concentrated seawater. J Exp Zool. 293:12–26.
Varsamos S, Nebel C, Charmantier G. 2005. Ontogeny of osmoregulation in postembryonic
fish, a review. Comp Biochem Physiol A. 141:401– 429.
Wakeman J, Wohlschlag D. 1983. Time course of osmotic adaptation with respect to blood
serum osmolality and oxygen uptake in the euryhaline teleost, Sciaenops ocellatus (red
drum). Contrib Mar Sci. 26:165–177.
Walters C, Gunderson L, Holling C. 1992. Experimental policies for water management in the
everglades. Ecol App. 2:189–202.
Wuenschel M, Martin G. 2006. Effect of temperature and salinity on otolith element
incorporation in juvenile gray snapper Lutjanus griseus. Mar Ecol Prog Ser. 324:229–239.
Yokel B. 1966. A contribution to the biology and distribution of the red drum, Sciaenops
ocellata. [MS Thesis]. [Coral Gables (FL)]: University of Miami.
196 X. Serrano et al.
Downloaded by [University of Miami] at 13:40 13 December 2011
