Journal of Fish Biology (2007) 70, 965–972
doi:10.1111/j.1095-8649.2007.01350.x, available online at http://www.blackwell-synergy.com
The influence of turbidity on three-spined
stickleback foraging
N. J. Q UESENBERRY , P. J. A LLEN
AND
J. J. C ECH J R *
Department of Wildlife, Fish and Conservation Biology, University of California,
Davis, 1 Shields Avenue, Davis, CA 95616, U.S.A.
(Received 3 March 2006, Accepted 30 October 2006)
Three-spined sticklebacks Gasterosteus aculeatus were used as a model to test for the effects
of turbidity on visual-predator foraging. While the number of feeding lunges and number
of prey consumed did not change with increasing turbidity, reactive distance to prey
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decreased.
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Key words: behaviour; foraging; harbour; reactive distance; stickleback; turbidity.
Turbidity is a pervasive problem in modified aquatic systems. Increasing urban
expansion leads to greater demands on aquatic systems, resulting in environmental alterations. Coastal environments, such as estuarine regions and harbours, are subjected to increased turbidity through boat traffic (Eriksson
et al., 2004), periodic dredging to maintain navigability (Hossain et al., 2004)
and increased eutrophication and intensified storm discharge due to development of associated upriver floodplains (Nixon, 1995). Such perturbations also
may occur in combination with wind-waves and natural tidal cycles (Ruhl
et al., 2001). The effects of increasing turbidity on visual-feeding marine fishes
remain unknown. A limited number of studies generally conducted with freshwater fishes have found that foraging attributes of reactive distance (Vinyard &
O’Brien, 1976), foraging behaviour (Vinyard & O’Brien, 1976; Sweka & Hartman,
2003) and capture success (Gregory & Northcote, 1993; Sweka & Hartman,
2001) may decrease with turbidity.
The three-spined stickleback Gasterosteus aculeatus L. is a species complex
of many, greatly varying, populations that are widely distributed in fresh
waters and along the coasts of northern Europe, the northern Pacific Rim
and North America (Bell & Foster, 1994). These fish are small, visual predators
*Author to whom correspondence should be addressed. Tel.: þ1 530 752 3103; fax: þ1 530 752 4154;
email: [email protected]
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(Hart & Gill, 1994) that feed on invertebrates such as crustaceans and insect
larvae, as well as fish eggs, fish larvae and plant matter (Wootton, 1976).
Three-spined sticklebacks forage continuously, but when near satiation, they
will either slow their foraging rate or engage in displacement behaviours (Hart
& Gill, 1994). Their foraging behaviour is also affected by their size, prey
density, season, palatability of prey and water temperature (Wootton, 1976;
Snyder, 1984; Hart & Gill, 1994). Three-spined sticklebacks rely primarily on
vision for prey capture (Hart & Gill, 1994), responding to movement and conspicuously coloured prey (Wootton, 1984). Prey capture comprises several distinct steps, which include: searching, detecting, approaching and final capture
(by lunging and ingestion) of prey (Wootton, 1984). This process may be
aborted at any point, and even after final capture, a fish may ingest the same
food item multiple times, before either eating or rejecting it.
Because three-spined sticklebacks are widespread geographically, and inhabit
marine environments which are affected by periodic turbidity, they are a good
model to study the effects of turbidity on fish foraging behaviour and success.
Individual three-spined sticklebacks were exposed to one of four turbidity levels
and their foraging behaviour and success were compared under each treatment.
It was hypothesized that three-spined stickleback reactive distance, number of
feeding lunges (foraging thrusts) and foraging success (prey consumption)
would decrease as turbidity increased.
Three-spined sticklebacks (complete morph) were captured in the summer of
2004 from Bodega Harbour (Sonoma County, CA, U.S.A.; 38°189 N; 123°039 W)
using a beach seine. This population of fish is known to reach large adult
sizes (70–90 mm total length, LT) and breed in salt water (Moyle, 2002).
Because the Bodega Harbour sediments are fine (i.e. including sands, silts
and clays; Koenig, 1963) they are apt to be stirred by storms, strong tides or
boat traffic in the adjacent channel. Water turbidity at the capture site ranged
from 22 nephelometric turbidity units (NTU; no disturbance) to 194 NTU
(during simultaneous rising tide and boat passage). Nearby turbidities have
reached considerably higher levels (>100 NTU following storm events; USGS,
2001). Water temperature was 153° C and salinity was 341. Approximately 60
three-spined sticklebacks were captured during the course of experiments. Few
fish displayed breeding colouration, therefore sex differentiation was not possible. Fish were transported 4 km in a large, insulated plastic container with
a portable air pump to the University of California’s Bodega Marine Laboratory (BML). At the BML, three-spined sticklebacks were maintained in three,
57 l pre-experimental aquaria with continuously flowing sea water (11–16° C,
following ambient ocean temperatures) and air stones. Suspended sediment
in the inflowing sea water settled rapidly and was removed with faecal material
by siphon daily.
Fish in pre-experimental aquaria were fed ad libitum adult brine shrimp
Artemia salina and finely chopped squid Loligo spp. twice on the first day
following capture, and food-deprived on the second day. On the third day, they
were used in experiments because pilot experiments showed that three-spined
sticklebacks fed readily after only 1 day of food deprivation. Each fish was
used only once, and all fish were returned to the capture location following
the completion of all experiments (held a maximum of 28 days).
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Experiments took place in a 38 l glass aquarium with one side sectioned off by
a clear acrylic sheet, to make a long, narrow chamber. This chamber was further
divided into a larger experimental chamber (9 36 31 cm deep) and a smaller
section (9 12 31 cm deep) with a submersible pump for water circulation.
The two sections were separated by a rigid plastic screen that allowed entry of
brine shrimp but prevented three-spined sticklebacks from approaching the
pump. The pump had a fine-screen filter that excluded brine shrimp, based on
a pilot experiment in which 10 brine shrimp were placed in the experimental
chamber overnight, and all 10 were recovered, intact, the following day. Water
was drawn by submersible pump from the experimental aquarium, and through
a stainless steel cooling coil (set in a water-bath) and back into the experimental
chamber. The water-bath had continuous flow-through sea water, ensuring that
temperatures remained within 1° C of those in the holding aquaria, and aiding
in bentonite suspension. The apparatus was conceptually similar to that used by
Sweka & Hartman (2001), although smaller and simpler.
Turbidities (5–10, 20–30, 40–60 or 60–80 NTU) were produced by adding
a fine bentonite clay suspension to the experimental chamber and stirring vigorously immediately before each experiment to ensure suspension. Water samples were removed at the same time and from the same depth for each
experiment and turbidity concentrations were verified by a calibrated turbidity
meter (Orion Aquafast II, Thermo Corp., Cambridge, MA, U.S.A.). The range
of turbidity treatments encompassed calm, non-turbid conditions (5–10 NTU;
no bentonite added) to simulated storm conditions (60–80 NTU), with turbidities >80 NTU rejected due to difficulties in visualizing fish movements and
foraging events.
Foraging behaviour (reactive distance, number of feeding lunges and number
of prey consumed) was measured using a grid (2 2 cm squares) that was
drawn on the side of the experimental chamber. A single, randomly selected
fish was transferred to the chamber (dip-net), and given 5 min to acclimate.
Single prey (A. salina, 0012 g mean live mass) were added to the chamber
(in 2 ml water), using a clear tube, 12 cm from the fish. At this distance prey
could always be added, regardless of the fish’s location. Between each feeding,
a similar volume, or blank, of sea water was added, to reduce the likelihood
of three-spined sticklebacks associating the tube with food. After all 10 prey
items had been delivered, blanks were added until the experiment had
ended. Reactive distance was defined as the distance at which a three-spined
stickleback responded to a prey item. A deliberate orientation towards a prey
item, accompanied by rapid sculling movements of pectoral and caudal fins was
regarded as a positive, prey-oriented response. For each fish, the maximum
reactive distance was estimated, using the grid, and recorded. During the
foraging period of each experiment, the number of feeding lunges was recorded
by means of a hand-held counter. The feeding lunge is a rapid forward movement to ingest prey, the ‘capture’ step in Wootton’s (1984) process of prey
acquisition. Sometimes feeding lunges did not appear to be directed towards
any visible prey item, but for consistency, these were recorded as feeding lunges
as well.
After the foraging period (10 min) had ended, a second turbidity sample was
taken, and the time and final temperature were recorded. The three-spined
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stickleback was immediately removed, its LT measured (nearest mm) on a
measuring board, and its wet mass determined using an electronic balance
( 001 g). The pump was turned off and removed, and its filter examined
for any brine shrimp. Next, the experimental chamber was carefully, and
repeatedly, swept with a net, and visually-inspected to remove any remaining
brine shrimp; those not recovered were recorded as consumed. The pump
was replaced, and an airstone was inserted into the chamber between experiments, to maintain high dissolved oxygen content.
Reactive distance and number of prey consumed were compared using
Kruskal–Wallis tests; LT, wet mass and number of feeding lunges were compared using a one-way ANOVA test (Sall et al., 2001). Number of feeding
lunges data were log10 transformed to meet the assumptions of normality and
homogeneity of variance. If the Kruskal–Wallis test was significant (P < 005),
a Bonferroni analogue (Neter et al., 1996) was used for multiple pair-wise
comparisons among turbidity groups. Number of feeding lunges data were also
regressed on time of day to check for any influence of conspecifics in prior
experiments. Unfortunately, data from several treatment groups (maximum
reactive distance and number of A. salina consumed data for the 20–30 and
40–60 NTU groups) on random experimental days were irretrievably lost due
to memory malfunctions.
With increasing turbidity three-spined sticklebacks decreased their reactive
distance (Kruskal–Wallis, d.f. ¼ 3, P < 0001) [Fig. 1 (a)], but there were
no significant differences in number of feeding lunges (ANOVA, d.f. ¼ 3, 36,
P > 005) [Fig. 1 (b)] or number of prey consumed (Kruskal–Wallis, d.f. ¼
3, P > 005) [Fig. 1 (c)]. Reactive distance was significantly greater at 5–10
and 20–30 NTUs than at either 40–60 or 60–80 NTUs, however, there were
no differences between 5–10 and 20–30 NTUs or between 40–60 and 60–80
NTUs (both based on Bonferroni analogue multiple pair-wise comparisons).
There were no differences between LT (mean S.E.: 77 1 mm, range
70–82 mm; ANOVA, d.f. ¼ 3, 36, P > 005) or wet mass (mean S.E.: 461
011 g, range 345–592 g; ANOVA, d.f. ¼ 3, 36, P > 005) among turbidity
treatment groups. Finally, there was not a significant relationship between
number of feeding lunges and time of day (ANOVA of linear regression,
d.f. ¼ 1, 38, P > 005).
This study demonstrated that increasing turbidity has significant impacts on
three-spined stickleback reactive distance, but not on number of feeding lunges
or foraging success (number of prey consumed) over the 5–80 NTU range. The
data indicate that turbidities >40 NTU significantly reduce three-spined stickleback reactive distance [Fig. 1(a)], supporting a decrease in reactive distance
with increased turbidity. Because reactive distance did not change between
the 40–60 and 60–80 NTU groups, a turbidity of 40 NTU probably represents
a visually related threshold in three-spined stickleback foraging behaviour. In
clear water, (<10 NTU) fish approached a prey item by swimming slowly
and stopping often (saltatory swimming; Hart, 1993), from distances up to
36 cm. This distance is similar to the 30 cm reactive distance of three-spined
sticklebacks foraging on benthic tubifex worms noted by Wootton (1976).
The fish often paused 8–10 cm away from a prey item before darting forwards
and engulfing it. In contrast, three-spined sticklebacks in the most turbid water
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INFLUENCE OF TURBIDITY ON FORAGING
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Maximum reactive distance (cm)
(a)
a
20
a
15
10
b
b
6
10
5
9
10
0
0
10
20
30
40
50
60
70
80
250
Number of feeding lunges
(b)
200
150
100
50
10
10
10
10
0
Number of Artemia salina consumed
0
10
20
30
40
50
30
40
50
60
70
80
10
(c)
8
6
4
2
10
9
9
10
0
0
10
20
60
70
80
Mean turbidity (NTU)
FIG. 1. (a) Maximum reactive distance, (b) number of feeding lunges and (c) number of Artemia salina
consumed by three-spined sticklebacks with increasing turbidity (in nephelometric turbidity units,
NTU). Values are means þ S.E., n are given on each bar and different lower case letters represent
significant differences among treatment groups (ANOVA or Kruskal–Wallis with Bonferroni
analogue, P < 005). Turbidity values are derived from the means of treatment turbidity ranges:
5–10 ¼ 75, 20–30 ¼ 25, 40–60 ¼ 50, 60–80 ¼ 70.
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N. J. QUESENBERRY ET AL.
conditions (>40 NTU) reacted almost instantly when a prey item came in close
proximity (4–8 cm), while ignoring other, presumably undetected, prey only
10–12 cm away. As turbidity increases, the volume of water in which a fish
may visually acquire prey shrinks, and consequently more prey avoid detection
(Vinyard & O’Brien, 1976).
Although it was predicted that the number of feeding lunges and foraging
success would decrease with increasing turbidity in three-spined sticklebacks,
this was not supported by the data. This may be due to the close confines of
the experimental design. Perhaps in the field, where prey may be more elusive,
three-spined sticklebacks are not able to forage as successfully under similar
turbidity conditions. Similarly, Moyle (2002) noted that it is unusual to find
three-spined sticklebacks in turbid water due to their visual-feeding nature,
although Marshall & Elliott (1998) found fish in turbidities >25 NTU. An
alternative explanation is that three-spined sticklebacks are able to compensate for decreased vision in moderate turbidities with other senses such as
olfaction. Interestingly, several studies of visual predatory fishes have found
that reactive distance and foraging efficiency do not decrease at moderate
turbidity levels (10–30 NTU; Granqvist & Mattila, 2004; Horpilla et al., 2004),
although they do decrease in turbidities >30 NTU (Horpilla et al., 2004), similar
to the reactive distance data from this study. Gregory & Northcote (1993)
suggested that moderate turbidity may enhance feeding by providing visual
contrast and enabling faster detection of prey. In the decreased visibility caused
by increasing turbidity, some species such as juvenile Atlantic cod Gadus
morhua L., perch Perca fluviatilis L. and juvenile Chinook salmon Oncorhynchus
tshawytscha (Walbaum) are able to compensate with olfactory senses (Meager
et al., 2005) or increased activity (Gregory & Northcote, 1993; Granqvist &
Mattila, 2004). In addition, the anti-predator behaviour of prey may also
decrease with turbidity (Granqvist & Mattila, 2004), although predator capture
effectiveness may be limited by prey mobility (Breitburg, 1988).
While moderate turbidities may provide some foraging benefits to threespined sticklebacks and provide fish with increased protection from predators
themselves, high turbidities can have deleterious effects, such as reducing the
photic zone, decreasing food abundance and interfering with fish feeding efficiency (Bruton, 1985). Field analyses on other species have shown that increasing turbidities can change fish community structure (Sandström & Karås,
2002), affect diet (Stuart-Smith et al., 2004) and reduce growth rates (Bruton,
1985). This study showed that a visually feeding marine species, the threespined stickleback, decreases reactive distance with turbidity, although foraging
success does not decline. A follow-up study to examine foraging success in
a larger experimental apparatus where food is not so readily available would
be useful to elucidate this relationship. Further, to better understand ecological
effects of turbidity in harbours and coastal systems, future field studies should
target three-spined stickleback distributions before and after chronic (tidal
fluxes) and acute (storm discharge and dredging) turbidity increases, especially
in relation to turbidities near 40 NTU. Similarly, the ecological understanding
of the effects of turbidity would be enhanced by laboratory studies examining
the combined influence of turbidity and predation risks on three-spined stickleback foraging behaviour.
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INFLUENCE OF TURBIDITY ON FORAGING
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We thank the Lloyd Swift family and the Department of Wildlife, Fish, and Conservation Biology at the University of California, Davis, for research support, K. Brown,
K. Menard and W. Newman (BML) for logistical assistance, B. Campos, E. Chen, S.
Feltman, M. Fish, J. Graham, G. Jones, D. Kratville, P. Lin, R. McGraw, J. Phillips
and R. Riley for technical or fish collection assistance, N. Willits, University of California,
Davis, for assistance with data analysis and P. B. Moyle, M. Karagosian, and two
anonymous reviewers for providing helpful comments on the manuscript. Research was
conducted under the auspices of UC Davis Animal Use and Care Protocol #04-11277.
Contribution Number 2363, Bodega Marine Laboratory, University of California, Davis.
References
Bell, M. A. & Foster, S. A. (1994). Introduction to the evolutionary biology of the
threespine stickleback. In The Evolutionary Biology of the Threespine Stickleback
(Bell, M. A. & Foster, S. A., eds), pp. 1–27. Oxford: Oxford University Press.
Breitburg, D. L. (1988). Effects of turbidity on prey consumption by striped bass larvae.
Transactions of the American Fisheries Society 117, 72–77.
Bruton, M. N. (1985). The effects of suspenoids on fish. Hydrobiologia 125, 221–241.
Eriksson, B. K., Sandström, A., Isæus, M., Schrebier, H. & Karås, P. (2004). Effects of
boating activities on aquatic vegetation in the Stockholm archipelago, Baltic Sea.
Estuarine, Coastal and Shelf Science 61, 339–349. doi: 10.1016/j.ecss.2004.05.009
Granqvist, M. & Mattila, J. (2004). The effects of turbidity and light intensity on the
consumption of mysids by juvenile perch (Perca fluviatilis L.). Hydrobiologia 514,
93–101.
Gregory, R. S. & Northcote, T. G. (1993). Surface, planktonic, and benthic foraging by
juvenile Chinook salmon (Oncorhynchus tshawytscha) in turbid laboratory conditions. Canadian Journal of Fisheries and Aquatic Sciences 50, 233–240.
Hart, P. J. B. (1993). Teleost foraging: facts and theories. In Behaviour of Teleost Fishes
(Pitcher, T. J., ed.), pp. 253–284. London: Chapman & Hall.
Hart, P. J. B. & Gill, A. B. (1994). Evolution of foraging behaviour in the threespine
stickleback. In The Evolutionary Biology of the Threespine Stickleback (Bell, M. A. &
Foster, S. A., eds), pp. 207–239. Oxford: Oxford University Press.
Horpilla, J., Liljendahl-Nurminen, A. & Malinen, T. (2004). Effects of clay turbidity and
light on the predator–prey interaction between smelts and chaoborids. Canadian
Journal of Fisheries & Aquatic Sciences 61, 1862–1870. doi: 10.1139/F04-123
Hossain, S., Eyre, B. D. & McKee, L. J. (2004). Impacts of dredging on dry season suspended
sediment concentration in the Brisbane River estuary, Queensland, Australia.
Estuarine, Coastal and Shelf Science 61, 539–545. doi: 10.1016/j.ecss.2004.06.017
Koenig, J. B. (1963). The geological setting of Bodega Head. California Mineral
Information Service, Division of Mines and Geology 16, 1–10.
Marshall, S. & Elliott, M. (1998). Environmental influences on the fish assemblage of the
Humber estuary, U.K. Estuarine, Coastal and Shelf Science 46, 175–184.
Meager, J. J., Solbakken, T., Utne-Palm, A. C. & Oen, T. (2005). Effects of turbidity on
the reactive distance, search time, and foraging success of juvenile Atlantic cod
(Gadus morhua). Canadian Journal of Fisheries & Aquatic Sciences 62, 1978–1984.
doi: 10.1139/F05-104
Moyle, P. B. (2002). Inland Fishes of California. Berkeley, CA: University of California
Press.
Neter, J., Kutner, M. H., Nachtsheim, C. J. & Wasserman, W. (1996). Applied Linear
Statistical Models. Boston, MA: WCB McGraw-Hill.
Nixon, S. W. (1995). Coastal marine eutrophication: a definition, social causes, and
future concerns. Ophelia 41, 199–219.
Ruhl, C. A., Schoellhamer, D. H., Stumpf, R. P. & Lindsay, C. L. (2001). Combined use
of remote sensing and continuous monitoring to analyse the variability of
suspended-sediment concentrations in San Francisco Bay, California. Estuarine,
Coastal and Shelf Science 53, 801–812. doi: 10.1006/ecss.2000.0730
# 2007 The Authors
Journal compilation # 2007 The Fisheries Society of the British Isles, Journal of Fish Biology 2007, 70, 965–972
972
N. J. QUESENBERRY ET AL.
Sall, J., Lehman, A. & Creighton, L. (2001). JMP Start Statistics: A Guide to Statistics and
Data Analysis Using JMP and JMPIN Software. Cary, NC: SAS Institute, Inc.
Sandström, A. & Karås, P. (2002). Effects of eutrophication on young-of-the-year
freshwater fish communities in coastal areas of the Baltic. Environmental Biology of
Fishes 63, 89–101.
Snyder, R. J. (1984). Seasonal variation in the diet of the threespine stickleback,
Gasterosteus aculeatus, in Contra Costa County, California. California Fish and
Game 70, 167–172.
Stuart-Smith, R. D., Richardson, A. M. M. & White, R. W. G. (2004). Increasing
turbidity significantly alters the diet of brown trout: a multi-year longitudinal
study. Journal of Fish Biology 65, 376–388. doi: 10.1111/j.0022-1112.2004.00456.x
Sweka, J. A. & Hartman, K. J. (2001). Influence of turbidity on brook trout reactive
distance and foraging success. Transactions of the American Fisheries Society 130,
138–146.
Sweka, J. A. & Hartman, K. J. (2003). Reduction of reactive distance and foraging
success in smallmouth bass, Micropterus dolomieu, exposed to elevated turbidity
levels. Environmental Biology of Fishes 67, 341–347.
Vinyard, G. L. & O’Brien, W. J. (1976). Effects of light and turbidity on the reactive
distance of bluegill (Lepomis macrochirus). Journal of the Fisheries Research Board of
Canada 33, 2845–2849.
Wootton, R. J. (1976). The Biology of the Sticklebacks. London: Academic Press.
Wootton, R. J. (1984). A Functional Biology of Sticklebacks. London: Croom Helm
Publishers.
Electronic Reference
USGS (2001). Summary of the Suspended-sediment Concentration Data, San Francisco Bay,
Water Year 1999, Open-file Report 01-100. Sacramento, CA: U.S. Geological
Survey. Available at: http://pubs.usgs.gov/of/2001/ofr01-100/
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