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International Journal of Comparative Psychology, 2010, 23, 70-81.
Copyright 2010 by the International Society for Comparative Psychology
This work was funded by a NSF GK-12 0139303 grant awarded to Saint Joseph’s Biology
Department and an internal grant from the Saint Joseph’s University chapter of Sigma Xi. We wish to
thank all of the people who have provided comments on this manuscript. Correspondence concerning
this article should be addressed to S.P. McRobert, Saint Joseph’s University, 5600 City Avenue,
Philadelphia, PA, 19131, U.S.A. (smcrober@sju.edu).
The Influence of Sex and Phenotype on
Shoaling Decisions in Zebrafish
Jennifer L. Snekser
Lehigh University, U.S.A.
Nathan Ruhl
Ohio University, U.S.A.
Kristoffer Bauer and Scott P. McRobert
Saint Joseph’s University, U.S.A.
Fish typically choose shoalmates with similar phenotypic characteristics to themselves, thus creating
shoals for which predators have difficulty identifying and attacking one specific individual. And
while shoaling should provide similar anti-predator benefits to both males and females, the two sexes
do not always make the same shoaling decisions. Here we explore the effect of phenotype on sex-
specific shoaling in three varieties of zebrafish (Danio rerio) and the closely related pearl danio
(Danio albolineatus). We hypothesized that males and females of each type of zebrafish (wildtype,
golden mutants and leopard mutants), as well as male and female pearl danios, would choose to shoal
rather than be alone and, when given a choice of shoalmates, would shoal with fish of their own
phenotype rather than dissimilar fish. As expected, our results show that most fish preferred to shoal
rather than be alone. However, while both sexes of wildtype zebrafish responded identically to
shoaling decisions, male and female mutant zebrafish and pearl danio fish differed in their response
to such choices. When given a choice of shoalmates, wildtype zebrafish of both sexes showed no
discrimination between different D. rerio strains, although they did choose to shoal with wildtype
conspecifics rather than pearl danios. The shoalmate preferences of the mutant zebrafish revealed that
males showed no discrimination between shoals of their own variety and wildtype shoals, while
mutant females preferred shoals of their own strain. Similarly, male pearl danios showed no
discrimination between shoals of their own species and shoals of wildtype zebrafish, while pearl
danio females preferred their own species. These results demonstrate the complex influence of sex
and phenotype on shoaling behavior.
Shoaling (forming loose social aggregations) is a behavior demonstrated
by many species of teleost fish, providing individuals with benefits such as
enhanced foraging opportunities, access to mates, and protection from predators
(Krause & Ruxton, 2002). With respect to the anti-predator benefits, it has been
suggested that it may be difficult for a predator to identify and attack any one
specific individual within a group of phenotypically similar fish (Pitcher, 1986).
This phenomenon, referred to as the confusion effect, causes predators to hesitate
momentarily before attacking aggregated prey, leading to a lower capture success
than when attacking solitary or dispersed prey (Milinski, 1979; Ohguchi, 1981). In
a related phenomenon, the oddity effect, a phenotypically distinct individual within
a shoal is more likely to be targeted by a predator (Landeau & Terborgh, 1986). It
is not surprising, therefore, that shoaling fish typically choose to associate with
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fish that bear a resemblance to themselves rather than fish that are phenotypically
different.
In studies on the confusion and oddity effects, a number of phenotypic
attributes have been shown to affect shoaling preferences for a variety of fish
species (reviewed in Krause, Butlin, Peuhkuri, & Pritchard, 2000). Such attributes
include body size (Hauser, Carvalho, & Pitcher, 1998; Krause & Godin, 1994;
McCann, Kohen, & Kline, 1971; Theodorakis, 1989), parasite load that causes
black spots on the body (Barber, Downey, & Braithwaite, 1998; Krause & Godin
1996), body shape (Hauser et al. , 1998), body coloration (McRobert & Bradner,
1998) and stripe pattern (Engeszer, Ryan, & Parichy, 2004; McCann, et al., 1971;
Rosenthal & Ryan, 2005). As predicted, fish are capable of discriminating between
potential shoalmates on the basis of each of these phenotypic features, typically
shoaling with fish that are similar in appearance. This assortative shoaling allows
fish to potentially incur the benefits of the confusion effect and avoid the costs of
the oddity effect.
One aspect of shoaling behavior that has been less well represented in the
literature is the effect of sex. Many studies disregard sex, either by examining only
one sex or by ignoring the sex of the fish altogether. Part of this omission may be a
perception that the two sexes would make similar shoaling choices, especially in
species in which males and females are phenotypically similar. In studies on a
sexually dimorphic species such as the guppy (Poecilia reticulate), it was found
that males are less likely than females to join shoals (Magurran, 1999), and female
guppies stayed in their shoals (Griffiths & Magurran, 1998) while males spent
more time moving between shoals (Magurran, 1998). In studies on another
sexually dimorphic species, the Siamese fighting fish (Betta splendens), both
males and females chose to shoal with larger groups of females, but females
avoided males, while males did not (Snekser, McRobert, & Clotfelter, 2006a).
Interestingly, sex-related shoaling differences have also been noted in species in
which males and females are phenotypically similar. Female rainbow fish
(Melanotaenia eachamensis) made shoaling choices based on relatedness of
individuals within the shoal, while males did not (Arnold, 2000). Similarly, female
zebrafish (Danio rerio) preferred to shoal with unfamiliar and unrelated males,
while males showed no such preference (Gerlach & Lysiak, 2006). Zebrafish
males and females also differed in their shoaling decisions when shoal sex and
shoal size were varied (Ruhl & McRobert, 2005; Ruhl, McRobert, & Currie,
2009). Additionally, male zebrafish have been shown to be more sensitive than
females to visual striping cues in shoaling assays (Engeszer, Wang, Ryan, &
Parichy, 2008).
Zebrafish are an ideal species to further explore the factors that influence
shoaling decisions. Zebrafish have long been used in genetic and developmental
studies and a recent surge in research has focused on their ecology and behavior
(reviewed by Spence, Gerlach, Lawrence, & Smith, 2008). The availability of a
large number of phenotypic variants (Detrich, Westerfield, & Zon, 1999; Nüsslein-
Volhard, 1994; Parichy, 2003) and closely related species (Fang, 2003; Mayden et
al., 2007) means that many naturally occurring variables exist for examining the
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relative importance of specific physical traits on shoalmate choice. Thus far,
studies on shoalmate choice of wildtype zebrafish have taken advantage of closely
related species (Engeszer et al., 2008; McCann & Carlson, 1982; Spence & Smith,
2007), pigment mutants and transgenics (Engeszer et al., 2004; Snekser,
McRobert, Murphy, & Clotfelter, 2006b; Spence & Smith, 2007; Engeszer et al.,
2008), and fin mutants (Kitevski & Pyron, 2003). Less attention has been focused
on the shoaling behavior of mutant zebrafish or closely related species, despite
evidence for strain differences in other behavioral contexts (Gumm, Snekser, &
Iovine, 2008; Itzkowitz & Iovine, 2007; Moretz, Martins, & Robison, 2006, 2007;
Robison & Rowland, 2005; Wright, Butlin, & Carlborg, 2006; Wright, Rimmer,
Pritchard, Krause, & Butlin, 2003).
The objective of this study was to explore possible sex differences in the
shoaling behavior of wildtype zebrafish, two mutant zebrafish strains (leopard and
golden) and the closely related pearl danio (D. albolineatus). In each case, we
predicted that males and females of each strain would prefer to associate with other
fish, regardless of phenotype, over an empty chamber and would prefer to
associate with fish of similar phenotypic characteristics in dichotomous choice
assays.
Method
Adult fish were obtained from commercial suppliers (World Wide Aquarium and Seven
Star Tropical Inc., Philadelphia, PA). Focal fish (whose behavior was observed) were housed in
separate tanks from stimulus fish (used in groups of three to elicit responses from focal fish). Fish
were further separated by variety and sex; sex was determined by general body shape (with females
being more rotund than males) and the presence of a genital papilla rostral of the anal fin in females.
All tanks were covered on three sides with opaque white paper to visually isolate the fish from other
varieties and the opposite sex. Tanks were maintained under fluorescent lighting on a 12L:12D cycle
at 23° C. All fish were fed commercial flake food once per day.
Three varieties of zebrafish (D. rerio) as well as the closely related pearl danio (D.
albolineatus) were used as both focal and stimulus fish. Wildtype zebrafish have five to seven dark
stripes of melanophores and iridophores alternating with light stripes of xanthophores and iridophores
(Parichy, 2006a,b; Quigley & Parichy, 2002). The mutant, golden, lacks melanophore pigmentation
resulting in a yellow coloration with faint yellow stripes (Lamason et al., 2005). The mutant, leopard,
has interrupted melanophore stripes, giving the fish a spotted appearance (Johnson, Africa, Walker, &
Weston, 1995). Pearl danios (D. albolineatus), a close relative of zebrafish, have the same general
body shape and size as D. rerio, but lack dark stripes altogether (Fang, 2003).
Test tanks were constructed by dividing aquaria (74 x 31 x 31 cm) into three compartments
(Fig. 1) with clear glass partitions sealed with silicone caulk 18 cm from each end. The central
compartment was further divided into left and right sides by opaque Plexiglas partitions (25 x 18 cm).
These partitions allowed focal fish to swim to either side of the central compartment but prevented
fish on one side from seeing the stimulus fish on the opposite side.
Each test session consisted of a 600 s observation period during which the time the focal
fish spent on each side of the central compartment was recorded. Twenty fish of each sex (chosen at
random from a holding tank) were tested in each assay and the same fish was not used more than
once in any assay. Prior to each test, a single focal fish was placed into the central compartment and
allowed one hour to acclimate. During this acclimation period, the stimulus shoals were held in their
end compartments. Stimulus fish were, in all assays, the same sex as the focal fish. An equal number
of tests were run with stimulus shoals in the left and right end compartments to reduce the risk of
‘tank effects’.
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Figure 1. Diagram of aerial view of dichotomous choice testing tank.
For wildtype zebrafish, we ran two types of behavioral assay. In the first set, wildtype
zebrafish (males or females) were given the choice of an empty chamber and a shoal of three fish of
one variety: wildtype, golden, leopard, or pearl danios. In the second set of assays (simultaneous
choice tests), wildtype zebrafish were given the choice between a shoal of three wildtype zebrafish
and another shoal of three fish: wildtype, golden, leopard, or pearl danios.
Similar behavioral tests were performed with the mutant zebrafish (golden and leopard)
and the pearl danios. In the first set of assays, male and female mutant zebrafish or pearl danios were
given the choice of an empty chamber and a shoal of three fish of the same variety or a shoal of three
wildtype zebrafish. In the second set of assays, male and female mutant zebrafish or pearl danios
were given the choice of a shoal of three wildtype zebrafish and a shoal of three fish of the same
variety as the focal fish.
The mean time spent on either side of the central compartment was calculated for each
assay. We assumed that if there was no preference for either shoal, the focal fish should spend 300 s
(or 50% of their time) on each side of the test tank. For this reason, we compared the association
times to the null expectation of 300s using one-sample t tests for each assay (see Bradner &
McRobert, 2001; Ruhl & McRobert, 2005; Ruhl et al., 2009; Snekser et al., 2006a,b).
Results
When given the choice between an empty compartment and a
compartment containing three fish of the same sex, male and female wildtype
zebrafish always shoaled regardless of the variety of stimulus fish. In simultaneous
choice tests, neither male nor female wildtype zebrafish showed a significant
preference when given the choice between shoals of conspecifics but did spend
significantly more time near wildtype zebrafish than near the heterospecific pearl
danios (Table 1 and Fig. 2).
When golden zebrafish were given a choice between a shoal of three fish
of the same variety and an empty compartment, both males and females spent
significantly more time near the shoal of golden zebrafish. However, when given a
choice between three wildtype zebrafish and an empty compartment, golden males
shoaled while golden females did not demonstrate a preference. In simultaneous
choice tests, golden females spent significantly more time near a shoal of golden
females than near a shoal of wildtype females, while golden males did not exhibit a
preference between golden males and wildtype males (Table 2 and Fig. 2).
- 74 -
Table 1
Mean association time ± SE exhibited by male and female wildtype zebrafish for each behavioral
choice test.
Note: n = 20 for each behavioral choice test. t-statistics (One-sample t test (H
0
= 0.5)) and
corresponding p-values are given for each test. Statistically significant preferences are indicated in
bold.
Table 2
Mean association time ± SE exhibited by mutant zebrafish (golden and leopard) for each behavioral
choice test.
Note: n = 20 for each behavioral choice test. t-statistics (One-sample t test (H
0
= 0.5)) and
corresponding p values are given for each test. Statistically significant preferences are indicated in
bold.
Sex of
Focal Fish Shoal 1 Mean time (s) Shoal 2 Mean time (s) SE t p
M 3 Wildtype 430 Empty 170 39.90 3.26 0.004
M 3 golden 402 Empty 198 29.75 3.43 0.003
M 3 leopard 415 Empty 185 16.72 6.87 <0.001
M 3 pearl 401 Empty 199 34.53 2.92 0.009
M 3 Wildtype 346 3 Wildtype 254 31.36 1.48 0.16
M 3 Wildtype 313 3 golden 287 27.08 0.48 0.64
M 3 Wildtype 312 3 leopard 288 29.79 0.39 0.70
M 3 Wildtype 362 3 pearl 238 28.74 2.14 0.04
F 3 Wildtype 476 Empty 124 20.97 8.39 <0.001
F 3 golden 390 Empty 210 27.94 3.22 0.005
F 3 leopard 447 Empty 153 22.33 6.59 <0.001
F 3 pearl 435 Empty 165 29.94 4.54 <0.001
F 3 Wildtype 288 3 Wildtype 312 23.88 0.49 0.63
F 3 Wildtype 355 3 golden 245 30.21 1.83 0.08
F 3 Wildtype 334 3 leopard 266 25.91 1.31 0.21
F 3 Wildtype 401 3 pearl 199 37.49 2.68 0.01
Sex of
Focal Fish Shoal 1 Mean time (s) Shoal 2 Mean time (s) SE t p
golden zebrafish
M 3 Wildtype 391 Empty 209 32.07 2.83 0.011
M 3 golden 422 Empty 178 37.57 3.24 0.004
M 3 Wildtype 265 3 golden 335 41.34 0.85 0.41
F 3 Wildtype 344 Empty 256 21.56 2.04 0.06
F 3 golden 431 Empty 169 31.11 4.21 <0.001
F 3 Wildtype 240 3 golden 360 21.85 2.72 0.013
leopard zebrafish
M 3 Wildtype 417 Empty 183 22.33 5.23 <0.001
M 3 leopard 445 Empty 155 34.20 4.25 <0.001
M 3 Wildtype 313 3 leopard 287 44.63 0.30 0.77
F 3 Wildtype 430 Empty 170 28.51 4.55 <0.001
F 3 leopard 437 Empty 163 30.67 4.46 <0.001
F 3 Wildtype 239 3 leopard 361 25.35 2.40 <0.001
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Figure 2. Mean + SE time spent with wildtype zebrafish in each of the dichotomous choice tests for
males (A) and females (B). The strain of fish listed first is that of the focal fish; WT = wildtype. * p <
0.05
When leopard zebrafish were given a choice between a shoal of three
leopard zebrafish and an empty end compartment, or between a shoal of three
wildtype zebrafish and an empty compartment, both males and females spent
significantly more time near the shoal of fish. In simultaneous choice tests, leopard
females spent significantly more time near a shoal of leopard females than near a
shoal of wildtype females while leopard males did not exhibit a preference
between leopard males and wildtype males (Table 2 and Fig. 2).
When pearl danios were presented with a choice between an empty
chamber and either a shoal of three pearl danios or a shoal of wildtype zebrafish,
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both males and females spent significantly more time near the shoal of fish. When
presented with a shoal of three pearl danios and a shoal of three wildtype zebrafish,
however, pearl danio females spent significantly more time near the pearl danio
shoal while males showed no significant preference (Table 3 and Fig. 2).
Table 3
Mean association time ± SE exhibited by pearl danios for each behavioral choice test.
Note: n = 20 for each behavioral choice test. t-statistics (One-sample t test (H
0
= 0.5)) and
corresponding p values are given for each test. Statistically significant preferences are indicated in
bold.
Discussion
Both sexes of wildtype zebrafish made similar shoaling decisions. Males
and females each chose to shoal rather than be alone, regardless of the strain of
shoal presented. Additionally, in simultaneous choice assays, neither sex showed a
preference when given a choice between a shoal of wildtype zebrafish and a shoal
of mutant zebrafish with atypical body coloration or stripe pattern. This lack of
shoaling preference is in concordance with a number of studies in which wildtype
zebrafish failed to discriminate between their own variety and other phenotypic
mutants, including leopard (Spence & Smith, 2007), and golden (Saverino &
Gerlai, 2008). However, these studies did not specifically examine the behavior of
both male and female zebrafish. In one study in which sex was considered, neither
male nor female wildtype zebrafish distinguished between wildtype shoals and
shoals of transgenic RFP Glofish (Snekser et al., 2006b).
However, the literature also contains studies in which wildtype zebrafish
demonstrate an ability to discriminate between phenotypically similar and
phenotypically distinct shoalmates. In studies utilizing altered photographs
(McCann et al., 1971), video playback models (Rosenthal & Ryan, 2005), or
stripe-less nacre zebrafish mutants (Engeszer et al., 2004), wildtype zebrafish
demonstrated a preference for shoals of fish with body color and stripe pattern
similar to their own. These studies, however, did not separate the sexes and
specifically compare the behavior of males to females.
In contrast to their lack of discrimination between different zebrafish
strains, both male and female wildtype zebrafish showed a significant preference
for conspecific shoals over shoals of the heterospecific pearl danio. It is difficult,
however, to determine whether the avoidance of the pearl danios was due to
differences in phenotype (i.e., lack of stripes), or some other difference between
the species, such as swimming behavior. Nonetheless, when taking all of the
Sex of Focal
Fish Shoal 1 Mean time (s) Shoal 2 Mean time (s) SE t p
M 3 Wildtype 482 Empty 118 36.42 4.99 <0.001
M 3 pearl 422 Empty 178 27.32 4.48 <0.001
M 3 Wildtype 275 3 pearl 325 53.27 0.47 0.641
F 3 Wildtype 407 Empty 193 37.99 2.82 0.011
F 3 pearl 464 Empty 136 34.30 4.78 <0.001
F 3 Wildtype 136 3 pearl 464 37.45 4.37 <0.001
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assays into account, body coloration and stripe pattern did not have a significant
impact on shoalmate choice for wildtype zebrafish, contrary to our initial
predictions. Perhaps the phenotypic differences need to be as dramatic as “stripes”
versus “no stripes” (i.e., Engeszer et al., 2004) to make a difference in terms of
shoaling benefits such as the confusion effect. In keeping with our initial
predictions, however, wildtype males and females made similar shoaling choices.
In contrast, the tests with zebrafish mutants (leopard and golden) and the
closely related pearl danio, body coloration and stripe pattern did appear to affect
shoalmate choice, but only for females. Males of these three varieties behaved
similarly to wildtype zebrafish, while females showed greater discrimination in
shoalmate choice. When presented with two shoals (wildtype fish vs. the same
variety as the test fish), males showed no significant preference for either shoal.
Males also chose to associate with shoals rather than be alone. Like males,
females, for the most part, preferred to shoal rather than be alone regardless of the
phenotype of the shoal. But unlike males, female pearl danios, leopard zebrafish,
and golden zebrafish preferred to shoal with phenotypically similar fish over
dissimilar fish.
Previous studies that focused on the shoaling tendencies of zebrafish
mutants found that leopard zebrafish did not discriminate between shoals of
leopard or wildtype zebrafish (Spence & Smith, 2007) or shoals of striped and
stripe-less video models (Rosenthal & Ryan, 2005). Similarly, the golden mutant
zebrafish showed no significant preference for striped or stripe-less models
(Rosenthal & Ryan, 2005) and did not sort themselves from shoals of wildtype
zebrafish (Saverino & Gerlai, 2008). Again, these previous studies ignored the sex
of the fish in analysis and it is thus difficult to draw complete comparisons
between these studies and the work presented here.
Overall, the results presented here show that sex can be a critical factor in
the shoaling behavior of zebrafish (D. rerio) and the pearl danio (D. albolineatus).
It also appears that stripe pattern and body coloration are phenotypic features that
impinge on shoalmate choice in these species. However, the results are complex
and, in some ways, create more questions than they answer. For example, why was
the behavior of wildtype zebrafish so different from that of the mutant zebrafish?
And why, within the mutant zebrafish strains and the pearl danio strain, did
females make different shoaling choices than males? Perhaps the sex differences
reflect a difference in the benefits provided by shoaling. Shoaling in males, in
more natural situations, may be influenced by potential mate associations, with any
shoal of zebrafish, regardless of body color or stripe pattern, providing an
opportunity for increased reproductive success. Conversely, females may be
making shoaling decisions based primarily on maximizing predator defense, and
thus choose to associate with phenotypically similar fish. Previous studies on
guppies indicate similar trends, with male strategies seemingly directed toward
reproduction and females strategies toward increased foraging efficiency and
survival (reviewed in Magurran & Garcia, 2000). Additional zebrafish shoaling
experiments are necessary to better understand the evolutionary impetus of each
sex to shoal.
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It is important to note that the results presented here may be limited due to
the use of captive-bred animals obtained from commercial suppliers. The fish we
studied may have been in captivity for many generations and therefore have not
been subject to the same selective pressures as wild fish. Despite this limitation,
fish from commercial suppliers will obviously continue to be a staple in research
and have already contributed substantially to our knowledge of zebrafish behavior
(e.g., Bass & Gerlai, 2008; Colwill, Raymond, Ferriere, & Escudero, 2005;
Gerlach & Lysiak, 2006; Kitevski & Pyron, 2003; Larson, O’Malley, & Melloni,
2006; McCann et al., 1971; McCann & Carlson, 1982; Miller & Gerlai, 2007;
Pyron, 2003; Rosenthal & Ryan, 2005; Ruhl & McRobert, 2005; Saverino &
Gerlai, 2008; Snekser et al., 2006b; Spence, Ashton, & Smith, 2007; Spence &
Smith, 2005, 2006, 2007, 2008). Furthermore, access to mutations and transgenic
fish available only in captive strains provide an incredibly valuable scientific
resource.
Finally, while we can design experiments aimed at identifying the specific
factors that mediate behavior, our interpretation of these studies is only
speculation. We will never be able to see through the eyes of a fish and therefore
we can only make suggestions about which factors influence behaviors such as
shoalmate choice and the potential differences in decision-making between male
and female fish. It is always possible that factors unseen by humans are responsible
for the behaviors we study and we must remember that the perceptual worlds of
our study organisms may be very different from our own (see Engeszer et al.,
2008; von Uexkull, 1909).
References
Arnold, K. E. (2000). Kin recognition in rainbowfish (Melanotaenia eachamensis): Sex,
sibs, and shoaling. Behavioral Ecology and Sociobiology, 48, 385-391.
Barber, I., Downey, L. C., & Braithwaite, V. A. (1998). Parasitism, oddity and the
mechanism of shoal choice. Journal of Fish Biology, 53, 1365-1368.
Bass, S. L. S., & Gerlai, R. (2008). Zebrafish (Danio rerio) responds differentially to
stimulus fish: The effects of sympatric and allopatric predators and harmless fish.
Behavioural Brain Research, 186, 107-117.
Bradner, J., & McRobert, S. P. (2001). Background coloration affects body colour
segregation in fish. Journal of Fish Biology, 59, 673-681.
Colwill, R. M., Raymond, M. P., Ferreire, L., & Escudero, H. (2005). Visual discrimination
learning in zebrafish (Danio rerio). Behavioural Processes, 70, 19-31.
Detrich III, H. W., Westerfield, M., & Zon, L. I. (1999). Overview of the zebrafish system.
Methods in Cell Biology, 59, 3-10.
Engeszer, R. E., Ryan, M. J., & Parichy, D. M. (2004). Learned social preference in
zebrafish. Current Biology, 14, 881-884.
Engeszer, R. E., Wang, G., Ryan, M. J., & Parichy, D. M. (2008). Sex-specific perceptual
spaces for a vertebrate basal social aggregative behavior. Proceedings of the
National Academy of Science, 105, 929-933.
Fang, F. (2003). Phylogentic analysis of the Asian cyprinid genus Danio (Teleostei,
Cyprinidae). Copeia, 4, 714-728.
- 79 -
Gerlach, G., & Lysiak, N. (2006). Kin recognition and inbreeding avoidance in zebrafish,
Danio rerio, is based on phenotype matching. Animal Behaviour, 71, 1371-1377.
Griffiths, S. W., & Magurran, A. E. (1998). Sex and schooling behaviour in Trinidadian
guppies. Animal Behaviour, 56, 689-693.
Gumm, J. M., Snekser, J. L., & Iovine, M. K. (2008). Fin-mutant female zebrafish (Danio
rerio) exhibit differences in association preferences for male fin length.
Behavioural Processes, 80, 35-39.
Hauser, L., Carvalho, G. R., & Pitcher, T. J. (1998). Genetic population structure in the
Lake Tanganyika sardines Limnothrissa miodon. Journal of Fish Biology
Supplement A, 53, 413-429.
Itzkowitz, M., & Iovine, M.K. (2007). Single gene mutations causing exaggerated fins also
cause non-genetic changes in the display behavior of male zebrafish. Behaviour,
144, 787-795.
Johnson, S. L., Africa, D., Walker, C., & Weston, J. A. (1995). Genetic control of adult
pigment stripe development in zebrafish. Developmental Biology, 167, 27-33.
Kitevski, B., & Pyron, M. (2003). Female zebrafish (Danio rerio) do not prefer mutant
longfin males. Journal of Freshwater Ecology, 18, 501-502.
Krause, J., Butlin, R. K., Peuhkuri, N., & Pritchard, V. L. (2000). The social organization
of fish shoals: A test of the predictive power of laboratory experiments for the
field. Biology Reviews, 75, 477-501.
Krause, J., & Godin, J. G. J. (1996). Influence of parasitism on shoal choice in banded
killifish (Fundulus diaphanus, Teleostei, Cyprinodontidae). Ethology, 102, 40-49.
Krause, J., & Godin, J. G. J. (1994). Shoal choice in the banded killifish (Fundulus
diaphanous, Teleostei, Cyprinodontidae): Effects of predation risk, fish size,
species composition and size of shoals. Ethology, 98, 128-136.
Krause, J., & Ruxton, G. D. (2002). Living in groups. New York: Oxford University Press.
Lamason, R. L., Mohideen, M.A., Mest, J.R., Wong, A.C., Norton, H. L., Aros, M.C., et al.
(2005). SLC24A5, a putative cation exchanger, affects pigmentation in zebrafish
and humans. Science, 310, 1782-1786.
Landeau, L., & Terborgh, J. (1986). Oddity and the ‘confusion effect’ in predation. Animal
Behaviour, 34, 1372-1380.
Larson, E. T., O’Malley, D. M., & Melloni Jr., R. H. (2006). Aggression and vasotocin are
associated with dominate-subordinate relationships in zebrafish. Behavioural
Brain Research, 167, 94-102.
Magurran, A. E. (1999). The causes and consequences of geographic variation in
antipredator behavior, perspectives from fish populations. In S. A. Foster & J. A.
Endler (Eds.), Geographic Variation in Behavior: Perspectives on Evolutionary
Mechanisms (pp. 139-163). New York: Oxford University Press. 336pp.
Magurran, A. E. (1998). Population differentiation without speciation. Philosophical
Transactions of the Royal Society B, 353, 275-286.
Magurran, A. E., & Garcia, C. M. (2000). Sex differences in behaviour as an indirect
consequence of mating systems. Journal of Fish Biology, 57, 839-857.
Mayden, R. L., Tang, K. L., Conway, K. W., Freyhof, J. R, Chamberlain, S., Haskins, M.,
et al. (2007). Phylogenetic relationships of Danio within the order Cypriniformes:
A framework for comparative and evolutionary studies of a model species.
Journal of Experimental Zoology (Mol Dev Evol), 308B, 642-654.
McCann, L. I., & Carlson, C. C. (1982). Effects of cross-rearing on species identification in
zebrafish and pearl danios. Developmental Psychology, 15, 71-74.
- 80 -
McCann, L. I., Kohen, D. J., & Kline, N. J. (1971). The effects of body size and body
markings on nonpolarized schooling behavior of zebrafish (Brachydanio rerio).
Journal of Psychology, 79, 71-7-5.
McRobert, S. P., & Bradner, J. (1998). The influence of body coloration on shoaling
preferences in fish. Animal Behaviour, 56, 611-615.
Milinski, M. (1979). Can an experienced predator overcome the confusion of swarming
prey more easily? Animal Behaviour, 27, 1122-1126.
Miller, N., & Gerlai, R. (2007). Quantification of shoaling behavior in zebrafish (Danio
rerio). Behavioural Brain Research, 184, 157-166.
Moretz, J. A., Martins
,
E. P., & Robison
,
B. D. (2007). Behavioral syndromes and the
evolution of correlated behavior in zebrafish. Behavioral Ecology, 18, 556-562.
Moretz, J. A., Martins, E. P., & Robison, B. D. (2006). The effects of early and adult social
environment on zebrafish (Danio rerio) behavior. Environmental Biology of
Fishes, 80, 91-101.
Nüsslein-Volhard, C. (1994). Of flies and fishes. Science, 266, 572-574.
Ohguchi, O. (1981). Prey density and selection against oddity by three-spined sticklebacks.
Zeitschrift fur Tierpsychology, 23, 1-79.
Parichy, D. M. (2006a). Homology and the evolution of novelty during danio pigment
pattern development. Journal of Experimental Zoology, 306B, 1-13.
Parichy, D. M. (2006b). Evolution of danio pigment pattern development. Heredity, 97,
200-210.
Parichy, D. M. (2003). Pigment patterns: Fish in stripes and spots. Current Biology, 13,
R947-R950.
Pitcher, T. J. (1986). Functions of shoaling behavior in teleosts. In T. J. Pitcher (Ed.), The
Behavior of Teleost Fish ( pp. 294-337). London: Chapman & Hall..554pp.
Pyron, M. (2003). Female preferences and male-male interactions in zebrafish (Danio
rerio). Canadian Journal of Zoology, 81, 122-125.
Quigley, I. K., & Parichy, D. M. (2002). Pigment pattern formation in zebrafish: A model
for developmental genetics and the evolution of form. Microscopy Research and
Techniques, 58, 442-455.
Robison, B. D., & Rowland, W. (2005). Zebrafish (Danio rerio) as a model organism in
conservation biology: Behavioral variation among wild and domesticated strains.
Canadian Journal of Fisheries and Aquatic Science, 62, 2046-2054.
Rosenthal, G. G., & Ryan, M. J. (2005). Assortative preferences for stripes in danios.
Animal Behaviour, 70, 1063-1066.
Ruhl, N., McRobert, S. P., & Currie, W. J. S. (2009). The effect of sex ratio on shoaling,
spawning and aggression in small laboratory populations of zebrafish (Danio
rerio). Lab Animal, 38, 264-269.
Ruhl, N., & McRobert, S. P. (2005). The effect of sex and shoal size on shoaling behavior
in Danio rerio. Journal of Fish Biology, 67, 1318-1326.
Saverino, C., & Gerlai, R. (2008). The social zebrafish: Behavioral responses to
conspecific, heterospecific and computer animated fish. Behavioural Brain
Research, 191, 77-87.
Snekser, J. L., McRobert, S. P., & Clotfelter, E. D. (2006a). Social partner preferences of
male and female fighting fish (Betta splendens). Behavioural Processes, 72, 38-
41.
Snekser, J. L., McRobert, S. P., Murphy, C. E., & Clotfelter, E. D. (2006b). Aggregation
behavior in wildtype and transgenic zebrafish. Ethology, 111, 1-10.
- 81 -
Spence, R., Ashton, R., & Smith, C. (2007). Oviposition decisions are mediated by
spawning site quality in wild and domesticated zebrafish, Danio rerio. Behaviour,
114, 953-966.
Spence, R., Gerlach, G., Lawrence, C., & Smith, C. (2008). The behaviour and ecology of
the zebrafish, Danio rerio. Biological Reviews, 83, 13-34.
Spence, R., & Smith, C. (2008). Innate and learned colour preference in the zebrafish,
Danio rerio. Ethology, 114, 582-588.
Spence, R., & Smith, C. (2007). The role of early learning in determining shoaling
preferences based on visual cues in the zebrafish, Danio rerio. Ethology, 113, 62-
67.
Spence, R., & Smith, C. (2006). Mating preferences of female zebrafish, Danio rerio, in
relation to male dominance. Behavioral Ecology, 17, 779-783.
Spence, R., & Smith, C. (2005). Male territoriality mediates density and sex ratio effects on
oviposition in the zebrafish, Danio rerio. Animal Behaviour, 69, 1317-1323.
Theodorakis, C. W. (1989). Size segregation and the effects of oddity on predation risk in
minnow schools. Animal Behaviour, 38, 496-502.
von Uexkull, J. (1909/1985). Environment (Umwelt) and the inner world of animals (C.J.
Mellor and D. Gove. Trans.). In G. M. Burghardt (Ed.), Foundations of
Comparative Ethology (pp. 222-245). New York: Van Nostrand Reinhold.
(Reprinted from J. von Uexkull (1909). Umwelt and Innenwelt der Tiere. Berlin:
J. Springer). 441pp.
Wright, D., Butlin, R. K., & Carlborg, O. (2006). Epistatic regulation of behavioural and
morphological traits in the zebrafish (Danio rerio). Behavioral Genetics, 36, 914-
922.
Wright, D., Rimmer, L. B., Pritchard, V. L., Krause, J., & Butlin, R. K. (2003). Inter and
intra-population variation in shoaling and boldness in the zebrafish (Danio rerio).
Naturwissenschaften, 90, 374-377.
