Girardinichthys Multiradiatus)

Behavioural Processes 100 (2013) 163–168

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Behavioural Processes

jou rnal homepage: www.elsevier.com/locate/behavproc

Female vibration discourages male courtship behaviour in the

Amarillo ﬁsh (Girardinichthys multiradiatus)

a b a

Lourdes Martínez Medina , Constantino Macías Garcia , Amira Flores Urbina ,

c a,∗

Javier Manjarrez , Alejandro Moyaho

Instituto de Fisiología, B. Universidad Autónoma de Puebla, Avenida 14 Sur 6301, Colonia San Manuel, Puebla, Pue 72570, Mexico

Instituto de Ecología, Universidad Nacional Autónoma de México, Apdo. Postal 70-275, México, D.F. 04510, Mexico

Facultad de Ciencias, Universidad Autónoma del Estado de México, Instituto Literario 100, Toluca, Estado de México 50000, Mexico

a r t i c l e i n f o a b s t r a c t

Article history: Amarillo ﬁsh females (Girardinichthys multiradiatus) vibrate when conspeciﬁc males approach them; the

Received 19 June 2013

reason behind this behaviour is unclear. Hypotheses are that females vibrate either to avoid aggression

Accepted 26 September 2013

from males or to court them. We prevented females from vibrating by temporarily blocking their lateral

line organs and eyes, on the assumption that they rely on these senses to detect approaching males.

Keywords:

Females with the lateral line organs obstructed vibrated less frequently than females with the lateral

Cobalt

line intact, indicating that the mechanosensory lateral line system is necessary for perceiving approa-

Freshwater ﬁsh

ching males. Males displayed more courtship behaviour to sighted females with the lateral line organs

Goodeinae

obstructed than to sighted females with the lateral line intact. A general tendency indicated that the less

Lateral line organs

the females vibrated the more the males courted them. These ﬁndings indicate that female vibration

Viviparous ﬁsh

discourages male courtship behaviour.

1. Introduction to central México (Doadrio and Domínguez, 2004; Webb, 2004;

Miller, 2005). As with other goodein species, the Amarillo ﬁsh

The importance of the lateral line system in the behaviour of ﬁsh shows conspicuous sexual dimorphism (Macías Garcia and Valero,

has frequently been demonstrated (Bleckmann, 1993). But, except 2010). Males have larger and more colourful dorsal and anal ﬁns

for the relatively complex inter-sexual vibrational communication than females, which they display during courtship (Macías Garcia,

of the himé salmon (Satou et al., 1994), most studies have dealt 1994) and male–male encounters (Macías Garcia, 1990). Females

with relatively simple topographic interactions with the environ- are dull except for a pigmented black spot around the vent, possibly

ment, including prey, or conspeciﬁcs. Examples include orientation derived from a pregnancy signal, which is also used by submissive

to water currents in several ﬁsh species (Montgomery et al., 1997), males to mimic females (Macías Garcia and Valero, 2001).

schooling (e.g. in saithe Pollachius virens; Pitcher et al., 1976) and Amarillo females of most goodein species show vibration, that is,

the predatory behaviour of the bluegill (Lepomis macrochirus; Enger they wag the head while leaning forwards when conspeciﬁc males

et al., 1989). Interactions involving more than just adjustments of approach them (Moyaho, 2002). Previous observations in the Ama-

position or orientation, and controlled by more than one sensory rillo ﬁsh suggested that females vibrate to avoid sexual harassment

modality (e.g. mechanoreception and vision) have seldom been by males (Macías Garcia et al., 1994). Thus, vibration could serve as

examined (Rüschenbaum and Schlupp, 2013). This is in part due an appeasement signal, albeit an expensive one (Valero et al., 2005).

to the difﬁculty in separating the effects of mechanical sensory This putative appeasement signal does not work in female–female

cues from those produced by other sensory modalities. Here we interactions, indicating that it is a signal directed particularly to

used temporary blockade of the lateral-line organs and eyes to males. If so, this suggests the alternative, non-exclusive hypothesis

discriminate between two competing hypotheses about the signif- that female vibration is a courtship display, as it was considered to

icance of vigorous vibration shown by females of the Amarillo ﬁsh be the case in related Goodea atripinnis (Nelson, 1975).

(Girardinichthys multiradiatus). This ﬁsh is one of several species Disentangling the possible functions of female vibration

of Goodeinae, a subfamily of freshwater, viviparous ﬁsh endemic requires evaluating the behaviour of males exposed to females

whose tendency to vibrate has been manipulated. Consequently

we ﬁrst established the nature of the sensory cues that evoke

∗ female vibration, and secondly we used this knowledge to manip-

Corresponding author.

E-mail address: [email protected] (A. Moyaho). ulate the female tendency to vibrate in the presence of males. We

164 L. Martínez Medina et al. / Behavioural Processes 100 (2013) 163–168

then evaluated the male responses to females and related them to (25 cm × 6 cm × 20 cm height) ﬁlled with water. Then, the ﬁsh was

the amount of vibration performed. gently pushed with a net against the tank’s front wall; from there

Although interacting cyprinodontiform ﬁsh use a variety of sen- it was measured using a plastic rule. Body mass of male and female

sory modalities, we focused on hydrodynamic cues because they ﬁsh was separately sorted into descending order. The four heaviest

are effective over short ranges (Webb et al., 2008; Bradbury and males and females formed the ﬁrst block; the same procedure was

Vehrencamp, 2011). As some lateral line receptors provide infor- repeated until the six blocks were completed. Each home aquarium

mation on water currents (Dijkgraaf, 1962; Münz, 1979), which was divided into 3 compartments (17 cm × 26 cm × 30 cm each)

may be produced by approaching conspeciﬁcs or predators (e.g., with acrylic dividers, and the ﬁsh, one-sex per aquarium, were

aquatic snakes), we used cobalt-dependent pharmacological block- individually placed within the compartments.

ade of the lateral line mechano-sensitivity (Karlsen and Sand, 1987; The order in which the blocks were tested was randomly

Satou et al., 1994; Janssen, 2000). In this way we could deter- selected, with one block run per day. The day before each block was

mine whether mechanical sensory cues were responsible for female run males and females were weighed again and four male–female

vibration. In addition, we temporarily concealed the female’s eyes dyads were formed according to body mass. Each dyad was ran-

because there is evidence that the sight of males also evokes female domly assigned to a treatment and to an observation tank, and the

vibration (Valero et al., 2005). order of observation was randomly selected. On the eve of each

trial the dyads were put in their corresponding observation tanks

2. Materials and methods to familiarize them with the experimental condition. A volunteer,

who was as blind as it was possible to the treatments applied to

2.1. Study population the ﬁsh, observed and recorded from 1230 to 1400 h the follow-

ing behaviours for 20 min (or less if the blindfolds covering the

Twenty-four male and female Amarillo ﬁsh (G. multiradiatus) eyes (see below) became detached from these): (1) Approaches,

from a dam in Lázaro, State of México, were used in this study. the number of times a male orientated himself towards and faced

The ﬁsh were collected using a 4.5-m long seine and brought a female. Concurrently, he moved towards her within approxi-

to the laboratory, where they were kept in mixed-sex groups in mately one body length. This is the average distance to which lateral

40 L glass aquaria and daily fed twice commercial food flakes. The line neuromasts detect water flows produced by fish (Dijkgraaf,

aquaria were equipped with sponge ﬁlters, aeration and aquatic 1962; Schellart and Wubbels, 1998; Wullimann, 1998). (2) Vibra-

weed for shelter. The aquaria with the ﬁsh were put in a regulated- tion, the number of times a female folded the dorsal and anal ﬁns

◦

temperature room (18–22 C) with a constant 12/12 h light/dark and lowered her head while ﬂicking it from side to side in a rapid

photoperiod (lights were turned on at 0700 h). Twenty-ﬁve days manner (Nelson, 1975; Macías Garcia, 1990). Tilting of the body

◦

before the experiment began the ﬁsh were separated by sex to varies in intensity from 0 to about 45 . (3) Flight, the number of

standardize their sexual response. All the ﬁsh were maintained in times a female ﬂed from a male approaching her. (4) Courtship,

accordance with institutional guidelines for the use of animals in the number of times a male either waived the median ﬁns or

research. displayed the ﬁgure-of-eight dance, which consists of the male

swimming forth and back in front of the female (Macías Garcia,

2.2. Experimental tank 1990; Gonzalez-Zuarth et al., 2011). (5) Chase, the number of times

a male orientated himself towards a female and pursued her.

We used 4 glass tanks (51 cm × 26 cm × 30 cm deep) for observ-

ing and recording the agonistic and courtship behaviour of 2.4. Mechanoreception (MI) and vision (VI) impairment

male–female dyads. Each tank had a gravel bottom, a diffuser con-

nected to a pump for aeration, and aquatic weed. We covered the Mechanoreception impairment consisted of exposing females

−1

−

back and sides of each tank with opaque paper. The aquatic weed to concentrations of either 0 mmol (MI ) or 1 mmol (MI+) L of

2+ TM

and paper were used for minimizing disturbance of the ﬁsh and cobalt chloride hexahydrate (Co ) (Fluka , Germany), which is

for presenting a uniform background during the observation of within the range of concentrations reported to inhibit the func-

behaviour. Four 20-W ﬂuorescent lamps, each placed on the top of tioning of the lateral-line organs (Karlsen and Sand, 1987; Satou

each tank, provided light for the observation. The four tanks were et al., 1994). Ninety minutes before each trial began, each female

put back-to-back and side-to-side on a table in a quiet room. A was taken out of the observation tank and placed in a glass jar con-

blind with a hole through which we observed the ﬁsh, provided us taining 1 L of water with the corresponding concentration of Co .

an appropriate condition for the observation. The jar had a diffuser connected to a pump to aerate the water.

We diminished the concentration of calcium (Ca ) in the water of

2.3. Experimental design the observation tanks to allow the Co to exert its effect as a cal-

cium channel antagonist (Stovner and Sognen, 1960). To diminish

2+ −1

We used four treatments to distinguish between the effect of the Ca concentration we added 0.5 mmol L of ethylene glycol-

mechanical and visual cues on female vibration; females had their bis tetraacetic acid (EGTA) (Sigma–Aldrich , St. Louis, MO, U.S.A.),

lateral line system intact or blocked and their eyes covered or which is a chelate with high afﬁnity for Ca . The addition of EGTA to

uncovered. The treatments were arranged in an incomplete six- the water of the observation tanks diminished the pH, and hence we

−1 TM

block balanced design (Cox, 1958) with two replicates per block. added 2 mol L of sodium hydroxide (Sigma–Aldrich , St. Louis,

Body size was used to group male–female dyads into blocks, as MO, U.S.A.) to restore the pH to the values recorded in the water of

it could be an indirect indicator of fecundity, mating success and the home aquaria (between 7.5 and 7.9).

survival (Werner and Gilliam, 1984; Gross and Sargent, 1985; After the treatment with Co , each ﬁsh was anesthetized by

Andersson, 1994; Macías Garcia et al., 1998). Body mass and placing it in a plate containing 100 ml of water with EGTA and 12

standard length, which is the distance from the snout tip to the drops of a solution containing benzocaine (Sigma–Aldrich , St.

end of the caudal peduncle, were used as measures of body size. Louis, MO, U.S.A.) diluted in acetone (1 g of benzocaine per 100 ml of

To estimate body mass, which was used to group the ﬁsh in blocks, acetone). Then we put the ﬁsh on a sponge soaked with water con-

each ﬁsh was put in a plastic bowl ﬁlled with water and weighted taining EGTA, and two small patches of black plastic (5 mm × 3 mm)

to the nearest g. To estimate standard length, which was used as were stuck on each eye (VI−) using adhesive tissue (3M Animal

a covariate (see below), each ﬁsh was put in a small glass tank Care Products, St. Paul, MN, U.S.A.). The patches of the sighted ﬁsh

L. Martínez Medina et al. / Behavioural Processes 100 (2013) 163–168 165

Table 1

(VI+) had a hole (about 1.5 mm diameter) cut out of for the pupil.

Statistical summary of (a) male approaches, (b) female vibration, (c) male courtship,

The patches were carefully ﬁxed so that no adhesive reached either

(d) female ﬂight, and (e) male chase in G. multiradiatus.

the operculum or the eyes. a

VI MI −

MI MI+

2.5. Data analyses (a)

VI+ 6.83 ± 1.49 6.17 ± 1.33

−

The number of male approaches was analyzed using linear VI 7 ± 3.04 6.33 ± 2.25

mixed models (LMMs) (Bolker et al., 2008), in which block was

(b)

deﬁned as a variable of random effects because we were not

VI+ 14.81 ± 10.99 1.85 ± 1.85

interested in estimating differences between blocks. Frequency of VI− 3.17 ± 3.17 –

approaches (square root transformation of data) was the response (c)

variable. MI, VI, female standard length (fSL) and male standard VI+ 2.78 ± 2.78 18.52 ± 9.37

− ±

length (mSL) were the explanatory variables. Since frequency of VI 7.14 5.46 –

male approaches was a function of fSL (see below), as previously (d)

reported (Bisazza, 1997), agonistic and courtship behaviours were VI+ – 8.33 ± 5.89

− ± ±

analyzed as proportion of male approaches. In this way we also VI 6.34 3.85 10.71 5.79

corrected any bias arisen from those cases in which the blind- (e)

folds became separated from the female’s eyes. Generalized Linear VI+ – 8.33 ± 11.78

VI− 2.77 ± 2.77 –

Mixed Models (GLMMs) were applied to data of female vibration,

a −1

courtship behaviour, ﬂight and chase using a binomial structure Mechanoreception (MI) and vision (VI) impairment. MI−, 0 mmol L of cobalt;

−1

−

of errors and a logit link function (Crawley, 2002). Again, block MI+, 1 mmol L of cobalt. VI , females with blindfolds; VI+ sighted females.

Mean ± SEM; ﬁgures from b to e are expressed as percentages of male

was deﬁned as a variable of random effects and each category of

approaches to which there was response.

behaviour as the response variable. MI and VI and the interaction

term between them were explanatory variables. In all these statis-

± −

tical analyses deletion tests were used for model simpliﬁcation so females more frequently (27.02 7.3%, n = 6) than VI+MI females

as to obtain a minimal adequate model (Crawley, 2002). Likelihood (4.87 3.36%, n = 6; Z = 2.43, p = 0.015, Fig. 3).

ratio tests ( ) were used for model selection, and Wald Z and t for Neither MI nor VI affected the mean proportion of female ﬂights

hypothesis testing. In addition, we used a loess smoothing method (Table 2), possibly as result of the variation in response within

(Martinez and Martinez, 2002) to model the relationship between

the proportion of female vibration and courtship behaviour. This

Table 2

model, which was run using MATLAB (v. 7.9.0.529), estimates two Summary of model simpliﬁcation of the ﬁt of LMMs to the number of male

parameters: ˛, which determines the degree of smoothing with approaches (a), and of GLMMs to female vibration (b), male courtship (c), female

ﬂight (d), and male chase (e).

high values yielding smoother curves, and which determines

the degree of the local regression. Cases in which occurred nei- Step Simpliﬁcation df LogLik Deviance p

ther courtship behaviour nor female vibration were discarded to change ( )

make the model robust. All other statistical analyses were done

(a) – 8 −17.88

using R (RDCT, 2011) and the lme4 package (Bates et al., 2011). Maximal

model

An alpha-value lower than 0.05 was considered statistically signif-

−

icant. 1 MI + VI + fSL + mSL 7 27.45 19.13 0.058

2 MI + VI + fSL 6 −27.79 0.69 0.406

3 MI + fSL 5 −27.82 0.06 0.799

4 fSL 4 −28.33 1.02 0.313

3. Results

5 Intercept 3 −31.36 6.06 0.013

(b) – 5 −12.9

Overall, the behaviours recorded as responses to male

Maximal

approaches varied among treatments and in some cases they were

model

absent (Table 1). Since males approached females to a similar extent

1 MI + VI 4 −13.26 0.72 0.396

−

regardless of the treatment (Table 1), the variation in response to 2 MI 3 13.87 1.22 0.269

3 Intercept 2 −17 6.26 0.012

male approaches was a result of the effect of the sensory impair-

ment imposed on the females. (c) – 5 −10.28

Only fSL contributed signiﬁcantly to total variation in frequency Maximal

model

of approaches (t17 = 2.51, p = 0.022, n = 12, Table 2 and Fig. 1).

1 MI + VI 4 −16.02 11.48 0.000

Approaches increased with fSL, although the proportion of the

(d) – 5 −9.76

variance explained by the statistical model was small (regression

2 Maximal

analysis, r = 0.22, F1,22 = 6.32, p = 0.019). This result is consistent

model

with previous studies with other species [see e.g., (Turner, 1993)],

1 MI + VI 4 −10.56 1.61 0.204

and indicates that female body size might reﬂect fecundity, assum- 2 VI 3 −10.57 0.02 0.899

−

ing that both traits correlate positively (Andersson, 1994; Herdman 3 Intercept 2 12.03 2.91 0.087

et al., 2004; Macías Garcia et al., 1998).

(e) – 5 −5.23

As regards female vibration, the minimal adequate model only Maximal

included MI (Table 2). The mean proportion of vibration in the model

1 MI + VI 4 −6.63 2.8 0.094

females exposed to MI+ (1.3 ± 1.3%, ±SEM) was signiﬁcantly lower

2 MI 3 −6.63 0.00 0.985

(Z = −2.09, p = 0.036, n = 12) than that of females exposed to MI−

3 Intercept 2 −6.64 0.01 0.942

(12 ± 3.56%; Fig. 2).

Mechanoreception (MI) and vision (VI) impairment, female (fSL) and male (mSL)

The minimal adequate model for courtship behaviour included

standard length. The plus mark denotes inclusion of an explanatory variable in the

all the terms (Table 2). However, only MI contributed signiﬁcantly

model. p-Values refer to the change in deviance when the respective terms are

to the variation in courtship behaviour; males courted VI+MI+ removed from the model.

166 L. Martínez Medina et al. / Behavioural Processes 100 (2013) 163–168 Number of approaches Mean percentage of courtship behaviour 246810121416182022 0 0 5 10 15 20 25 30 35 26 28 30 32 34 36 38 40 42 0 1 −1

Female standard length (mm) Cobalt (mmol) l

Fig. 1. The number of male approaches increases with female standard length. Each Fig. 3. Impairment of the function of the female lateral line system prompted

circle represents the approaches number of one male towards one female of a given males to display courtship behaviour. The bars represent the mean percentage of

length. The solid line is the best ﬁt of a regression analysis to the data, r = 0.22, courtship displays and the vertical lines on each bar SEM. The difference between

−1

F1,22 = 6.32, p = 0.019, n = 24. the courtship displayed to the group of female ﬁsh with 0 mmol L and the group

−1

with 1 mmol L of cobalt was statistically signiﬁcant, Z = 2.43, p = 0.015, n = 6.

males also did not show courtship behaviour, very likely because

treatments (Table 1). The minimal adequate model was a null

the females ran away (Table 1).

model (−3.232 ± 0.416, coefﬁcient ± SE), and none of the deletion

tests indicated a signiﬁcant loss of the explanatory power of the

reduced models (Table 2, p > 0.05). 4. Discussion

The mean proportion of male chases directed towards females

did not vary regardless of the treatments applied to females We assessed whether female vibration serves as a courtship

(Tables 1 and 2). Indeed the minimal adequate model was a display or as an appeasement response to sexual harassment

null model (−4.356 ± 0.711). Finally, the loess-smoothing model engendered by males. We used a stimulus control approach, tem-

revealed a negative association between the proportions of vibra- porarily blocking the perception of the cues (mechanical or visual)

tion and courtship (Fig. 4). When the females did not vibrate at all, that we had reason to believe were involved in female detection of

approaching males. We did not directly demonstrate the physio-

logical effect of Co on the functioning of the lateral line organs of Proportion of vibrations Mean percentage of vibrations

−0.125 0.125 0.375 0.625 0 2 4 6 8 10 12 14 16 18

0 1 −0.1 0.0 0.1 0.20.30.40.50.6 −

Cobalt (mmol) l 1 Proportion of courtship displays

Fig. 2. Impairment of the function of the female lateral line system inhibits female Fig. 4. Female vibration decreases with male courtship in 8 male–female dyads

vibration. The bars represent the mean percentage of female vibration and the verti- of ﬁsh. Each circle represents the joint proportion of vibration and courtship of

cal lines on each bar ± SEM. The difference between the treatments was statistically each dyad. The solid line is the ﬁt of a loess-smoothing model to the data with

signiﬁcant, Z = −2.09, p = 0.031, n = 12. the following estimates for the parameters: ˛ = 0.5 and = 1.

L. Martínez Medina et al. / Behavioural Processes 100 (2013) 163–168 167

the ﬁsh used in this study. Nonetheless the behavioural difference this conclusion, but instead suggest that female vibration inhibits

between treated and untreated females, as well as the known effect male aggression by discouraging males from escalating courtship.

of Co (Karlsen and Sand, 1987; Satou et al., 1994), convinced us Both female ﬂight and male chase, which are indicators of male

that the observed effects were the result of the action of Co . As aggression, were not observed when females vibrated more.

to the patches of plastic used to cover the females’ eyes, pilot trials In conclusion the ﬁndings of this study indicate that female

indicated that the females with blindfolds swam round the aquar- vibration of G. multiradiatus is an appeasement signal and suggest

ium close to the walls. They moved as if they wanted to remove that it may also have a function in eliciting male courtship. Further

the patches from their eyes. These observations thus suggest the studies will reveal which components of female vibration either

females with blindfolds were unable to see. After a few minutes attract males and stimulate them to display courtship or deter them

the females seemingly became accustomed to the blindfolds. from escalating courtship.

Our results indicate that hydrodynamic cues play a determin-

ing role in eliciting female vibration. However, both acoustic and

Acknowledgements

hydrodynamic components could have been important for females

to be able to identify approaching males. There are examples where

We thank H. Ajuria Ibarra who observed and recorded the

the two sensory modalities are involved in the spatial localization

ﬁsh’s behaviour. We also thank E. Beristain Castillo and J.L. Salazar

of stimulus sources (Webb et al., 2008 for a review concerning mul-

Bautista for their help to collect and care the ﬁsh. We are indebted to

timodal sensory integration). In fact, sighted females also vibrated

R. Berra and M. Mogdans for suggestions on methodological issues.

when mechanoreception was impaired suggesting that visual cues

The work described in this paper forms part of a B.Sc. thesis submit-

are also capable of eliciting vibration albeit to a lesser degree. This

ted to the B. Universidad Autónoma de Puebla by LMM. This work

is consistent with the report that G. multiradiatus females vibrated

was partially funded by the Vicerrectoria de Investigación of the B.

within a closed respirometer on sight of a male (Valero et al., 2005),

Universidad Autónoma de Puebla.

although such outcome could also be the result of acoustic cues.

In contrast to the decrease of female vibration, courtship dis-

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