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Reproductive behaviors and sex roles during a diurnal cycle of the goby, Lythrypnus pulchellus (Teleostei: Gobiidae)

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Abstract

Reproductive behaviors are a key factor to achieve successful spawning and fertilization in sexual species. Among harem polygynous site-attached reef fishes, relative size and sexual proportions may be determinant to establish hierarchies and sexual roles during reproductive behavior. In the present study the pattern of reproductive behavior (courtship, intrasexual competition and parental care) of the gorgeous goby, Lythrypnus pulchellus, a small cryptobenthic diurnal reef species endemic to the tropical eastern Pacific is described for the first time. We tested the plasticity of sex roles using two treatments, one biased towards males and one biased towards females. The influence of daylight on reproductive behaviors was also assessed. The characterization, frequency and duration of reproductive displays were obtained from video-recorded observations under laboratory captive conditions each day from 8:00 to 19:00 h for 10 min every hour over 5 days. Sixteen displays were identified, of which “Jerk”, “Nest Defense”, “Parental Care” and “Nipping” were exhibited only by males. “Nest Approach” and “Solicitation” were displayed only by females, and the remaining 10 behaviors were identified in both sexes. The apparent “rule” to form a social hierarchy among individuals of the more abundant sex was body size, with the largest becoming the dominant individual. Females courted more than males in both biased sex ratios experiments. Comparing the rate of courtship between males in the male-biased treatment with males in the female-biased treatment, it was evident that courtship rate was higher in the latter case. In the male-biased treatment, the rate of courtship was higher in the smaller (subordinate) male than in the larger (dominant) male. However, males and females are similar in competition in any of the biased sex ratio experiments. It leads to the conclusion that the gorgeous goby shows plasticity in their reproductive behaviors in response to OSR. The frequencies and durations of reproductive behaviors of both males and females decreased according to time of day in both biased sex ratio experiments, except for the courtship behaviors “Nest approach” in females and “Nest defense” in males that increases throughout the day. The elucidation of the plasticity of mating behaviors is relevant to understand the interactions in sequential hermaphrodite fishes as L. pulchellus.

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Acknowledgements

We thank E. Calvillo, J. Angulo, M. Cota and A. González for assistance in field work at the aquaculture farm. P. Monsalvo, G. Robles, L. M. Vázquez and J. Cobos helped maintain aquariums and fish health throughout the study. M. Trujillo-García helped with behavioral observations and fish maintenance. R. Andrade and D. Paz García assisted with video and photograph editing. Thanks also to N. Bocanegra Castillo, L. Campos Dávila and R. Ochoa for laboratory assistance, and to M. C. Blázquez for comments on an earlier draft of the manuscript. This work was partially funded by the project PEP of CIBNOR to EFB. S. M.-A. was a recipient of student fellowships from CONACYT (351061).

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Correspondence to Eduardo F. Balart.

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10164_2019_624_MOESM1_ESM.mp4

S1 Video showing examples of reproductive behaviors of the gorgeous goby, Lythrypnus pulchellus. Courtship displays: Nest defense, a male remains in the nest or at its entrance. When another individual swims past or approaches the nest, the male quickly enters the nest or sometimes displaces the individual approaching the nest; Nest approach, a female approaches the nest but maintains a distance of a body-length away from it; Solicitation, is the slow forward movement of a female at a distance ≤ 15 cm from a male, followed by an immobile posture in which she either faces the nest entrance or aligns herself perpendicular to the male, while displaying various postures such as arching or curving the body. Females sometimes flap rapidly one of the pectoral fins, while keeping the dorsal fin erected to show her distended abdomen to the male, indicating the presence of mature eggs and thus ready to spawn; Male direct approach, a male rapidly approaches a female at a distance of <5 cm. This type of approach can end with physical contact of both individuals; Female displacement, a female quickly swims away from a male at a distance of ~5 cm in response to an Approach, a Direct Approach or a Threat; Jerk, is zigzag forward swimming motion along with quick and intermittent lateral movements of the body performed by the male. These can be directed toward a nest or displayed to the female; Spawning, a female enters the nest and deposits eggs on its upper surface while performing quick and “choppy” lateral movements, and the male makes similar movements as he subsequently fertilizes the egg mass. During spawning, the male fertilizes the eggs or guards the nest entrance. At the end of spawning, the female exits the nest leaving the male inside. Parental care: a male remains in or at the entrance to the nest after eggs have been laid and fertilized. He often rapidly moves pectoral and caudal fins and makes rapid lateral and “choppy” body movements. Female intrasexual competition displays: Direct approach, a female rapidly approaches another at a distance of <5 cm. This type of approach can end with physical contact of both individuals; and Displacement, a female quickly swims away from another at a distance of ~5 cm in response to an Approach, a Direct Approach or a Threat. Video by Sayuri Muñoz-Arroyo (MP4 69033 kb)

10164_2019_624_MOESM2_ESM.tif

Fig. S1 Frequency of courtship behaviors (individual behavior bouts) in: a) Treatment 1(T1, 1 female + 2 males, dominant and subordinate); and b) Treatment 2 (T2, 2 females, dominant and subordinate + 1 male). Abbreviations: Ap. F to DM, Female approach to dominant male; Ap. DM to F, Dominant male approach to female; Ap. SM to F, Subordinate male approach to female; Ap. F to SM, Female approach to subordinate male; Ap. M to DF, Male approach to dominant female; Ap. DF to M, Dominant female approach to male; Ap. SF to M, Subordinate female approach to male; Ap. M to S, Male approach to subordinate female; Avo. F of DM; Female avoidance of dominant male; Avo. DM of F, Dominant male avoidance of female; Avo. SM of F, Subordinate male avoidance of female; Avo. F of SM, Female avoidance of subordinate male; Avo. M of DF, Male avoidance of dominant female; Avo. DF of M, Dominant female avoidance of male; Avo. SF of M, Subordinate female avoidance of male; Avo. M of SF, Male avoidance of subordinate female; DApr. F to DM, Female direct approach to dominant male; DApr. DM to F, Dominant male direct approach to female; DApr. SM to F, Subordinate male direct approach to female; DApr. F to SM, Female direct approach to subordinate male; Dis. F of DM, Female displacement of dominant male; Dis. DM of F, Dominant male displacement of female; Dis. SM of F, Subordinate male displacement of female; Dis. F of SM, Female displacement of subordinate male; Jerk DM, Dominant male jerk; Jerk SM, Subordinate male jerk; Sol. F to DM, Female solicitation to dominant male; Sol. F to SM, Female solicitation to subordinate male, TWag DM, Dominant male tail waggle; TWag F, Female tail waggle; TWag SM, Subordinate male tail waggle. DApr. M to DF, Male direct approach to dominant female; DApr. DF to M, Dominant female direct approach to male, DApr. SF to M, Subordinate female direct approach to male; DApr. M to SF, Male direct approach to subordinate female; Dis. M of DF, Male displacement of dominant female; Dis. DF of M, Dominant female displacement of male; Dis. SF of M, Subordinate female displacement of male, Dis. M of SF, Male displacement of subordinate female; Sol. DF, Dominant female solicitation; Sol. SF, Subordinat female solicitation; TWag. DF, Dominant female tail waggle; TWag. M, Male tail waggle; TWag. SF, Subordinate female tail waggle. Black lines show the median, dotted the whiskers and points the outliers. Number of individuals for Treatment 1 = 1 female, 2 males for tank (number total of individuals for 3 replicated tanks = 3 females, 6 males). Number of individuals for Treatment 2 = 2 females, 1 male for tank (number total of individuals for 3 replicated tanks = 6 females, 3 males). (TIFF 725 kb)

10164_2019_624_MOESM3_ESM.tif

Fig. S2 Frequency of intrasexual competition behaviors in: a) Treatment 1 (T1, 1 female + 2 males, dominant and subordinate); and b) Treatment 2 (T2, 2 females, dominant and subordinate + 1 male). Abbreviations: Ap. SM to DM, Subordinate male approach to dominant male; Ap. DM to SM, Dominant male approach to subordinate male; Avo. SM of DM, Subordinate male avoidance of dominant male; Avo. DM of SM, Dominant male avoidance of subordinate male; Bite DM, Dominant male bite; Bite SM, Subordinate male bite; DApr. SM to DM, Subordinate male direct approach to dominant male; DApr. DM to SM, Dominant male direct approach to subordinate male; Dis. SM of DM, Subordinate male displacement of dominant male; Dis. DM of SM, Dominant male displacement of subordinate male; Shake DM, Dominant male shake; Shake SM, Subordinate male shake; TWag. DM, Dominant male tail waggle; TWag. SM, Subordinate male tail waggle. Ap. SF to DF, Subordinate female approach to dominant female; Ap. DF to SF, Dominant female approach to subordinate female; Avo. SF of DF, Subordinate female avoidance of dominant female; Avo. DF of SF, Dominant female avoidance of subordinate female; Bite DF; Dominant female bite; Bite SF; Subordinate female bite; DApr. SF to DF, Subordinate female direct approach to dominant female; DApr. DF to SF, Dominant female direct approach to subordinate female; Dis. SF of DF, Subordinate female displacement of dominant female; Dis. DF of SF, Dominant female displacement of subordinate female; Shake DF, Dominant female shake; Shake SF, Subordinate female shake; Dominant female tail waggle; TWag. SF, Subordinate female tail waggle. Black lines show the median, dotted the whiskers and points the outliers. Number of individuals for Treatment 1 = 1 female, 2 males for tank (number total of individuals for 3 replicated tanks = 3 females, 6 males). Number of individuals for Treatment 2 = 2 females, 1 male for tank (number total of individuals for 3 replicated tanks = 6 females, 3 males). (TIFF 628 kb)

10164_2019_624_MOESM4_ESM.tif

Fig. S3 Effect plots of GLMM applied to frequency of courtship records using behavioral data: a) Treatment 1 (T1, 1 female + 2 males, dominant and subordinate); and b) Treatment 2 (T2, 1 male + 2 females, dominant and subordinate). Solid line shows effect of daylight hour on frequency of courtship behaviors. Number of individuals for Treatment 1 = 1 female, 2 males for tank (number total of individuals for 3 replicated tanks = 3 females, 6 males). Number of individuals for Treatment 2 = 2 females, 1 male for tank (number total of individuals for 3 replicated tanks = 6 females, 3 males). (TIFF 2660 kb)

10164_2019_624_MOESM5_ESM.tif

Fig. S4 Effect plots of GLMM applied to frequency of competition records using behavioral data: a) Treatment 1 (T1, 1 female + 2 males, dominant and subordinate); and b) Treatment 2 (T2, 2 females, dominant and subordinate + 1 male). Solid line shows effect of daylight hour on frequency of behaviors. Number of individuals for Treatment 1 = 1 female, 2 males for tank (number total of individuals for 3 replicated tanks = 3 females, 6 males). Number of individuals for Treatment 2 = 2 females, 1 male for tank (number total of individuals for 3 replicated tanks = 6 females, 3 males). (TIFF 741 kb)

10164_2019_624_MOESM6_ESM.tif

Fig. S5 Effect plots of GLMM applied to duration of courtship records using behavioral data: a) Treatment 1 (T1, 1 female + 2 males, dominant and subordinate); and b) Treatment 2 (T2, 1 male + 2 females, dominant and subordinate). Solid line shows effect of fish sex-status identity (ID) and daylight hour on frequency of courtship behaviors. The pink bars and the blue shaded regions in the hour plots mean standard errors. Black lines at the bottom is the rug plot shows the amount of data of each hour. Number of individuals for Treatment 1 = 1 female, 2 males for tank (number total of individuals for 3 replicated tanks = 3 females, 6 males). Number of individuals for Treatment 2 = 2 females, 1 male for tank (number total of individuals for 3 replicated tanks = 6 females, 3 males). (TIFF 1685 kb)

10164_2019_624_MOESM7_ESM.tif

Fig. S6 Effect plots of GLMM applied to duration of competition records using behavioral data: a) Treatment 1 (T1, 1 female + 2 males, dominant and subordinate); and b) Treatment 2 (T2, 2 females, dominant and subordinate + 1 male). Solid line shows effect of fish sex-status identity (ID) and daylight hour on frequency of behaviors. The pink bars and the blue shaded regions in the hour plots mean standard errors. Black lines at the bottom is the rug plot shows the amount of data of each hour. Number of individuals for Treatment 1 = 1 female, 2 males for tank (number total of individuals for 3 replicated tanks = 3 females, 6 males). Number of individuals for Treatment 2 = 2 females, 1 male for tank (number total of individuals for 3 replicated tanks = 6 females, 3 males). (TIFF 788 kb)

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Muñoz-Arroyo, S., Martínez-Rincón, R.O., Findley, L.T. et al. Reproductive behaviors and sex roles during a diurnal cycle of the goby, Lythrypnus pulchellus (Teleostei: Gobiidae). J Ethol 38, 79–98 (2020). https://doi.org/10.1007/s10164-019-00624-3

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