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Alternative Reproductive Tactics and Inverse Size-Assortment in a High-Density Fish Spawning Aggregation"

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Alternative Reproductive Tactics and Inverse Size-Assortment in a High-Density Fish Spawning Aggregation UC Santa Barbara UC Santa Barbara Previously Published Works Title Fake spawns and floating particles: a rebuttal of Karkarey et al. "Alternative reproductive tactics and inverse size-assortment in a high-density fish spawning aggregation". Permalink https://escholarship.org/uc/item/13z9383t Journal BMC ecology, 18(1) ISSN 1472-6785 Authors Erisman, Brad E Barreiros, João P Rhodes, Kevin L et al. Publication Date 2018-11-27 DOI 10.1186/s12898-018-0206-8 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Erisman et al. BMC Ecol (2018) 18:48 https://doi.org/10.1186/s12898-018-0206-8 BMC Ecology CORRESPONDENCE Open Access Fake spawns and foating particles: a rebuttal of Karkarey et al. “Alternative reproductive tactics and inverse size‑assortment in a high‑density fsh spawning aggregation” Brad E. Erisman1* , João P. Barreiros2 , Kevin L. Rhodes3 and Robert R. Warner4 Abstract Courtship and spawning behaviors of coral reef fshes are very complex, and sufcient sampling efort and proper methods are required to draw informed conclusions on their mating systems that are grounded in contemporary theories of mate choice and sexual selection. We reviewed the recent study by Karkarey et al. (BMC Ecol 17:10, 2017) on the spawning behavior of Squaretail coralgrouper (Plectropomus areolatus) from India and found no evidence to support their fndings of alternative reproductive tactics, unique school-spawning involving a single male with multi- ple females, or inverse size-assortment. The study lacks scientifc credibility due to a lack of rigor in the methodology used, misinterpretation of observed behaviors, misinterpretation of the literature, and insufcient data. Their approach led the authors to produce spurious results and profound, invalid conclusions that violate the most basic assumptions of mate choice and sexual selection theory as applied to mating systems in marine fshes. Keywords: Spawning aggregation, High mating density, Alternative reproductive tactics, Shoal and pair courtship tactics, Inverse size-assortment, Squaretail coralgrouper Main text males courted small females on the reef slope while small In a recent issue in this journal, Karkarey et al. [1] con- males courted equal-sized or larger females on the shelf.” ducted an observational study of the mating system Both of these reported mating behaviors would appear of the Squaretail coralgrouper (Plectropomus areo- to violate the most basic assumptions of mate choice and latus) at a “pristine” site of Bitra, a remote atoll in the sexual selection theory as applied to marine fshes, and northern Lakshadweep archipelago of India. As part of thus the study demanded further scrutiny. their principal fndings, Karkarey et al. [1] described an After careful consideration, we report here that the extraordinary mating behavior referred to as a “unique results of Karkarey et al. [1] are unsupportable and their school-spawning tactic” in which multiple females conclusions are invalid, as both were based on false inter- group-spawned with a single male. Tis mating style has pretations of behavioral observations, a lack of rigor in never been reported in any broadcast spawning species the methods chosen, and a lack of data to support their of marine fsh, and as such, it would be a unique and conclusions. In discussing their fndings, the authors important discovery. Similarly, they also reported that P. failed to provide any explanation on the proximate or areolatus at Bitra showed a habitat-specifc, inverse size- ultimate causes of such unique behaviors that were assortment in relationship to courtship in which “large grounded in or supported by empirical evidence from contemporary theories on sexual selection, mate choice, and mating systems in marine fshes. Te legitimacy *Correspondence: [email protected] 1 Marine Science Institute, The University of Texas at Austin, 750 Channel of the study was further undermined by the exclusion, View Drive, Port Aransas, TX 78373‑5015, USA misinterpretation, and improper citation of previous Full list of author information is available at the end of the article studies on the mating behavior of P. areolatus and other © The Author(s) 2018. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat​iveco​mmons​.org/licen​ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creat​iveco​mmons​.org/ publi​cdoma​in/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Erisman et al. BMC Ecol (2018) 18:48 Page 2 of 7 marine fshes and seminal literature on mating systems see from any distance (BEE, KLR, JPB, RRW pers. obs.). and sexual selection. Based upon the serious issues con- Upon reviewing the video in slow motion, we confrmed tained in the study, which we grouped into fve categories the object circled in Fig. 2d of Karkarey et al. [1] is not described below, we concluded that the study by Karka- a gamete cloud at all but rather a small, white particle rey et al. [1] lacks scientifc merit and should be retracted drifting in the water column very close to the camera from the literature. lens. Te particle appears clearly in the clip at 0:14 s, dur- ing the slow motion footage, where it is located in open (1) False observations of spawning events involving water just below the center of the aggregation. It then a single male with multiple females moves from left to right and passes rapidly across the Karkarey et al. [1] claim they observed two instances camera lens and in directly in front of the group of fsh as (once each in 2013 and 2014) of a unique and novel they come together (0:15 s), giving the false appearance “school-courtship culminating in gamete release”, each of a possible, faint, small, gamete cloud when viewed cas- involving a single male and 4 to 5 female P. areolatus from ually at normal speed. Immediately after, it becomes clear within a larger school of females. To support their claim, that the ‘gamete cloud’ is a particle, as the object changes they provide a photograph in the manuscript (Fig. 2d in directions completely and moves rapidly from right to [1]) taken from a video clip of the frst supposed spawn- left in a diferent direction, on a diferent plane, and at a ing event observed in 2013, which is also included in the much faster rate than any of the fsh associated with the publication as supplementary information (Additional event. Te particle exits the screen at 0:18 s of the video fle 2 in [1]). Te authors contend that the photograph clip, while passing in front of other fsh that are viewable and the video clip reveal a “school-spawning tactic” that on the screen. We provide still frames of the particle and “involved an upward spawning rush within the school in its movement in Fig. 1 and encourage readers to carefully the water column commonly seen in mass-spawning fsh”. compare this sequence with Fig. 2d and the supplemen- Tey also explain that females involved in the observed tary video provided by Karkarey et al. [1] to draw their spawning event could be “clearly identifed based on their own conclusions. distended bellies” and “simultaneously released gametes as a cohesive unit”. (2) No empirical evidence of single male–multiple female Each of us has observed the video fle numerous times, spawning in P. areolatus, groupers, or any other coral reef both in real time and in slow motion, and we can fnd no fsh plausible evidence of spawning or of any of the behaviors Karkarey et al. [1] misrepresents the novelty of female described by Karkarey et al. [1]. In direct contrast to the P. areolatus schools. As early as 1999, Johannes et al. [2] article’s description of spawning in the video, the group- reported that the “schools of female P. areolatus swim- ers swim rapidly downward toward the reef rather than ming to, from or within spawning aggregations seem to upward, with individuals colliding briefy in a very disor- be the only example of single-sex schooling behavior we ganized manner before dispersing. Te event ends with know of among groupers within this genus”. Johannes the lead individual (small, with dark color phase typi- et al. [2] also described in great detail that when roving cal of females; see page 44 in [2]) involved in the event schools of females passed over males occupying territo- swimming rapidly downward and into the reef as it is ries on the reef, the males would “break quickly into the pursued by a larger individual exhibiting the camoufage school [of females], pushing sideways vigorously with color phase (which can be either a male or a female [2]). their bodies against females, apparently trying to sepa- Most of the individuals involved in the incident appear to rate them from the school… In apparent response to exhibit the dark color phase typical of schooling females these eforts, individual females would leave the school [2]. Te “spawning” event occurs far in the distance, with and move to the bottom.” Johannes et al. [2] proposed no individuals with distended bellies apparent, suggest- several plausible explanations for the formation of female ing these individuals are not females ready to spawn. schools, including anti-predator measures and protection Further inspection of the proposed “gamete cloud” of harassment and mobbing by males. Karkarey et al. [1] (circled in Fig. 2d in [1]) served as the most conclusive cite the work done by Johannes et al.
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