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Corresponding author: Rucha Karkarey ( rucha@ncf-india.org ) Academic editor: Chris Harrod
© 2019 Rucha Karkarey, Amod Zambre, Kavita Isvaran, Rohan Arthur.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Karkarey R, Zambre A, Isvaran K, Arthur R (2019) Hypothesizing novel mating behaviours in the squaretail grouper based on direct behavioural observations. Rethinking Ecology 4: 103-104. https://doi.org/10.3897/rethinkingecology.4.33383
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Historically unfished, high-density spawning aggregations are vanishingly uncommon. Behavioural observations from such aggregations are rare, and may be sometimes novel and unexpected. Given the weight of evidence required to document spawning aggregations, how can we best report rare and unusual behavioural variations in spawning populations? Based on two years of in-water observations of a high-density spawning aggregation of the squaretail grouper in the Lakshadweep Archipelago, we described a previously unreported male alternative reproductive tactic (ART) and an inverse size assortment with large males courting several small females that shoaled mid-water (https://doi.org/10.1186/s12898-017-0120-5). In critiquing our manuscript, it has been suggested that our observations, methodologies and interpretation are inadequate, flawed, and do not fit within currently accepted theory (https://doi.org/10.1186/s12898-018-0206-8). While offering a detailed counter of the main methodological and theoretical criticisms we question how best to document and interpret novel behaviours in poorly known systems. Reporting novelty itself can hardly be the basis of criticism. Our report relied on direct in-water observations, conducted at peak densities over two spawning years. The critique ignores this, choosing instead to focus on a supplementary video which was not the basis of our conclusions. Like other researchers working on this species, we did not directly observe mating, but report courtship as a well-established proxy used across mating systems studies. Apart from these methodological concerns, the authors suggest that there is no theoretical support for our observations. However, sexual selection theory provides well-established frameworks showing that, at very high mating densities, a variety of tactics can emerge, that often vary considerably between populations and locations. In our original paper, we use this broader theory of sexual selection together with detailed behavioural data to propose plausible evolutionary explanations that bear testing in these novel, high-density systems. We agree with the authors that novel observations should be scrutinised carefully as they can challenge our current understanding of the range of behaviours populations display and serve as a springboard for theoretical advancement. Given their rarity, these observations should be evaluated against the rigour of their documentation and the transparency of their reporting. In this context, we hope our carefully documented observations serve as a useful addition to the fascinating and complex natural history of species like the squaretail grouper.
Theoretically grounded natural history is the foundation on which behavioural ecology rests. Observations in the real world demonstrate the range of responses species can show under a spectrum of contexts and conditions. Behaviours at extremes of this spectrum are particularly insightful since they serve as vital tests of theory. Given how important these observations are, it is only right that they are subject to greater intellectual scrutiny than mere confirmations of the norm. However, field observations at these extremes are typically rare and often limited to anecdotal accounts that are difficult to verify. It is therefore critical, in the few instances where circumstances make it possible, that studies follow standardly accepted protocol and are transparent in their reporting. These are the standard burdens of proof required for any observational study, and the scientific community should ask no less – and no more of these observations to include them in the canon of theoretical and observed species behaviours. When done right, observations at the extreme can challenge and advance our understanding of behavioural theory, even when they may require further observations and tests to confirm them.
In a manuscript published in the journal BMC Ecology (
Our paper documented mating behaviours of the squaretail grouper at a natural and extreme end of the density spectrum that had not been previously addressed in the literature. The squaretail grouper has more usually been observed at spawning aggregations exposed to years of fishing and human disturbance. We monitored reproductive behaviour for over two years in the absence of fishing activities, using carefully designed and well-established ecological and behavioural methodologies. At peak densities, we recorded an average of 72.08 ± 27.46 fish per 1000 m3 (200m2 × 5m depth) across the spawning site. Densities were more than 4 times higher on the slope of the spawning site, where we documented the alternative school spawning tactic (
1. the influence of density on the expression of alternative reproductive tactics and
2. the role of female behaviour and choice in influencing male mating tactics.
Both these are common processes that have been tested across the animal kingdom.
Here, we respond to the allegations made by
We observed courtship patterns at the Bitra aggregation for two years using in-water observations by three of us (RK, RA and AZ). All the conclusions of our original manuscript are based on direct observations. Much of the critique of our works focuses on a forensic analysis of a supplementary video we submitted along with the manuscript. However, this gives the video more importance than it deserves. The video was captured by a remote underwater camera, when we were NOT in the water and at no point in our paper do we present the video as conclusive evidence but merely as supporting what we observed in situ.The two incidents of ‘school spawning’ have been described as a sequence of events, culminating in gamete release in our manuscript (
The work of
The authors of the critique call into question our observations and our broader understanding of grouper mating systems, although we have specifically acknowledged the diversity of mating strategies of groupers with relevant citations (
A major point of contention is how population density specifically affects grouper mating systems.
Variation in mating tactics between populations of the same species is hardly unusual. Density(or potential mates) can interact with environmental factors to affect mating tactics in complex ways (
Firstly, there is a rich body of work showing that male and female mating tactics are more variable than previous thought. Males and females may make mating decisions that are not initially “intuitive” but are adaptive when studied over individual lifetimes. For example, paternity studies have shown that in bighorn sheep (Ovis canadensis), subordinate, younger males following a ‘low-benefit’ harassment tactic gain almost as much paternity as dominant males following a mate-guarding tactic (
Secondly, multiple females mating with a single male is not puzzling but seen commonly as in the case of leks. In lek mating systems, females are commonly choosy about mates, exhibit strong mate choice and mating success is commonly highly skewed towards a small percentage of males. In addition, even in such extreme polygynous systems, associations between multiple females and a single male, and female-female competition for individual males on leks have been reported (
The authors suggest that we did not sample during spawning periods. However, as we described in detail in the paper (
To reiterate, we found that groupers arrive two days before the new moon, reached their highest densities on new moon day and then dropped in density by 80% the day after new moon, and by 98% by the third day after the new moon. In the absence of histological means to assess spawning time, we triangulated the spawning time based on the dramatic drop in densities after new moon day and the absence of highly gravid females at the aggregation site after new moon days. In addition to this, from our focal behavioural observations we found that males spent upto 50% more time in intra-sexual aggression on the evenings of new moon days compared to days and periods prior to and after the new moon. Taken together, our in-water observations gave us enough confidence that we were sampling as close to the spawning period as possible (ie. afternoons of new moon days).
The criticism that we used invalid methods to estimate courtship rates has also been carefully addressed in our original paper. We have clearly described that we do not measure courtship rates, but in fact measure ‘association rates’ as a proxy for ‘potential mating opportunities’ (
Male fitness is ideally measured over an individual’s life time and using genetic methods to determine paternity (
We wholeheartedly agree with
Writing in the 1970s, Paul
RK and RA conceived and designed the experiments, performed the experiments, analyzed the data, authored and reviewed drafts of the paper and approved the final draft. AZ performed the experiments, authored or reviewed drafts of the paper. KI conceived and designed the experiments, analyzed the data and authored or reviewed drafts of the final paper. RK and RA 60%, KI 20%, AZ 20%.
We would like to thank T. Alcoverro, S. Quader and M. Gangal for their support and invaluable feedback on this rebuttal. We would also like to thank two anonymous reviewers for significantly improving the quality of the manuscript.