Interspecific interactions of Lunartail Grouper (Variola Louti) in Ras Mohammed,
Red Sea, Egypt
Matteo Buffi, Paolo Norambuena & Pietro Storelli
Abstract:
Marine ecosystems, especially reef ecosystems are often governed by interspecific relationships of different nature. Those associations are flexible and can change over a day period depending on the activity of different collaborators. Groupers (Family Serranidae), are well known for their variate associations, from a cleaning service by Cleaner Wrasse to initiate hunting collaborations with Moray Eels. The latter, in particular, even tough being spotted several times is still considered as a rare event. In this work different activity patterns, namely cleaning and cooperative hunting behaviors, have been studied for the Lunartail Groupers of Ras Mohammed, Red Sea, Egypt. By observing and recording the duration of different activities of the fish regarding trhee different times of the day (morning, noon and evening) and their size. We have been able to see a trend in which the groupers tend to start cooperative hunting association during dusk times (morning and evening) and contrarily to perform more cleaning associations during midday. Confirming our hypothesis of different collaboration activities during different time of the day. Our findings suggest that such associations are not rare as thought. Something relevant for conservation strategies, as disrupting one of those association could provoke a chain of event for other associated marine species.
Keywords: Interspecific-Cooperation, foraging, coral reef, Lunartail Grouper, Ras Mohammed, Red Sea, Egypt.
Introduction
Groupers are carnivorous, predator fishes belonging to the family of Serranidae, which are distributed worldwide. This particular group of fishes is generally known to solitarily hunt by patiently waiting on the seafloor for its preys, until rapidly accelerating toward them from below (Diamant and Shpigel, 1985). Interestingly, this group of fishes has been witnessed to hunt otherwise. Some of the species among this group have been observed to actuate interspecific interactions with other marine organisms, and in general, interspecific feeding associations are reportedly not uncommon (Strand, 1988). Reef fishes (such as the previously named piscivorous serranids) opportunistically follow other foraging associates, as they can benefit from increased foraging opportunities, success and prey diversity during the course of the interaction (Strand, 1988).
In some cases, these interactions assume the form of a real cooperative hunt with other heterospecific predators (Diamant and Shpigel, 1985; Bshary et al., 2006). Grouper species like Plectropomus pessuliferus marisrubri and coral trout Plectropomus leopardus were studied for cooperative hunting with Octopuses, Moray eels and Napoleon wrasses (Diamant and Shpigel, 1985; Bshary et al., 2006; Vail et al., 2013). Cooperative hunting between Groupers and Moray eels in well established in nature and recognized in literature: This particular behaviour allows the Grouper to benefit from the escaping fishes that are busted out from corals by the Moray partner, which is particularly more apt to invade the coral crevices and holes that are sheltering small preys, thanks to its sinuous body. Such temporary cooperative feeding association created consequently increase the foraging success and decrease in vulnerability to predators of both partners (Diamant and Shpigel, 1985). It is interesting to note that a cooperative hunting association between a Grouper and Moray eel is usually initiated by the former, which approach the Moray and perform a clearly visible signal consisting of head shaking movements, body shaking and pointing to the target (Bshary et al., 2006; Vail et al., 2013; Vail et al., 2014).
During our marine biology excursion in the Ras Muhammad National Park, on the shores of the Red Sea in Egypt, we had the opportunity to make an observational study on wild Lunartail groupers (Variola louti), a serranid carnivorous grouper present on site (Harmelin-Vivien and Bouchon, 1976). More precisely, we had the occasion to collect data on their ability to create interspecific cleaning associations with Cleaner wrasses (Labroides dimidiatus) and cooperative hunting associations with Gray moray eels (Gymnothorax griseus) and Octopuses. The goal of the study, presented in this paper, is to examine the diurnal and crepuscular activity patterns of the Lunartail grouper on the Egyptian shores of the Red Sea, to answer the question of when Lunartail groupers are more occurring to engage in interspecific cleaning or foraging associations.
In general, patterns of fish activity are influenced by daylight cycle and illumination, and more specifically, patterns of a predator behaviour are strongly influenced by the activity patterns of their preys (Pitcher, 1986). Consequently, in the optic of determining the timing of establishment of associations between fishes, it should be plausible to assume that their creation depend primarily on the activity patterns of both associates and ultimately to the activity patterns of their shared preys, if we are speaking about feeding associations between predators. Serranid groupers show a variety of daily activity patterns and appear to be quite flexible about them, with species actives at different times of the day (day, night, or crepuscular times) (Pitcher, 1986). On the other hand, Cleaner fish activity seems to be restricted to daylight (Pitcher, 1986). Finally, Moray eels rarely leave their shelters in the corals during diurnal hours and become more active in hunting starting from dusk and during the night (Diamant and Shpigel, 1985). Moreover, as sun sets behind the horizon and daylight let gradually place to obscurity, a sequence of events take place in the reef that can be summarized by the “changeover”, or evacuation of the water column from diurnal fishes (which seek shelter in corals) and by the emergence of nocturnal predators (Pitcher, 1986).
Our hypothesis is that the particular time of the day and size of the Lunartail grouper have an influence on the occurrence of foraging associations (and more precisely, cooperative hunting with other predators) or cleaning associations with Cleaner wrasses (Labroides dimidiatus) respectively. As the activity patterns of the associated predators and the cleaners do not overlap, we predict the Lunartail groupers to be at rest during the day, spending their time quietly floating around cleaning stations and being cleaned during the brightest moments of the day (especially noon), and to be more active during crepuscular hours such as dawn and dusk. During dusk, we predict groupers to initiate more frequently feeding associations with other predator species and cooperatively hunt with them. Moreover, frequency of both cleaning and feeding associations should increase proportionately with the Lunartail grouper size, as larger groupers should need more cleaning services in function of their size and should be less able to hunt preys in small crevices and coral holes.
Methods
Study area and time of the study
We conducted our study in the core of Ras Muhammad National Park, located on the southern point of the Sinai Peninsula at about 18 km South-West of the Egyptian city of Sharm El Sheikh. The area, on the northern coastline of the Red Sea, is well known among tourists, divers and scientists for its crystal clear waters, its patchy coral reef structure and the presence of numerous reef species of fishes, invertebrates and other marine organisms. In the purpose of the study, we conducted multiple daily snorkeling swims along the 1.15 km of coast around our base camp on the beach, during the week between the 13th and the 20th of April 2018.
Observation and data collection
Observers entered in the seawaters from the shore three times per day, to snorkeling along the shore and conduct direct observations of Lunartail groupers behaviour. The first period of observation of the day was the morning (between 6h00 and 8h00), the second was at noon (between 11h00 and 13h00) and the last one was in the evening (between 16h00 and 18h00). Once an observer found a free roaming Lunartail grouper, the former started following the latter for the duration of 1 hour, collecting data of its behaviour during the observation period. Consequently, each observer had to find and observe a single Lunartail grouper for 1 hour, three times a day.
During the surveillance of a single Lunartail grouper individual, each observer classified the exact timing (precision in seconds) and nature of its activities by filling in a pre-prepared ethogram on a scuba dive slate (activities are specified in Table 1). These observations were sufficient to accurately map the entire activity of the fish during the observation period for further analyses, namely the extrapolation of the time spent with a Cleaner wrasse, the time spent alone, or the time spent during a temporary association such as cooperative hunting with other species.
​
​
​
​
​
​
​
​
​
​
​
​
​
​
​
Finally, each observer noted the approximate size in cm (from head to the extent of the caudal fin) of every observed fish. Sizes were visually estimated on place, after a first day of training which granted each observer to be able to correctly estimate the size of a fish from different distances, with an error of less than the required minimum approximation of ten centimeters. This was done in order to avoid pseudoreplication and consider all the observations as independent data. For future studies, would be better to mark each individual and their territory in order to have a more reliable way of recognizing each subject.
Statistical analysis
All of the statistics were run on R software (version 3.5.2). Unfortunately, due to the low number of replicates and the short time of interactions recorded (especially the cooperative hunting) we have not been able to use the entirety of our data. Consequently, we summarized the timing data collected and created two datasets to test the hypothesis that the two factors of different time of the day (morning, noon, evening) and the size of the fish have an effect on the occurrence of one of the two respective cooperative behaviours of the Lunartail grouper considered. The first behaviour is being cleaned by Cleaner wrasses and the second is the establishment of a temporary association with another predator.
The two datasets are binomial, with response “yes” or “no” depending if the interaction occurred or not during the observed period. In order to analyze the data we used a Bayesian Generalized Linear Model as the data showed some periods with no response for a given behaviour (e.g. Noon had no sight of associative behaviour), thus impeding normal GLM analysis.
Results
Number of replicates and total time of observation
By the end of the study, 23 Lunartail groupers have been observed for a total observation time of 23 hours of observation.
Influence of the time of the day
The results confirm the hypothesis that the time of the day has an influence on both cooperative behaviours exhibited by the Lunartail grouper (see Figure 7 and Figure 8). More precisely, the period of the day influences both the occurrence of cooperative hunting (p–value: 0.010) and cleaning behaviour (p–value: 0.002). The number of cooperative hunting interactions was found to differ between noon and evening (p–value: 0.0284), with 5 observations on 9 replicates for the evening against 0 observations on 9 replicates during noon. Morning does not show a significant difference with either the noon or the evening period, but it is still possible to foresee a trend for morning cooperative hunting with 2 observation on 5 replicates.
For the cleaning behaviour, no significant p-values were found to assess a difference of occurrence between the morning, noon and the evening, probably due to the low number of replicates. Anyway, it is still possible to foresee a trend as in the morning there were no observation of cleaning on 5 replicates, against 8 observation on 9 replicates for the noon period and 5 observation on 9 replicates for the evening period.
Influence of the size of the fish
Regarding the size of the fish, no significant difference was found on cooperative behaviours of hunt and cleaning, probably because of the low number of replicates and consequently of different sizes recorded. Anyway, a trend seems to be apparent for both the cooperative hunting and the cleaning, as bigger fishes seem to have more interspecific relations (see Figure 7 and Figure 8).
Discussion
Heterospecific associations observed
Our field observations confirm that the Lunartail grouper (Variola louti) of the Red Sea is able to initiate interspecific cooperative hunting with Gray moray eels (Gymnothorax griseus), in a similar fashion described for their related species worldwide. The interspecific signalling between groupers and its associates described in various papers (Bshary et al., 2006; Vail et al., 2013; Vail et al., 2014) has also been frequently observed between the Lunartail grouper and Gray moray eels, with the same shaking of the entire body and head. Interestingly the grouper was also seen once cooperating with a Giant Moray eel (Gymnothorax javanicus). Feeding associations of a seemingly more opportunistic nature with octopuses have been recorded as well. Lunartail groupers have also been observed to profit from the cleaning service offered by Cleaner wrasses (Labroides dimidiatus), as expected.
Role of the time of the day
Results support the hypothesis that cooperative hunting and cleaning occurrence is dependent from the time of the day. Speaking about predation, the highest number of observations of both cooperative hunting and simple opportunistic feeding associations were recorded during the evening period. This is in accord with the literature and with our predictions: Lunartail groupers usually show a higher hunting activity during the crepuscule (Harmelin-Vivien and Bouchon, 1976). The occurrence of cooperative hunting between groupers and Gray moray eels during the evening is only possible thanks to the emergence of the latter, which are mainly nocturnal predators (Diamant and Shpigel, 1985). Conversely, no cooperative hunting was detected during the daytime, as observers spotted no Gray moray eel during snorkeling swims, probably because of the fact that Gray moray eels rarely exit their diurnal retreats (Diamant and Shpigel, 1985). From the total of 7 cooperative hunting observations reported, only 2 were in early morning. This trend is also in accord with the general definition of “crepuscule” period, which include both moments of dusk and dawn. The two periods, in fact, share the same light conditions and are respectively the opening and closing acts of the reef “changeover”, where predatory activities of the night respectively increase and decrease rapidly (Pitcher, 1986). Interestingly, these dynamics appear not to be limited to the heterospecific combination of Lunartail grouper and Gray moray eel, as the former have also been frequently observed in company of octopuses during sunsets.
Role of the size of the grouper
Size of fishes in correlation to frequency of both cleaning and hunting associations seems to delineate a trend. Larger fishes appear to exhibit increased frequency of interspecific relations than smaller ones. This is at least apparently in accord with the initial predictions, for which fishes of larger size need an increased amount of cleaning services and at the same time, suffer more from the lack of the ability to hunt for small preys hidden in coral crevices and need a hunting associate to compensate for their size. Unfortunately, the number of replicates obtained is insufficient to draw actual conclusions, so these explanations are to be considered mere speculations until supported by significant data.
Insufficient replicates only reveal trends
Unfortunately, we collected insufficient replicates to draw strong conclusions about the occurrence of intraspecific interactions, especially for the case of cleaning interactions. Replicates were also insufficient to estimate an eventual correlation between interspecific interactions and size of the grouper. In any case, for these cases it was possible to foresee several trends that reinforce our first predictions: Lunartail groupers appear to prefer to benefit from cleaning interaction mainly at noon, and size seems to be positively correlated with the frequency of interspecific interactions.
The low number of replicates are due to the fact that the time period was short. In some occasion the observers were not able to find a subject, or the latter interrupted the eye contact too soon usually by swimming into the blue.
Implications of interspecific interactions in the ecosystem
Even if accessing limited data to strongly demonstrate our hypothesis, our personal observations lead us to suppose that interspecific interactions, and especially the two considered during this study (cleaning and cooperative hunting), have a large impact on the marine ecosystem. Literature presents studies on multispecies foraging associations and how these binomial interactions influence the rest of species present in the coral reefs (Lukoschek and McCormick, 2000). Like other groupers (i.e. species of genus Plectropomus), Lunartail Groupers could suffer a drop in the population over time, in Egypt and elsewhere, due to overfishing (Frisch et al., 2016). With a good management of fisheries, mainly in collaboration with traditional local fishermen, it’s possible to establish no-fishing zones where groupers are able to survive and reproduce (Galal et al., 2002) and in this case initiate interspecific associations that influence their partners and ultimately the entire ecosystem. In this optic, an optimized version of our study should be able to find more information about the timing, nature and composition of different interspecific interactions and to re-evaluate their importance in the trophic chains of the marine ecosystem. The knowledge gained about the timing of the different intraspecific activities performed by groupers during the arc of 24 hours could allow a better management of fishing laws and also to re-evaluate the real implications of a possible disappearance of a predator and the interaction that it creates with his partners.
A week was a very small period to collect information, but with a project structured on several month of data collection it should be probable to have more interesting results and possibly confirm our initial hypothesis. In addition, methods need to be improved, for example by delimiting areas of patrolling for the different observers and if possible, by marking individual groupers to maximizing the pseudo-replication avoidance. Furthermore, this study was all made by snorkeling. Scuba diving would be much more effective especially for filming the interactions as the depth and the low visibility due to the dusk time impaired the possibility to have a decent video.
In conclusion, even with our low number of replicates we have been able to spot, especially the cooperative hunting behavior, 7 associations. Thus, this interspecific collaboration may be a lot more frequent than expected. Making even more important to conserve the diversity of the reef, as the demise of one of the actors could impair a bigger ecological relationship bringing it to collapse.
Acknowledgements
We thank Prof. Redouan Bshary, Dominique Roche and Triki Zegni for the on-site supervision in Egypt. We would also like to thank Radu Slobodeanu for the precious statistical advising.
References
-
Diamant A., Shpigel M. (1985). Interspecific feeding associations of groupers (Teleostei: Serranidae) with octopuses and moray eels in the Gulf of Eilat (Agaba). Environ. Biol. Fishes (13): 153–159.
-
Strand S. (1988). Following Behavior: Interspecific Foraging Associations among Gulf of California Reef Fishes. Copeia (2): 351–357
-
Bshary R., Hohner A., Ait-el-Djoudi K., Fricke H. (2006). Interspecific Communicative and Coordinated Hunting between Groupers and Giant Moray Eels in the Red Sea. PLoS Biol. (4): 431
-
Vail A. L., Manica A., Bshary R. (2013). Referential gestures in fish collaborative hunting. Nat. Commun. (4)
-
Vail A. L., Manica A., Bshary R. (2014). Fish choose appropriately when and with whom to collaborate. Curr. Biol. (24): 791–793
-
Harmelin-Vivien M. L., Bouchon C. (1976). Feeding behavior of some carnivorous fishes (Serranidae and Scorpaenidae) from Tuléar (Madagascar). Mar. Biol. (37): 329–340
-
Pitcher T. J. (1986). The behaviour of Teleost fishes. Springer US.
-
Lukoschek V., McCormick M. I. (2000). A review of multi-species foraging associations in fishes and their ecological significance. Proceedings of the 9th International Coral Reef Symposium (1): 467–474
-
Frisch A. J., Cameron D. S., Pratchett M. S., Williamson D. H., Williams A. J., Reynolds A. D., Hoey A. S., Rizzari J. R., Evans L., Kerrigan B., Muldoon G., Welch D. J., Hobbs J.-P. A. (2016). Key aspects of the biology, fisheries and management of Coral grouper. Rev. Fish Biol. Fish. (26): 303–325
-
Galal N., Ormond R. F. G., Hassan O. (2002). Effect of a network of no-take reserves in increasing catch per unit effort and stocks of exploited reef fish at Nabq, South Sinai, Egypt. Marine and Freshwater Research (53): 199–205
Author contributions
M.B., P.N., and P.S. designed the study, performed the observation and data collection and wrote the manuscript. M.B. did the statistical analyses.
Data accessibility
Data are currently available only to private access of the authors.
Funding
This work was supported by private funding and by the University of Neuchâtel.
Competing interests
The authors declare no conflict of interest.
Copyright
© 2019 All rights reserved to the authors. Any use of this material without permission is prohibited.