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Cleaner fish–client interactions in Ras Mohamed National Park, Egypt; a comparison to Lizard Island, Australia

Staubli Virginie, Porta Sophie, Niklaus Simon

INTRODUCTION

In nature, there are many social relationships between different species. A particular fish has specially attracted the attention of biologists: the bluestreak cleaner wrasse, Labroides dimidiatus (Figure 1), is part of a key mutualistic relationship in coral reef ecology (Bshary 2003; Grutter et al. 2003). Cleaner fishes occupy small territories (so-called “cleaning stations”) in which they interact with a variety of reef fish species (so-called “clients”). Cleaners can cooperate by removing ectoparasites from client fishes, but can also cheat by feeding on the mucus and scales of their client fishes (Randall 1958 and Grutter 1997).

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Cleaners adjust levels of cooperation in function of the options they have; visiting clients that have access to other cleaning stations (so-called “visitors”) receive faster service than clients that must wait for inspection because they only have access to one cleaning station (so-called “residents”)(Bshary 2001). As cleaners have more than 2000 interactions per day with a great variety of client fishes and are fully dependent on cleaning for their diet (Grutter 1995), their performance during the interactions have thus a major impact on their fitness (Salwiczek et al. 2012).

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Therefore, the aim of this project is to quantify and analyse cleaner fish-client interactions in Ras Mohamed National Park in Egypt, and to compare our results with data collected on Lizard Island in Australia. Our project is divided into two parts; first, the analysis of the data collected in Egypt, and secondly, a comparison with data collected in Australia.

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Our analysis will focus on the interaction time between a cleaner fish and a client, the number of interactions over a time unit, and the time percentage a cleaner spends interacting over a time unit.

 

We suppose that we will find differences between countries, but also between the different Australian sites, as environment may varies between these areas.

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Figure 1 : Labroides dimidiatus, part of the Labridae family. Picture in Ras Mohammed National Park, Sharm el Sheikh, Egypt.

Photo by Staubli Virginie.

MATERIAL AND METHODS

Site and subject

Data from Egypt were collected between April 15th and April 19th of year 2018 in Ras Mohamed National Park, Egypt (Figure 2). Twelve different cleaning-stations (Figure 3) were chosen to avoid recording the same individual multiple times and thus avoid pseudo-replication. In shallow water, the study area consists of small reef patches that are isolated from each other by sandy areas. Before starting to record data, cleaning stations of Labroides dimidiatus were localized and marked by colored rocks to facilitate the identification of the cleaning stations. All colored rocks were removed once the experiences finished.

Data collection

Videos were collected either by snorkeling or diving using Canon G15 and G16 in different cleaning-stations. Natural cleaning interactions were filmed for 30 minutes between 7 a.m. and 5 p.m. (Figure 5a to 5e). Twelve adult cleaners were randomly selected and when in couple, we tried to identify and only follow the female cleaner wrasse (generally the smallest individual). Divers and snorkelers kept an approximate distance of 2 meters during filming.

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We considered an interaction as soon as the cleaner followed a client for at least one second, and the end of an interaction as soon as the cleaner leaved the client. We considered a new interaction if the cleaner switched to another client but came back to a previous client.

Data extraction

For each cleaner fish, we analysed the number of interactions by time unit (30 minutes), the number of interactions with large clients by time unit, the mean duration of interactions and the percentage of time cleaners spent interacting over 30 minutes.

All videos were randomly analysed by one of us. From each video, we extracted for each cleaner-client interaction the client species, family, the maximal size of the species and the duration of the interaction.

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Species, family and the maximal specie’s size were identified using the guide book Red Sea reef guide, 2000, Helmut Debelius. Client fishes’ sizes were divided into two categories: large (L) and small (S). According to Triki et al. (2018), large fish are considered having a body size > 10 cm and small fish a body size ≤ 10 cm.

Statistical analysis

Data were analysed using the software RStudio v1.0.143. Regarding the data collected in Egypt, we first investigated the mean interaction time and the interaction number in function of the cleaner fish over 30 minutes; we ran a linear model to analyse the interaction time and a generalized linear models (GLM) with a quasi-poisson distribution to model the interaction number in function of the cleaner’s ID.

Then, we ran a third model, also linear, to investigate if the cleaner’s ID and the client’s species had any effect on the interaction time. Finaly, we split the client fish species into two groups in function of their size; according to the Red Sea reef guide, client’s species were considered as Large (L) when > 10 cm and Small (S) when ≤ 10 cm, and analysed using a linear model if the client’s size had any effect on the interaction time with the cleaner.

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In a second time, we compared data from Egypt with previous data collected in Australia. We ran a generalized linear model (GLM) with quasi-poisson error to compare the mean interaction number (in 30 minutes) between the different countries and then among the 3 Australian (MB, NHS, BV) (Figure 4) and the Egyptian data-collection-sites.

We then proceeded the same way to compare the mean duration of a cleaner-client interaction, the time proportion cleaners spent interacting during a 30-minute-observation and finally the proportion of interactions with large clients (L).

RESULTS

Egypt

Analysis of data collected in Egypt showed that the cleaner’s ID (n=12) had a significant effect on the mean interaction time (p-value = 0.000722). The cleaner’s ID also had a significant effect on the interaction number over 30 minutes (p-value = 0.000345). Both the cleaner’s ID and the client’s species had an effect on the mean interaction time (p-value=7.57e-05, p-value=2.2e-16). However, there was no significant interaction between the cleaner’s ID and the client’s species. Finally, results also demonstrated that the client’s size (large or small) also significantly impacted the interaction time (p-value=1.22e-08) (Figure 6).

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Figure 6: Boxplot representing the interaction time [seconds] with Large (L) or small (S) client fish in Sharm el Sheikh (SH_2018), Egypt. There is a statistically significant difference between large and small client fish

(p-value = 1.22e-08).

Egypt vs. Australia

Comparison with data collected in Australia showed that there is a significant difference in the mean interaction time between the two countries (p-value= 0.0118) (Figure 7). There is also a significant difference between some sites: between SH_2018 (mean = 7.39 seconds) and MC_2011 (mean = 4.08 seconds) (p-value = 0.0002), and between NHS_2014 (mean = 6.38 seconds) and MC_2011 (p-value = 0.023) (Figure 8).

However, results showed no significant difference in the interaction number in 30 minutes between cleaners from Australia and from Egypt, neither between the different Australian sites. Analysis of the amount of time the cleaners spent interacting in 30 minutes showed no difference between both countries (p-value= 0.793) neither between sites. Finally, we observed no difference in the proportion of interactions with large clients between countries (p-value= 0.462) and between sites.

DISCUSSION

Egypt

We found that the mean interaction time and interaction number varied between the cleaner-fishes. Indeed, according to the Egypt’s data, some cleaner fishes spent more time interacting with their clients than other cleaners. This could be explained by the presence of bystander client reef fish (Pinto, Ana et al. 2011); a cleaner fish increases its current levels of cooperation and interaction when a bystander client fish is present (Pinto, Ana et al. 2011). Indeed, during data collection we could not control any factors such as the presence of other clients species or other animal species during the interaction between a cleaner and client fish, which could have disrupted the current interaction.

 

According to previous observations (Colosio et al. 2015 and Delisle et al. 2016, all unpublished data, Egypt excursion), the presence of observers can affect species’ and families’ diversity around the cleaning-station, which could explain the significant effect of client’s species and the cleaner’s ID on the interaction time. Furthermore, according to Titus et al. 2015, the presence of SCUBA divers can negatively impact natural ecosystems, for example by depressing cleaning rates.

 

Another explanation for the variation between cleaner fishes and the interaction time could be explained by the fact that the pairs of cleaner (a couple of Labroides dimidiatus) prolong the interaction duration with their client fish (Gingins et al. 2014). During our observations, we followed several cleaning stations with couples of L. dimidiatus and only some of them had a single cleaner fish in the territory; this could potentially have influenced the interaction time between the different cleaners (n=12), but other statistical analysis would be needed to verify this hypothesis in Egypt.

 

Finaly, the significant differences in the mean interaction time between cleaner-fishes may be also due to individual variations between cleaners.  Another explanation would be that our sampling was carried out within 30 consecutive minutes, which may be poorly representative of a cleaner’s daily activity.  

 

We also assume that the cleaner individual differences in the mean interaction time potentially be due to different reef environments where the cleaning-stations were located. Indeed, according to Wismer et al. (2014), cleaner fishes from continuous reefs have significantly more interactions than cleaners from patch reefs. Reef environments were not taken into account in our analysis. Indeed, some cleaning-stations that we sampled were isolated from other reefs while others were closer to other reefs.

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The model analyzing the effect of client’s species and the cleaner’s ID on the interaction time revealed that both factors had a significant effect on the interaction time. According to S. Tebbich et al. (2002), Labroides dimidiatus and the client reef fish build up their relationship. S. Tebbich found that cleaner fishes spend more time near  the familiar than the unfamiliar clients. This could explain the significant effect of client species on the interaction time in function of cleaner’s ID.

 

We also found that the client size can significantly affect the interaction time with cleaner fish. Indeed, our Egypt’s data demonstrated that large clients have a longer interaction time with cleaner than small client fishes. Previous researches demonstrated that the frequency and duration of inspection were positively correlated with the mean parasite load and mean surface area of different fish species (Grutter 1995). Larger fish, which have more parasites, were inspected more often and for a longer duration than smaller fish with fewer parasites. Moreover, the average ectoparasite load of some hosts has been shown to be species-specific (Grutter 1994), and cleaner fishes prefer host species with more ectoparasites (Gorlick 1984) or with more mucus (Gorlick 1978). Parasites and surface area play an important role in fish cleaning interactions. Because size and parasite load are closely related, cleaner fish may use size as an indicator of food availability (Grutter 1995).

Egypt vs. Australia

We found that the mean interaction time was significantly different between both countries. This could be explained by the fact that Australian reefs may have experienced greater environmental disturbances. Triki et al. (2018) found that reef fishes and cleaner fishes abundance declined after environmental perturbations such as a cyclone or coral bleaching, which could have influenced cleaner fish-client interactions. It would be interesting to provide further research on the history of Red Sea disturbances.

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The differences observed between the different Australian sites MC_2011 and NHS_2014 (Figure 8) can also partially be explained by the same reasons as those described in Egypt.

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Finaly, the interaction number, the time spent interacting and the percentage of interaction with large clients by time unit do not significantly differ nor between countries (Australia and Egypt) neither between the different sites (Big Vicky’s 2014, Mermaid 2011, North horse shoe 2014 and Sharm el Sheikh 2018). We suppose that these Australian and Egyptian reefs are probably similar and do not truly differ in ecosystems. Therefore, there is probably not much difference between client species from Australia and from Egypt.

AKNOWLEDGEMENTS

We kindly thank the staff of Ras Mohammed National Park for their welcome and devotion. We also thank our diving instructor Kathi and the diving center i-Dive Dahab for the rental of diving equipment. We sincerely thank Zegni Triki for access to her data from Australia and without whom the execution of this project would not have been possible. We also truly thank our professors Redouan Bshary and Dominique Roche for their help and support.

REFERENCES

  1. Bshary, Redouan. "The cleaner fish market." Economics in nature (2001): 146-172.

  2. Bshary, Redouan. "The cleaner wrasse, Labroides dimidiatus, is a key organism for reef fish diversity at Ras Mohammed National Park, Egypt." Journal of Animal Ecology 72.1 (2003): 169-176.

  3. Colosio, S., Demairé, C. and Quattrini, F. (2015). Impact of observers on fish diversity and size at common cleaner wrasse (Labroides dimidiatus) cleaning stations. On: http://marine-bio.wixsite.com/egypt-field-course/project-2. Consulted on January 14th 2019.

  4. Delisle, L., Levorato E. and McNeely William (2016). Does the presence of divers have an effect on diversity, abundance and size of clients at cleaner wrasse (Labroides dimidiatus) cleaning stations? On: http://marine-bio.wixsite.com/egypt-field-course/project-4. Consulted on January 14th 2019.

  5. Gingins, Simon, and Redouan Bshary. "Pairs of cleaner fish prolong interaction duration with client reef fish by increasing service quality."  26.2 (2014): 350-358.

  6. Gorlick, Dennis L. "Preference for ectoparasite-infected host fishes by the Hawaiian cleaning wrasse, Labroides phthirophagus (Labridae)." (1984): 758-762.

  7. Gorlick, Dennis L. . Diss. University of Hawaii at Manoa, 1978.

  8. Grutter, Alexandra S. "Relationship between cleaning rates and ectoparasite loads in coral reef fishes." 118 (1995): 51-58.

  9. Grutter, Alexandra S. "Relationship between cleaning rates and ectoparasite loads in coral reef fishes." Marine Ecology Progress Series 118 (1995): 51-58.

  10. Grutter, Alexandra S. "Spatial and temporal variations of the ectoparasites of seven reef fish species from Lizard Island and Heron Island, Australia." 115 (1994): 21-30.

  11. Grutter, Alexandra S., and Redouan Bshary. "Cleaner wrasse prefer client mucus: support for partner control mechanisms in cleaning interactions." Proceedings of the Royal Society of London B: Biological Sciences 270.Suppl 2 (2003): S242-S244.

  12. Pinto, Ana, et al. "Cleaner wrasses Labroides dimidiatus are more cooperative in the presence of an audience." Current Biology 21.13 (2011): 1140-1144.

  13. Randall, John E. "A review of the labrid fish genus Labroides, with descriptions of two new species and notes on ecology." (1958).

  14. Salwiczek, Lucie H., et al. "Adult cleaner wrasse outperform capuchin monkeys, chimpanzees and orang-utans in a complex foraging task derived from cleaner–client reef fish cooperation." PLoS One 7.11 (2012): e49068.

  15. Slobodkin, Lawrence B., and Lev Fishelson. "The effect of the cleaner-fish Labroides dimidiatus on the point diversity of fishes on the reef front at Eilat." The American Naturalist 108.961 (1974): 369-376.

  16. Soares, Marta C., et al. "Tactile stimulation lowers stress in fish." Nature Communications 2 (2011): 534.

  17. Titus, Benjamin M., Marymegan Daly, and Dan A. Exton. "Do reef fish habituate to diver presence? Evidence from two reef sites with contrasting historical levels of SCUBA intensity in the Bay Islands, Honduras." PLoS One 10.3 (2015): e0119645.

  18. Triki, Zegni, et al. "A decrease in the abundance and strategic sophistication of cleaner fish after environmental perturbations." Global change biology 24.1 (2018): 481-489.

  19. Wismer, Sharon, et al. "Variation in cleaner wrasse cooperation and cognition: influence of the developmental environment?." Ethology 120.6 (2014): 519-531.

Book reference : Red Sea reef guide, 2000, Helmut Debelius

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