Fig 4. Individual Pseudanthias squamipinnis (7.3 ± 0.8 g) 30 h following the introduction of 15 Neobenedenia sp. oncomiracidia.
Photos are of left and right lateral sides of two representative fish from the experimental treatment, with shrimp (a-d), and the control, without shrimp (e-h). Image courtesy PLOS ONE
doi:10.1371/journal.pone.0117723.g004
Where pesticidal chemicals often fail or prove deadly to many organisms in reef aquaria, the common Scarlet Skunk Cleaner Shrimp, Lysmata amboinensis, has been found to be a highly effective biocontrol against all live stages of ectoparasites that kill and disfigure fishes in captive systems. The shrimp were found to have diminished the population of harmful parasites by half in experimental aquaria, and the fish emerging from systems with and without Scarlet Skunk Cleaner Shrimp present showed marked differences in their physical condition and apparent level of health.
The research may provide new stimulus in the aquarium trade for using cleaner shrimp as effective parasite guards in holding and quarantine systems, as well as in display aquaria.
What are the best methods of preventing losses of valuable marine livestock in captive systems? The authors noted that cleaner fish species have been used in salmon aquaculture but questioned the potential for this in marine ornamental systems. The latest research on cleaner shrimp (Lysmata amboinensis) conducted by researchers Thane A. Militz and Kate S. Hutson at James Cook University in Queensland, Australia, adds some tantalizing new evidence to ongoing debates about what methods work best for stopping ectoparasite losses in the aquarium trade.
Cleaner shrimp are well known to engage symbiotic cleaning services by removing ectoparasites from the bodies of “client” fishes on the reef and in captive systems. The researchers discovered that the shrimp also helped police the aquarium systems in which they were kept, consuming both eggs and larvae of a well-known noxious fluke that attacks fishes such as the Lyretail Anthias shown. The study also shows parasites are much less successful in infecting anthias in aquaria that contain cleaner shrimp compared to aquaria without cleaner shrimp.
A commentator for the Marine Aquarium Trade Research from Papua New Guinea has promoted the news to the aquarium hobby, saying: “Having a cleaner shrimp in your tank is almost the equivalent of having a doctor and home pest-exterminator for your home aquaria! You can check out the research, freely available to the public, here: http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0117723 (See also Marine Aquarium Trade Research: PNG on Facebook.)
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Abstract from PLOS ONE
Cleaner organisms exhibit a remarkable natural behaviour where they consume ectoparasites attached to “client” organisms. While this behaviour can be utilized as a natural method of parasitic disease control (or biocontrol), it is not known whether cleaner organisms can also limit reinfection from parasite eggs and larvae within the environment. Here we show that cleaner shrimp, Lysmata amboinensis, consume eggs and larvae of a harmful monogenean parasite, Neobenedenia sp., in aquaculture. Shrimp consumed parasite eggs under diurnal (63%) and nocturnal (14%) conditions as well as infectious larvae (oncomiracidia) diurnally (26%). Furthermore, we trialled the inclusion of cleaner shrimp for preventative parasite management of ornamental fish, Pseudanthias squamipinnis, and found shrimp reduced oncomiracidia infection success of host fish by half compared to controls (held without shrimp). Fish held without cleaner shrimp exhibited pigmentation changes as a result of infection, possibly indicative of a stress response. These results provide the first empirical evidence that cleaner organisms reduce parasite loads in the environment through non-symbiotic cleaning activities. Our research findings have relevance to aquaculture and the marine ornamental trade, where cleaner shrimp could be applied for prophylaxis and control of ectoparasite infections.
Introduction
Parasitism has long been considered the most common lifestyle on earth with virtually all living organisms serving as potential hosts [1,2]. Parasites permeate all ecosystems and trophic levels and the aquaculture environment (inclusive of aquatic holding systems) is no exception. Manipulation of several biotic and abiotic factors in aquaculture, such as food availability, population density, water quality parameters, physical handling and the absence of predation, offsets the natural ecosystem balance [3–5]. This manipulation often favours proliferation of parasites with direct life cycles, as stressors may interact with parasites, their hosts, and the host—parasite relationship in myriad ways [6,7]. Aquaculture remains the fastest primary growth industry in the world but is heavily burdened by parasitic outbreaks [8]. The complications and ramifications of traditional chemical treatments have led industry to seek natural alternatives to parasite management. Biocontrols have been proposed as a natural means to restore ecosystem balance in aquaculture and reduce parasite intensities, most often in the form of ‘cleaner’ organisms. A diversity of aquatic organisms have been identified to engage in cleaning activities [9], with cleaner fish and shrimp proving most feasible for cohabitation with aquaculture stock.
Research efforts assessing the application of cleaner organisms in aquaculture have focused exclusively on host-cleaner symbioses for removal of host-attached parasite life stages. Secondary benefits of cleaner organisms extending beyond host-attached parasite removal have been demonstrated (cleaner fish remove fouling organisms from salmon cages [10,11]) but never extended to the possibility of non-symbiotic parasite removal. However, eggs and larval stages of parasites often persist within the culture environment and may render ‘clean’ fish immediately susceptible to reinfection [12,13]. In the case of the cleaner wrasse, Labroides dimidiatus, the nocturnal suspension of cleaning behaviour has been demonstrated to result in a resurgence of parasite abundance in natural systems that undermine daily cleaning efforts [12]. This phenomenon is a principle problem behind reactive disease treatments targeting a single life stage of the infectious agent and could undermine the effectiveness of cleaner biocontrols in the culture environment. Consequently, assessing the extent to which cleaner organisms engage in environmental, or non-symbiotic, ‘cleaning’ is highly advantageous.
This paper aims to demonstrate that the beneficial services of cleaner organisms extend beyond symbiosis to include removal of all off-host life stages of a marine monogenean parasite. We assessed the capacity for the cleaner shrimp, Lysmata amboinensis, to engage in non-symbiotic cleaning behaviours under diurnal and nocturnal conditions. The impact cleaner shrimp have on infection success of a potential host fish was also evaluated.
Conclusions
The success of temperate aquatic biocontrols (i.e. cleaner fish in salmon culture [10,11,44]) employed for their symbiotic cleaning services demonstrates the potential for cleaner organisms in tropical aquaculture. However, the application of tropical cleaner fish is limited by nightly suspension of cleaning activities [32,33] and the capacity for parasite eggs and larvae in the culture environment to reinfect host fish [12]. Furthermore, problems with using cleaner fish to treat client fish in aquaculture are already being realised through the potential for disease transfer from cleaner fish to clients [45]. By use of a crustacean cleaner the evolutionary distance between cleaner and client is greatly increased thereby limiting capacity for disease transfer. Here we show that the cleaner shrimp, Lysmata amboinensis, consumed all off-host life stages of a monogenean parasite of significant concern to aquaculture, cleaned under nocturnal conditions, and reduced infection success on host fish. The closed experimental aquaria utilized in this study mimic aquaculture systems commonly employed in the live fish and aquarium trade which can enable immediate application of these research findings. Discovery of this cleaner organism’s role in environmental pest-control greatly expands the potential efficacy of cleaner shrimp as biocontrols in food producing sectors and warrants further investigation into other secondary benefits of cleaner organisms.
Reference:
Militz TA, Hutson KS (2015) Beyond Symbiosis: Cleaner Shrimp Clean Up in Culture. PLoS ONE 10(2): e0117723. doi:10.1371/journal.pone.0117723
