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Figures Abstract Outbreaks of the corallivorous crown-of-thorns seastar Acanthaster planci COTS represent one of the greatest disturbances to coral reef ecosystems in the Indo-Pacific, affecting not only coral reefs but also the coastal communities which rely on their resources.

While injection approaches are increasingly used in an attempt to control COTS densities, most of them display severe drawbacks including logistical challenges, high residual environmental impacts or low cost-effectiveness. We investigated the lethal doses, intra- and inter-specific disease transmission and immune responses of COTS when injected with fresh lime juice extracted from local Citrus arantifolia and white spirit vinegar.

High COTS mortality was achieved with small volumes: Multiple immune measures suggested that death was very likely caused by pH stress from the acidic solutions rather than a bacterial infection.

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Contagion to either conspecifics or a variety of other reef species was not observed, even at COTS densities 15 times higher than the highest naturally reported. We conclude that injections of lime juice and vinegar offer great advantages when compared to current best practises and constitute a cheap and natural option for all reefs affected by COTS.

May 25, ; Accepted: August 19, ; Published: September 10, Copyright: This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Data Availability: All relevant data are within the paper and its Supporting Information files.

This project was funded by grants from the Fisheries Department of Vanuatu www. This was the main grant for this work, which covered fieldwork Vanuatu and functioning costs hatchery and aquaculture facilities, technical staff, laboratory materials of the study. Support was also provided by grants from the Government of New Caledonia www.

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  • The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Support was also provided by grants from the LabEx Corail www. Suzanne Mills in Vanuatu during the project. The authors have declared that no competing interests exist.

    Introduction At low density, the corallivorous crown-of-thorns seastar COTS , Acanthaster planci Linnaeus is an integral part of coral reef ecosystems. Yet, population outbreaks of this species represent the most severe biological disturbance experienced by coral reefs across the Indo-Pacific, from the coast of South Africa to the Gulf of California [ 1 — 5 ]. Outbreaks of COTS cause widespread damage to reef-building corals [ 6 , 7 ] and the cascading effects from coral loss can severely harm the entire coral community [ 8 — 11 ].

    There is historical evidence that coral reefs can recover from COTS outbreaks; however, given the current widespread declines in coral cover, they drive even more pressure on already weakened systems [ 12 — 13 ]. For example, it is predicted that the absence of COTS alone would reverse the currently declining curve of coral cover on the Great Barrier Reef [ 14 ].

    Furthermore, the frequency of COTS outbreaks has been increasing over recent decades [ 15 — 17 ] and the outbreaks themselves are reaching record-breaking levels e. Currently, the impacts of COTS outbreaks can only be limited through direct human intervention. While numerous approaches have been developed over the last few decades see review [ 19 ] , manual collection followed by disposal ashore is the most common technique used across the Pacific.

    It is one of the most robust methods to regulate COTS outbreaks, at least on a small scale [ 20 ].

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    Injection approaches—where COTS are injected with a variety of noxious solutions—are increasingly used, as they are highly cost-effective and fairly safe when handled correctly [ 21 ]. However, they also include drawbacks: Yet, injections with sodium bisulphate are required at such high concentrations that they can lower oxygen levels in seawater [ 25 , 26 ].

    Sodium hypochlorite, ammonium hydroxide, copper sulphate and ammonia were used on the Great Barrier Reef until they were judged potentially toxic to fish and many invertebrates [ 27 , 28 ].

    Other solutions may favour bacterial induction and the growth of a particular type of pathogen [ 29 ]. As a cultural medium for vibrios, thiosulfate—citrate—bile—sucrose agar TCBS was found to induce disease and ultimately death in COTS, but with potential knock-on effects on the coral-associated community [ 30 , 31 ]. Recently, single injections of 10 ml of TCBS protein ingredients oxbile and oxgall induced a strong immune response and death in COTS with no evidence of negative impacts on the coral community, and were considered a promising alternative control method [ 32 ].

    Nevertheless, the costs of the current injection methods are out of the reach for many stakeholders. The price of injections may reach circa 35 USD per seastar e. Even the alternative oxbile and bile salts injection method proposed by Rivera-Posada et al.

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  • In some Pacific countries, the cost of importing g container s of oxbile exceeds USD, freight cost included. Against this backdrop, developing more cost-effective approaches is critical.

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    In this paper we investigate an innovative method of controlling COTS outbreaks with injections of natural acidic solutions: Acetic acid, the active component of white vinegar, has previously been found to be lethal to COTS [ 34 , 35 ].

    However, these findings were based on limited, unrepeated experiments and potential impacts on other organisms via horizontal transmission were not tested. Lime juice extracted from limes, Citrus aurantifolia, contains a high percentage of citric acid and has never been tested on COTS. Both are common, inexpensive acidic agents that can be widely found in the Pacific region and do not require permits or special handling procedures.

    This work was conducted in Vanuatu, a small archipelago in the Western Pacific where the presence of COTS has frequently been reported in recent decades [ 36 — 40 ]. The objectives were to 1 establish the effects of injecting both different acidic solutions and different volumes including single vs. Our ultimate goal is to propose a highly efficient, affordable, and less harmful alternative compared to the control methods currently in use in the Pacific sodium bisulphate, TCBS, oxbile and bile salts.

    Materials and Methods Study location—collection of test specimens Experiments were conducted from February to September at the marine hatchery and aquaculture facilities of the Fisheries Department of Port-Vila, Vanuatu. In the field, COTS were manually collected by snorkelers; specimens damaged during collection were discarded and not used for the experiments. COTS were transported to the marine hatchery in l containers filled with seawater regularly renewed, then maintained in large concrete tanks 5.

    Acidic injection trials Lime juice was extracted from the fruit of Citrus aurantifolia and filtered twice prior to use average pH 1. Aquaria injection trials Eight injection treatments were tested: For lime juice, we tested three different single-shot volumes: Experimental blocks consisted of eight individual aquaria 60 l with constant filtered seawater inflow The specimens of COTS were randomly assigned to either control no injection; three individuals or acidic injection five individuals treatment per trial.

    We carried out four replicate trials for each treatment, such that 32 individuals were used for each of the eight injection treatments, i. Specimens were injected in the arm junction using disposable syringes; for double-shot treatments, injections were performed in two opposite arm junctions.

    Each individual was monitored every 12 h for four days for clinical signs of stress such as mucus production, necrosis and loss of limbs; death was identified by the absence of reaction or movement from the podia [ 18 , 32 ]. Field trials Due to unfavourable field conditions, only one experimental trial was carried out. Experimental blocks consisted of two plastic cages 4 m2, 1 cm mesh size anchored to the reef substrate. COTS were injected and monitored using the same protocol as for the aquaria experiment.

    Contagion trials A contagion experiment was carried out to investigate the presence of intra- and inter-species transmission of disease or other noxious substances linked to our injection method.

    Experimental blocks consisted of 3 large concrete tanks 5. The 30 specimens belonged to phylums Cnidaria, Echinodermata, Mollusca and Chordata Table 1 and had been collected from a healthy, shallow fringing reef located near the marine hatchery. Coral samples were placed in cages in order to prevent direct feeding injuries from COTS.

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  • Three temporal contagion trials were performed: The injection volume was chosen in order to avoid massive COTS mortality at the beginning of the trial so that we would be able to investigate the long-term effects of contagion. The trials ran for seven days after injection; specimens were monitored every 12h using the same protocol as for the aquaria experiment.

    An additional control trial where none of the six COTS were injected was simultaneously carried out.

    Field trials Due to unfavourable field conditions, only one experimental trial was carried out. Three temporal contagion trials were performed:

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