Western Indian Ocean JOURNAL OF Marine Science Volume 18 | Issue 2 | Jul – Dec 2019 | ISSN: 0856-860X Chief Editor José Paula Western Indian Ocean JOURNAL OF Marine Science Chief Editor José Paula | Faculty of Sciences of University of Lisbon, Portugal Copy Editor Timothy Andrew Editorial Board Lena GIPPERTH Aviti MMOCHI Sweden Tanzania Serge ANDREFOUËT Johan GROENEVELD France Cosmas MUNGA South Africa Kenya Ranjeet BHAGOOLI Issufo HALO Mauritius South Africa/Mozambique Nyawira MUTHIGA Kenya Salomão BANDEIRA Christina HICKS Mozambique Australia/UK Brent NEWMAN Betsy Anne BEYMER-FARRIS Johnson KITHEKA South Africa USA/Norway Kenya Jan ROBINSON Jared BOSIRE Kassim KULINDWA Seycheles Kenya Tanzania Sérgio ROSENDO Atanásio BRITO Thierry LAVITRA Portugal Mozambique Madagascar Louis CELLIERS Blandina LUGENDO Melita SAMOILYS Kenya South Africa Tanzania Pascale CHABANET Joseph MAINA Max TROELL France Australia Sweden Published biannually Aims and scope: The Western Indian Ocean Journal of Marine Science provides an avenue for the wide dissem- ination of high quality research generated in the Western Indian Ocean (WIO) region, in particular on the sustainable use of coastal and marine resources. 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ISSN 0856-860X Cover image: Macrophthalmus depressus at Saco da Inhaca, Mozambique (© Jose Paula, 2014) WIO Journal of Marine Science 18 (2 ) 2019 87-89 Short communication 87 Sometimes hard to swallow: Attempted feeding on a porcupinefish results in death of both predator and prey Bart Shepherd 1,*, Hudson T. Pinheiro2, Luiz A. Rocha2 1 Steinhart Aquarium, 2 Department of Ichthyology, * Corresponding author: California Academy of Sciences, California Academy of Sciences, [email protected] San Francisco, CA, San Francisco, CA, USA USA Abstract Predator-prey relationships are critical components of population dynamics across all ecosystems. Interactions between predators and dangerous prey are especially likely to result in a co-evolutionary arms race. To avoid pre- dation, porcupinefishes (Diodontidae) present a suite of physical and chemical defences, including spines, inflation, and the potent neurotoxin, tetrodotoxin, which is concentrated in the internal organs. A failed predation attempt is described here on a longspined porcupinefish,Diodon holocanthus, by a benthopelagic predator, Carangoides fulvogut- tatus, resulting in the death of both the predator and the prey. Keywords: asymmetrical selection; co-evolution; coral reef; ecology; fishes; Indian Ocean; predation; Zanzibar Predator-prey relationships are critical components pronounced inflation, and the potent neurotoxin of population dynamics and ubiquitous across all eco- tetrodotoxin, which is concentrated in the internal systems (Gokhale and Wignall, 2019). They are often organs (Brainerd, 1994; Wainwright et al., 1995; Bane presented as an evolutionary arms race; selection et al., 2014). This assemblage of defense mechanisms pressures within these relationships are bi-directional should effectively limit predation, however, a case is and can be asymmetrical (Brodie and Brodie, 1999). reported here where a benthopelagic fish attempted For example, the life-dinner principle characterizes a to prey upon an adult longspined porcupinefish (Dio- race between predators and prey: if predators lose, don holocanthus), and died in the process. A yellow- they may be able to hunt again, but if the prey is caught spotted trevally, Carangoides fulvoguttatus (Carangidae, and eaten, this removes it from the system and elim- approximately 1 m TL) was retrieved, dead and float- inates future reproductive potential. Therefore, the ing at the surface off the east coast of Zanzibar, on consequences are much more severe for the prey than 11 December 2018 (Fig. 1a). Upon close examination, for the predator (Dawkins and Krebs, 1979). Preda- a large longspined porcupinefish (approximately tor-prey relationships are also shaped by interactions 30 cm TL) was found in the buccal cavity (Fig. 1b). between intra and inter-specific behavioural types (e.g. The porcupinefish was barely alive, semi-inflated, with aggressive vs. docile; Chang et al., 2017). The type of its spines lodged between the trevally’s gill arches, and predator-prey interaction that is most likely to result was thus unable to extricate itself from the mouth of in a co-evolutionary arms race is in systems involving its predator (Fig. 1c). dangerous prey (Brodie and Brodie, 1999). Considering the effectiveness of the suite of defen- Porcupinefishes (Diodontidae) are circumtropical and sive strategies employed by porcupinefish, was this a inhabit a large variety of shallow water ecosystems naive predation attempt or a failed case of intentional (Nelson et al., 2016). They are slow swimmers that consumption by an overly aggressive trevally? The lit- rely upon a suite of anti-predator adaptations: spines, erature reports a relatively high diversity of predators http://dx.doi.org/10.4314/wiojms.v18i2.9 88 WIO Journal of Marine Science 18 (2 ) 2019 87-89 | B. Shepherd et al. Figure 1. (a) Adult yellowspotted trevally, Carangoides fulvoguttatus (approx. 1 m TL), found dead, floating at the ocean surface off the east coast of Zanzibar. (b)Diodon holocanthus (approx. 30 cm TL) trapped in the buccal cavity, as viewed through the mouth of the trevally. (c) Detail of Diodon holocanthus, as viewed from beneath the operculum. that feed upon juvenile porcupinefishes, including the defences of porcupinefishes and variable resistance to pelagic and reef fishes Coryphaena hippurus, Epinephelus their internal toxins, as in other taxa (Geffeney et al., itajara, Galeocerdo cuvier, Haemulon plumieri, Lutjanus ana- 2002). Therefore, this predation attempt could have lis, L. cyanopterus, L. griseus, L. synagris, Peprilus paru, Sphy- been intentional, reinforced by the trevally’s (hypo- raena barracuda and Tylosurus crocodilus (Randall, 1967; thetical) prior experiences of successfully feeding on Oxenford and Hunte, 1999). In May 2017, photographs smaller porcupinefishes. The documentation of mor- circulated on the internet of a lemon shark, Negaprion talities in individuals from other species that have brevirostris, dead on a beach in the Maldives, with a por- attempted to prey upon porcupinefishes supports the cupinefish stuck in its mouth (Weisberger, 2017). Other assertion that this is not an uncommon event. marine animals also interact with porcupinefishes; there is a documented case of a bottlenose dolphin The longspined porcupinefish’s spines, one of its pri- found dead with a slender-spined porcupinefish (Diodon mary defense mechanisms, locked the fish inside the nichthemerus) lodged in the posterior pharynx and upper predator and prevented it from escaping. Is this a case esophagus (Byard et al., 2010), as well as reports of them where an anti-predator adaptation has gone too far? being preyed upon by killer whales, Orcinus orca. Spines evolved as a defence mechanism (Shono et al., 2018), ostensibly to prevent the fish from being taken Porcupinefishes are slow swimmers that are regularly into the mouth of a predator. However, spines are not observed out in the open, including up in the water necessarily a guarantee of protection (Willman, 2007). column, and are thus easy for predators to target. They In the case of the porcupinefishes, if the fish is swal- depend upon physical (spines, inflation) and chemical lowed head first, it will easily slide into the predator’s (tetrodotoxin poison) defences to avoid this predation. mouth, due to the orientation of the spines and their Although selection pressure is usually stronger on the biomechanical erection mechanism (Brainerd, 1994). prey, predators that capture dangerous prey will expe- Nevertheless, selection pressure might be stronger rience a severe consequence with a high predictabil- for the prey here as well. Following