The biology and ecology of the ocean sunfish Mola mola: a review of current knowledge and future research perspectives

Relatively little is known about the biology and ecology of the world's largest (heaviest) bony fish, the ocean sunfish Mola mola, despite its worldwide occurrence in temperate and tropical seas. Studies are now emerging that require many common perceptions about sunfish behaviour and ecology to be re-examined. Indeed, the long-held view that ocean sunfish are an inactive, passively drifting species seems to be entirely misplaced. Technological advances in marine telemetry are revealing distinct behavioural patterns and protracted seasonal movements. Extensive forays by ocean sunfish into the deep ocean have been documented and broad-scale surveys, together with molecular and laboratory based techniques, are addressing the connectivity and trophic role of these animals. These emerging molecular and movement studies suggest that local distinct populations may be prone to depletion through bycatch in commercial fisheries. Rising interest in ocean sunfish, highlighted by the increase in recent publications, warrants a thorough review of the biology and ecology of this species. Here we review the taxonomy, morphology, geography, diet, locomotion, vision, movements, foraging ecology, reproduction and species interactions of M. mola. We present a summary of current conservation issues and suggest methods for addressing fundamental gaps in our knowledge.

Environmental context explains Levy and Brownian movement patterns of marine predators

An optimal search theory, the so-called Levy-flight foraging hypothesis(1), predicts that predators should adopt search strategies known as Levy flights where prey is sparse and distributed unpredictably, but that Brownian movement is sufficiently efficient for locating abundant prey(2-4). Empirical studies have generated controversy because the accuracy of statistical methods that have been used to identify Levy behaviour has recently been questioned(5,6). Consequently, whether foragers exhibit Levy flights in the wild remains unclear. Crucially, moreover, it has not been tested whether observed movement patterns across natural landscapes having different expected resource distributions conform to the theory's central predictions. Here we use maximum-likelihood methods to test for Levy patterns in relation to environmental gradients in the largest animal movement data set assembled for this purpose. Strong support was found for Levy search patterns across 14 species of open-ocean predatory fish (sharks, tuna, billfish and ocean sunfish), with some individuals switching between Levy and Brownian movement as they traversed different habitat types. We tested the spatial occurrence of these two principal patterns and found Levy behaviour to be associated with less productive waters (sparser prey) and Brownian movements to be associated with productive shelf or convergence-front habitats (abundant prey). These results are consistent with the Levy-flight foraging hypothesis(1,7), supporting the contention(8,9) that organism search strategies naturally evolved in such a way that they exploit optimal Levy patterns.

Tracking leatherback turtles (Dermochelys coriacea) during consecutive inter-nesting intervals: Further support for direct transmitter attachment

Over recent years there have been substantial efforts to record and interpret the post-nesting movements of leatherback turtles (Dermochelys coriacea) breeding in tropical regions. Less well documented are the movements undertaken by individual turtles during the breeding season itself, or more specifically between sequential nesting events. Such movements are of interest for two reasons: (1) gravid female leatherbacks may range extensively into the territorial waters and nesting beaches of neighbouring countries, raising questions for conservationists and population ecologists; and (2) the magnitude of movements themselves help elucidate underlying reproductive strategies (e.g. whether to rest near to the nesting or forage extensively). Here, satellite relay data loggers are used (SRDLs) to detail the movements and behaviour of two female leatherback turtles throughout three consecutive inter-nesting intervals in the Commonwealth of Dominica, West Indies. Both near-shore residence and extensive inter-nesting movements were recorded, contrasting previous studies, with movements away from the nesting beach increasing towards the end of the nesting season. Using this behavioural study as a backdrop, the suitability of attaching satellite transmitters directly to the carapace was additionally explored as an alternative approach to conventional harness deployments. Specifically, the principal aims were to (1) gather empirical data on speed of travel and (2) assess dive performance (aerobic dive limit) to enable comparisons with turtles previously fitted with harnesses elsewhere in the Caribbean (n = 6 turtles; Grenada, WI). This produced mixed results with animals bearing directly attached transmitters travelling significantly faster (55.21 km day(-1): SD 6.68) than harnessed individuals (39.80 km day(-1); SD 6.19); whilst no discernable difference in dive performance could be found between the two groups of study animals. (C) 2009 Elsevier B.V. All rights reserved.

Satellite tracking of the World's largest bony fish, the ocean sunfish (Mola mola L.) in the North East Atlantic

Satellite-linked archival transmitters were used to record the movements of three ocean sunfish (Mola mola) in the North East Atlantic. Patterns of depth use and temperature experienced by individual fish were integrated into 4-hour intervals throughout the tracking period and relayed via the Argos system. Data were recorded for 42, 90 and 54 days respectively from the three fish. The first two were tagged off southern Portugal at the end of February 2007 and travelled principally northward, while the third fish was tagged off west Ireland in August 2007 and travelled southward. These patterns are consistent with seasonal migration of ocean sunfish to high latitudes and their Subsequent return south. Maximum depths recorded by the three fish were 432 m, 472 m and 320 m respectively. All three individuals showed a diel pattern in depth use, occurring deeper during the day and shallower at night, a pattern consistent with sunfish tracking normally vertically migrating prey. Sunfish sometimes remained continuously at deeper (>200 m) depths during the day, but at other times they showed extensive movement through the water column typically travelling between their maximum depth and the surface within each 4-h period. The overall pattern to emerge was that ocean sunfish travel extensively in both horizontal and vertical dimensions, presumably in search of their patchily-distributed jellyfish prey.

Widespread occurrence of the jellyfish Pelagia noctiluca in Irish coastal and shelf waters

An oceanic cruise (October 2007) revealed the widespread occurrence of Pelagia noctiluca in the NE Atlantic just prior to a major fish kill induced by P. noctiluca in Irish coastal waters.

The role of infrequent and extraordinary deep dives in leatherback turtles (Dermochelys coriacea)

Infrequent and exceptional behaviours can provide insight into the ecology and physiology of a particular species. Here we examined extraordinarily deep (300-1250 m) and protracted (>1h) dives made by critically endangered leatherback turtles (Dermochelys coriacea) in the context of three previously suggested hypotheses: predator evasion, thermoregulation and exploration for gelatinous prey. Data were obtained via satellite relay data loggers attached to adult turtles at nesting beaches (N=11) and temperate foraging grounds (N=2), constituting a combined tracking period of 9.6 years (N=26,146 dives) and spanning the entire North Atlantic Ocean. Of the dives, 99.6% (N=26,051) were to depths <300 m with only 0.4% (N=95) extending to greater depths (subsequently termed 'deep dives'). Analysis suggested that deep dives: (1) were normally distributed around midday; (2) may exceed the inferred aerobic dive limit for the species; (3) displayed slow vertical descent rates and protracted durations; (4) were much deeper than the thermocline; and (5) occurred predominantly during transit, yet ceased once seasonal residence on foraging grounds began. These findings support the hypothesis that deep dives are periodically employed to survey the water column for diurnally descending gelatinous prey. If a suitable patch is encountered then the turtle may cease transit and remain within that area, waiting for prey to approach the surface at night. If unsuccessful, then migration may continue until a more suitable site is encountered. Additional studies using a meta-analytical approach are nonetheless recommended to further resolve this matter.

Diving behaviour of jellyfish equipped with electronic tags

Jellyfish are one of the most abundant and conspicuous members of our coastal marine fauna and are now known to play major trophic roles in marine systems. However, little is known about the movements and behaviour of individuals. We equipped individual compass jellyfish (Chrysaora hysoscella) (n = 15) off the Dingle coast, Ireland, with miniature time-depth recorders to log their depth over periods of a few hours. Vertical movements were extensive, with all jellyfish changing their depth during tracking. A range of vertical movements were seen including initial diving from the surface down to a maximum of 29.6 m after device attachment, some jellyfish remaining near the bottom, some moving up and down in mid-water and some moving back near the surface. These results show that jellyfish actively reposition themselves in the water column over small time-scales and open the way for more extensive studies equipping jellyfish with electronic tags.

Stranding events provide indirect insights into the seasonality and persistence of jellyfish medusae (Cnidaria : Scyphozoa)

It is becoming increasingly evident that jellyfish (Cnidaria: Scyphozoa) play an important role within marine ecosystems, yet our knowledge of their seasonality and reproductive strategies is far from complete. Here, we explore a number of life history hypotheses for three common, yet poorly understood scyphozoan jellyfish (Rhizostoma octopus; Chrysaora hysoscella; Cyanea capillata) found throughout the Irish and Celtic Seas. Specifically, we tested whether (1) the bell diameter/wet weight of stranded medusae increased over time in a manner that suggested a single synchronised reproductive cohort; or (2) whether the range of sizes/weights remained broad throughout the stranding period suggesting the protracted release of ephyrae over many months. Stranding data were collected at five sites between 2003 and 2006 (n = 431 surveys; n = 2401 jellyfish). The relationship between bell diameter and wet weight was determined for each species (using fresh specimens collected at sea) so that estimates of wet weight could also be made for stranded individuals. For each species, the broad size and weight ranges of stranded jellyfish implied that the release of ephyrae may be protracted (albeit to different extents) in each species, with individuals of all sizes present in the water column during the summer months. For R. octopus, there was a general increase in both mean bell diameter and wet weight from January through to June which was driven by an increase in the variance and overall range of both variables during the summer. Lastly, we provide further evidence that rhizostome jellyfish may over-wintering as pelagic medusa which we hypothesise may enable them to capitalise on prey available earlier in the year.

The energy density of jellyfish: Estimates from bomb-calorimetry and proximate-composition

Two techniques are described to calculate energy densities for the bell, gonad and oral arm tissues of three scyphozoan jellyfish (Cyanea capillata, Rhizostoma octopus and Chrysaora hysoscella). First, bomb-calorimetry was used, a technique that is readily available and inexpensive. However, the reliability of this technique for gelatinous material is contentious. Second, further analysis involving the more labour intensive proximate-composition analysis (protein, fat and carbohydrate) was carried out on two species (C capillata and R. octopus). These proximate data were subsequently converted to energy densities. The two techniques (bomb-calorimetry and proximate-composition) gave very similar estimates of energy density. Differences in energy density were found both amongst different species and between different tissues of the same species. Mean ( +/- S.D.) energy density estimates for whole animals from bomb-calorimetry were 0.18 +/- 0.05, 0.11 +/- 0.04, and 0.10 +/- 0.03 kJ g wet mass(-1) for C. capillata, R. octopus, and C. hysoscella respectively. The implications of these low energy densities for species feeding on jellyfish are discussed. (c) 2007 Elsevier B.V. All rights reserved.

The broad-scale distribution of five jellyfish species across a temperate coastal environment

Jellyfish (medusae) are sometimes the most noticeable and abundant members of coastal planktonic communities, yet ironically, this high conspicuousness is not reflected in our overall understanding of their spatial distributions across large expanses of water. Here, we set out to elucidate the spatial (and temporal) patterns for five jellyfish species (Phylum Cnidaria, Orders Rhizostomeae and Semaeostomeae) across the Irish & Celtic Seas, an extensive shelf-sea area at Europe's northwesterly margin encompassing several thousand square kilometers. Data were gathered using two independent methods: (1) surface-counts of jellyfish from ships of opportunity, and (2) regular shoreline surveys for stranding events over three consecutive years. Jellyfish species displayed distinct species-specific distributions, with an apparent segregation of some species. Furthermore, a different species composition was noticeable between the northern and southern parts of the study area. Most importantly, our data suggests that jellyfish distributions broadly reflect the major hydrographic regimes (and associated physical discontinuities) of the study area, with mixed water masses possibly acting as a trophic barrier or non-favourable environment for the successful growth and reproduction of jellyfish species.

The ocean sunfish Mola mola: insights into distribution, abundance and behaviour in the Irish and Celtic Seas

Here we provide baseline data on the distribution and abundance of Mola mola within the Irish and Celtic Seas, made during aerial surveys from June to October during 2003-2005. These data were considered in conjunction with concurrent observations of three potential jellyfish prey species found throughout the region: Rhizostoma octopus, Chrysaora hysoscella and Cyanea capillata. A total area of 7850 km(2) was surveyed over the three years with an observed abundance of 68 sunfish giving a density of 0.98 ind/100 km(2). Although modest, these findings highlight that the species is more common than once thought around Britain and Ireland and an order of magnitude greater than the other apex jellyfish predator found in the region, the leatherback turtle (Dermochelys coriacea). furthermore, the distribution of sunfish sightings was inconsistent with the extensive aggregations of Rhizostoma octopus found throughout the study area. The modelled distributions of predator-prey co-occurrence (using data for all three jellyfish species) was less than the observed co-occurrence with the implication that neither jellyfish nor sunfish were randomly distributed but co-occurred more in the same areas than expected by chance. Finally, observed sunfish were typically small (similar to 1 in or less) and seen to either bask or actively swim at the surface.

Jellyfish aggregations and leatherback turtle foraging patterns in a temperate coastal environment

Leatherback turtles (Dermochelys coriacea) are obligate predators of gelatinous zooplankton. However, the spatial relationship between predator and prey remains poorly understood beyond sporadic and localized reports. To examine how jellyfish (Phylum Cnidaria: Orders Semaeostomeae and Rhizostomeae) might drive the broad-scale distribution of this wide ranging species, we employed aerial surveys to map jellyfish throughout a temperate coastal shelf area bordering the northeast Atlantic. Previously unknown, consistent aggregations of Rhizostoma octopus extending over tens of square kilometers were identified in distinct coastal

Developing a simple, rapid method for identifying and monitoring jellyfish aggregations from the air

Within the marine environment, aerial surveys have historically centred on apex predators, such as pinnipeds, cetaceans and sea birds. However, it is becoming increasingly apparent that the utility of this technique may also extend to subsurface species such as pre-spawning fish stocks and aggregations of jellyfish that occur close to the surface. In light of this, we tested the utility of aerial surveys to provide baseline data for 3 poorly understood scyphozoan jellyfish found throughout British and Irish waters: Rhizostoma octopus, Cyanea capillata and Chrysaora hysoscella. Our principal objectives were to develop a simple sampling protocol to identify and quantify surface aggregations, assess their consistency in space and time, and consider the overall applicability of this technique to the study of gelatinous zooplankton. This approach provided a general understanding of range and relative abundance for each target species, with greatest suitability to the study of R. octopus. For this species it was possible to identify and monitor extensive, temporally consistent and previously undocumented aggregations throughout the Irish Sea, an area spanning thousands of square kilometres. This finding has pronounced implications for ecologists and fisheries managers alike and, moreover, draws attention to the broad utility of aerial surveys for the study of gelatinous aggregations beyond the range of conventional ship-based techniques.