Andrew G. Jeffs

Sound as an Orientation Cue for the Pelagic Larvae of Reef Fishes and Decapod Crustaceans

The pelagic life history phase of reef fishes and decapod crustaceans is complex, and the evolutionary drivers and ecological consequences of this life history strategy remain largely speculative. There is no doubt, however, that this life history phase is very significant in the demographics of reef populations. Here, we initially discuss the ecology and evolution of the pelagic life histories as a context to our review of the role of acoustics in the latter part of the pelagic phase as the larvae transit back onto a reef. Evidence is reviewed showing that larvae are actively involved in this transition. They are capable swimmers and can locate reefs from hundreds of metres if not kilometres away. Evidence also shows that sound is available as an orientation cue, and that fishes and crustaceans hear sound and orient to sound in a manner that is consistent with their use of sound to guide settlement onto reefs. Comparing particle motion sound strengths in the field (8 x 10(-11) m at 5 km from a reef) with the measured behavioural and electrophysiological threshold of fishes of (3 x 10(-11) m and 10 x 10(-11), respectively) provides evidence that sound may be a useful orientation cue at a range of kilometres rather than hundreds of metres. These threshold levels are for adult fishes and we conclude that better data are needed for larval fishes and crustaceans at the time of settlement. Measurements of field strengths in the region of reefs and threshold levels are suitable for showing that sound could be used; however, field experiments are the only effective tool to demonstrate the actual use of underwater sound for orientation purposes. A diverse series of field experiments including light-trap catches enhanced by replayed reef sound, in situ observations of behaviour and sound-enhanced settlement rate on patch reefs collectively provide a compelling case that sound is used as an orientation and settlement cue for these late larval stages.

THE USE OF ENERGY STORES IN THE PUERULUS OF THE SPINY LOBSTER JASUS EDWARDSII ACROSS THE CONTINENTAL SHELF OF NEW ZEALAND

Abstract Nektonic pueruli of the spiny lobster, Jasus edwardsii, were caught from two locations about 20 km apart across the continental shelf on the south east of the North Island, New Zealand. The pueruli were assayed for total protein, glucose, glycogen, and lipid content. Only the lipid content differed between pueruli caught onshore and offshore (mean difference=3.1 mg or 3.4% of dry mass). The average difference in lipid content measured over this distance was used to calculate the rate of energy consumption and timing for pueruli to actively swim from the continental shelf to shore. These results confirmed previous theoretical estimates and indirect measures. Furthermore, the rate of energy consumption would allow all of the pueruli caught offshore to swim to shore based on their total measured lipids. However, some individuals with low energy stores may be energetically compromised at arrival which may affect their subsequent moulting and survival. The results of this study indicate that lipid is the primary format for energy storage of the nektonic puerulus of the spiny lobster and that these lipid reserves have sufficient energetic capacity to allow the puerulus to actively swim the distance across the shelf to settle on the coast.

How do spiny lobster post‐larvae find the coast?

Abstract The larvae or phyllosomes of many species of spiny lobsters (Palinuridae) are known to complete their development in offshore oceanic waters. Phyllosomes metamorphose to non‐feeding, nektonic post‐larvae or pueruli, which move into shallow coastal waters where they settle to become benthic dwelling juveniles. There is growing evidence that the movement of pueruli is directed toward the coast rather than a process of random dispersal. The migration inshore by the non‐feeding pueruli is likely to be one of the more extreme examples of onshore orientation among marine organisms, but is still poorly understood. This article provides a synthesis of the current state of knowledge of the possible cues and sensory mechanisms that might be used by pueruli of spiny lobsters for orienting toward the coast from offshore waters. The review is used to identify the potential cues that would benefit from future research efforts.

Lipid reserves used by pueruli of the spiny lobster Jasus edwardsii in crossing the continental shelf of New Zealand

Lipid is known to fuel the movement of the nektonic puerulus stage of the spiny lobster Jasus edwardsii across the continental shelf of New Zealand. Lipid class analysis of pueruli caught from two locations across the continental shelf showed that phospholipid predominated (86-96% of total lipid), with only smaller proportions of sterol (0.9-8.7%) and diacylglycerol (1.2-7.6%). Only traces of triacylglycerol, hydrocarbon and wax ester were present (<0.1% of total lipid). Comparison of the lipid class content of pueruli caught onshore and offshore showed that phospholipid reserves are primarily utilised during this important phase in the lifecycle and that diacylglycerol plays a less significant secondary role. Histology identified concentrations of phospholipid in fat bodies located in the haemocoel. The use of phospholipid as the dominant storage medium in the puerulus stage is unlike many other marine taxa, including crustacea, which tend to use triacylglycerol and wax ester. The use of phospholipid as a storage medium may well be related to its characteristic transparency, an important feature of this nektonic stage of lobster development that is highly vulnerable to pelagic visual predators.

Lipids and nutrition of the southern rock lobster, Jasus edwardsii, from hatch to puerulus

We examined the lipid class and fatty-acid composition of the southern rock lobster, Jasus edwardsii, phyllosomas larvae and puerulus stage to improve understanding of their nutrition in relation to aquaculture. Lipid is critical in the nutrition of larval crustaceans, including lobsters. Specimens were from Tasmanian waters, Australia, and North Island, New Zealand, waters. Analyses were by TLC-FID and capillary GC and GC-MS. Phyllosomas larvae and nektonic pueruli were low in storage lipid (triacylglycerol), and phospholipid was the major lipid class. Sterol, mainly cholesterol, was the next most abundant class. The ratio of the essential omega-3 fatty acid eicosapentaenoic acid (EPA) to the omega-6 fatty acid arachidonic acid (AA) was lower in newly hatched phyllosomas (1.2-1.3) than in other phyllosomas (stages III-XI; 2.8-6.7) and pueruli (3.8). Ratios of the omega-3 fatty acid DHA (docosahexaenoic acid) to EPA were also lower in newly hatched phyllosomas (0.5) than in later-stage phyllosomas (1.5-2.1) and pueruli (1.2). We have followed up these compositional data by successfully enriching the live diet (Artemia) of early phyllosomas with AA, EPA and DHA. This dietary manipulation has achieved ratios of these key polyunsaturated fatty acids similar to those of wild phyllosomas. These findings will be of significance to the future of rock-lobster aquaculture.

Determining the Diet of Larvae of Western Rock Lobster (Panulirus cygnus) Using High-Throughput DNA Sequencing Techniques

The Western Australian rock lobster fishery has been both a highly productive and sustainable fishery. However, a recent dramatic and unexplained decline in post-larval recruitment threatens this sustainability. Our lack of knowledge of key processes in lobster larval ecology, such as their position in the food web, limits our ability to determine what underpins this decline. The present study uses a high-throughput amplicon sequencing approach on DNA obtained from the hepatopancreas of larvae to discover significant prey items. Two short regions of the 18S rRNA gene were amplified under the presence of lobster specific PNA to prevent lobster amplification and to improve prey amplification. In the resulting sequences either little prey was recovered, indicating that the larval gut was empty, or there was a high number of reads originating from multiple zooplankton taxa. The most abundant reads included colonial Radiolaria, Thaliacea, Actinopterygii, Hydrozoa and Sagittoidea, which supports the hypothesis that the larvae feed on multiple groups of mostly transparent gelatinous zooplankton. This hypothesis has prevailed as it has been tentatively inferred from the physiology of larvae, captive feeding trials and co-occurrence in situ. However, these prey have not been observed in the larval gut as traditional microscopic techniques cannot discern between transparent and gelatinous prey items in the gut. High-throughput amplicon sequencing of gut DNA has enabled us to classify these otherwise undetectable prey. The dominance of the colonial radiolarians among the gut contents is intriguing in that this group has been historically difficult to quantify in the water column, which may explain why they have not been connected to larval diet previously. Our results indicate that a PCR based technique is a very successful approach to identify the most abundant taxa in the natural diet of lobster larvae.

Location, location, location: finding a suitable home among the noise

While sound is a useful cue for guiding the onshore orientation of larvae because it travels long distances underwater, it also has the potential to convey valuable information about the quality and type of the habitat at the source. Here, we provide, to our knowledge, the first evidence that settlement-stage coastal crab species can interpret and show a strong settlement and metamorphosis response to habitat-related differences in natural underwater sound. Laboratory- and field-based experiments demonstrated that time to metamorphosis in the settlement-stage larvae of common coastal crab species varied in response to different underwater sound signatures produced by different habitat types. The megalopae of five species of both temperate and tropical crabs showed a significant decrease in time to metamorphosis, when exposed to sound from their optimal settlement habitat type compared with other habitat types. These results indicate that sounds emanating from specific underwater habitats may play a major role in determining spatial patterns of recruitment in coastal crab species.

Crabs on cue for the coast: the use of underwater sound for orientation by pelagic crab stages

Several studies have suggested that underwater sound may provide an orientation cue for the pelagic stages of coastal crustacea, such as crabs and lobsters, to find their way from the open ocean to the coast where they can settle. Yet, there has been no field evidence to support this phenomenon and it is unclear whether pelagic crustacean stages even have the ability to orient towards sources of underwater sound, such as that which emanates from reefs. Artificial sources of natural underwater sound were deployed offshore in conjunction with light traps to determine if the larval and post-larval stages of coastal crabs were attracted to coastal reef sound. The results demonstrated that the pelagic stages of crabs respond to underwater sounds and that they may use underwater sound to orient towards the coast. The orientation behaviour was modulated by lunar phase, being evident only during first- and last-quarter moon phases, at the time of neap tides. Active orientation during neap tides may take advantage of these incoming night-time tides for predator avoidance or may permit more effective directed swimming activity than is possible during new and full moon spring tides.

PCR enrichment techniques to identify the diet of predators

The increasing sensitivity of PCR has meant that in the last two decades PCR has emerged as a major tool in diet studies, enabling us to refine our understanding of trophic links and to elucidate the diets of predators whose prey is as yet uncharacterized. The achievements and methods of PCR‐based diet studies have been reviewed several times, but here we review an important development in the field: the use of PCR enrichment techniques to promote the amplification of prey DNA over that of the predator. We first discuss the success of using group‐specific primers either in parallel single reactions or in multiplex reactions. We then concentrate on the more recent use of PCR enrichment techniques such as restriction enzyme digests, peptide nucleic acid clamping, DNA blocking and laser capture microdissection. We also survey the vast literature on enrichment techniques in clinical biology, to ascertain the pitfalls of enrichment techniques and what refinements have yielded some highly sensitive methods. We find that while there are several new approaches to enrichment, peptide nucleic acid clamping and DNA blocking are generally sufficient techniques for the characterization of diets of predators and highlight the most important considerations of the approach.

Adaptive avoidance of reef noise.

Auditory information is widely used throughout the animal kingdom in both terrestrial and aquatic environments. Some marine species are dependent on reefs for adult survival and reproduction, and are known to use reef noise to guide orientation towards suitable habitat. Many others that forage in food-rich inshore waters would, however, benefit from avoiding the high density of predators resident on reefs, but nothing is known about whether acoustic cues are used in this context. By analysing a sample of nearly 700,000 crustaceans, caught during experimental playbacks in light traps in the Great Barrier Reef lagoon, we demonstrate an auditory capability in a broad suite of previously neglected taxa, and provide the first evidence in any marine organisms that reef noise can act as a deterrent. In contrast to the larvae of species that require reef habitat for future success, which showed an attraction to broadcasted reef noise, taxa with a pelagic or nocturnally emergent lifestyle actively avoided it. Our results suggest that a far greater range of invertebrate taxa than previously thought can respond to acoustic cues, emphasising yet further the potential negative impact of globally increasing levels of underwater anthropogenic noise.