Luke Harman

Gill Damage to Atlantic Salmon (Salmo salar) Caused by the Common Jellyfish (Aurelia aurita) under Experimental Challenge

Background Over recent decades jellyfish have caused fish kill events and recurrent gill problems in marine-farmed salmonids. Common jellyfish (Aurelia spp.) are among the most cosmopolitan jellyfish species in the oceans, with populations increasing in many coastal areas. The negative interaction between jellyfish and fish in aquaculture remains a poorly studied area of science. Thus, a recent fish mortality event in Ireland, involving Aurelia aurita, spurred an investigation into the effects of this jellyfish on marine-farmed salmon. Methodology/Principal Findings To address the in vivo impact of the common jellyfish (A. aurita) on salmonids, we exposed Atlantic salmon (Salmo salar) smolts to macerated A. aurita for 10 hrs under experimental challenge. Gill tissues of control and experimental treatment groups were scored with a system that rated the damage between 0 and 21 using a range of primary and secondary parameters. Our results revealed that A. aurita rapidly and extensively damaged the gills of S. salar, with the pathogenesis of the disorder progressing even after the jellyfish were removed. After only 2 hrs of exposure, significant multi-focal damage to gill tissues was apparent. The nature and extent of the damage increased up to 48 hrs from the start of the challenge. Although the gills remained extensively damaged at 3 wks from the start of the challenge trial, shortening of the gill lamellae and organisation of the cells indicated an attempt to repair the damage suffered. Conclusions Our findings clearly demonstrate that A. aurita can cause severe gill problems in marine-farmed fish. With aquaculture predicted to expand worldwide and evidence suggesting that jellyfish populations are increasing in some areas, this threat to aquaculture is of rising concern as significant losses due to jellyfish could be expected to increase in the future.

Fat head: an analysis of head and neck insulation in the leatherback turtle (Dermochelys coriacea).

SUMMARY Adult leatherback turtles are gigantothermic/endothermic when foraging in cool temperate waters, maintaining a core body temperature within the main body cavity of ca. 25°C despite encountering surface temperatures of ca. 15°C and temperatures as low as 0.4°C during dives. Leatherbacks also eat very large quantities of cold, gelatinous prey (medusae and pyrosomas). We hypothesised that the head and neck of the leatherback would have structural features to minimise cephalic heat loss and limit cooling of the head and neck during food ingestion. By gross dissection and analytical computed tomography (validated by ground truthing dissection) of an embalmed specimen we confirmed this prediction. 21% of the head and neck was occupied by adipose tissue. This occurred as intracranial blubber, encapsulating the salt glands, medial portions of the eyeballs, plus the neurocranium and brain. The dorsal and lateral surfaces of the neck featured thick blubber pads whereas the carotid arteries and jugular veins were deeply buried in the neck and protected laterally by blubber. The oesophagus was surrounded by a thick sheath of adipose tissue whereas the oropharyngeal cavity had an adipose layer between it and the bony proportion of the palate, providing further ventral insulation for salt glands and neurocranium.

Ontogenetic changes in tracheal structure facilitate deep dives and cold water foraging in adult leatherback sea turtles.

SUMMARY Adult leatherbacks are large animals (300–500 kg), overlapping in size with marine pinniped and cetacean species. Unlike marine mammals, they start their aquatic life as 40–50 g hatchlings, so undergo a 10,000-fold increase in body mass during independent existence. Hatchlings are limited to the tropics and near-surface water. Adults, obligate predators on gelatinous plankton, encounter cold water at depth (<1280 m) or high latitude and are gigantotherms that maintain elevated core body temperatures in cold water. This study shows that there are great ontogenetic changes in tracheal structure related to diving and exposure to cold. Hatchling leatherbacks have a conventional reptilian tracheal structure with circular cartilaginous rings interspersed with extensive connective tissue. The adult trachea is an almost continuous ellipsoidal cartilaginous tube composed of interlocking plates, and will collapse easily in the upper part of the water column during dives, thus avoiding pressure-related structural and physiological problems. It is lined with an extensive, dense erectile vascular plexus that will warm and humidify cold inspired air and possibly retain heat on expiration. A sub-luminal lymphatic plexus is also present. Mammals and birds have independently evolved nasal turbinates to fulfil such a respiratory thermocontrol function; for them, turbinates are regarded as diagnostic of endothermy. This is the first demonstration of a turbinate equivalent in a living reptile.

Opening and closing mechanisms of the leatherback sea turtle larynx: a crucial role for the tongue

SUMMARY A combination of dissection and computed tomography scanning has provided significant novel insights into the structure and function of the Dermochelys coriacea larynx and its associated muscles. Several previously unknown features of the laryngeal aditus (glottis) are described and their functional significance in its opening and closure are considered. The tongue plays an essential part in producing and maintaining closure during dives and feeding bouts. Closure is brought about by compression of the glottis under the action of the two hyoglossus muscles. The tongue thus plays the role of the epiglottis of mammals, sealing the entrance to the larynx. As is already clear, opening is brought about by abduction of the arytenoid cartilages. In addition, there is a powerful mechanism for maintaining the larynx in close apposition to the hyoid plate during feeding and neck flexion, thereby enhancing the efficiency of feeding.

Determination of spatial and temporal variability of pH and dissolved oxygen concentrations in a seasonally hypoxic semi-enclosed marine basin using continuous monitoring

Measurement and prediction of ocean acidification effects for nearshore marine ecosystems is currently a major objective of climate change research. This study examines the scales of pH variability in both surface waters (<10 m depth) and deeper waters associated with localised seasonal hypoxia over two years at Lough Hyne marine reserve, Cork, Ireland. Lough Hyne, a semi-enclosed marine system, experiences localised seasonal (approximately May to September each year) hypoxia and eventual anoxia below a depth of circa 25 m, due largely to its bathymetric profile. We report the relationships between pH and other environmental parameters such as dissolved oxygen (DO) and temperature at this location, and we provide data, obtained using continuous autonomous sensing technology, which demonstrates that the variability in pH measurements in the waters of Lough Hyne marine reserve are comparable to predictions of future ocean acidification. This is of interest as comparatively few directly measured time series of pH in marine waters are reported, and additionally the first pH measurements were reported from Lough Hyne over 6 decades ago in 1952. This work also measures for the first time the steep chemical gradients associated with the transition from anoxia to normoxia that result in profound pH changes at Lough Hyne, providing insight into natural variability in pH experienced by marine organisms at such locations.

Behavioural responses of shallow-water benthic marine scavengers to fish carrion: a preliminary study

Abstract Observations of the behavioural responses of near-shore marine scavengers to fish carrion were made at two depths (1–2 m, 16–18 m). Gobies and juvenile whelks were the most numerous scavengers, but appeared to consume little biomass. The first scavengers to appear at carrion (seconds/minutes) were swimming forms, later (minutes) joined by fast-moving, crawling portunid crabs. Large scavengers (crabs/starfish/catsharks) arrived after tens of minutes/hours. Scavengers were ‘direct feeders’ on the bait (crabs and some fish) or ‘indirect feeders’ (gobies and whelks) on scraps generated by direct feeders. Scavengers spent little time in aggression. While fish spent relatively low proportions of their time feeding (e.g. Lipophrys pholis: 2.2–15.8%), crabs fed almost continuously (e.g. Carcinus maenas: 97.8–99.3%) before leaving baits. Crab presence depressed fish feeding. Crabs were wasteful feeders that macerated the baits, generating scraps for indirect feeders and attracting more scavengers. Large scavengers consumed most bait.

Using tagging data and aerial surveys to incorporate availability bias in the abundance estimation of blue sharks (Prionace glauca)

There is worldwide concern about the status of elasmobranchs, primarily as a result of overfishing and bycatch with subsequent ecosystem effects following the removal of top predators. Whilst abundant and wide-ranging, blue sharks (Prionace glauca) are the most heavily exploited shark species having suffered marked declines over the past decades, and there is a call for robust abundance estimates. In this study, we utilized depth data collected from two blue sharks using pop-up satellite archival tags, and modelled the proportion of time the sharks were swimming in the top 1-meter layer and could therefore be detected by observers conducting aerial surveys. The availability models indicated that the tagged sharks preferred surface waters whilst swimming over the continental shelf and during daytime, with a model-predicted average proportion of time spent at the surface of 0.633 (SD = 0.094) for on-shelf, and 0.136 (SD = 0.075) for off-shelf. These predicted values were then used to account for availability bias in abundance estimates for the species over a large area in the Northeast Atlantic, derived through distance sampling using aerial survey data collected in 2015 and 2016 and modelled with density surface models. Further, we compared abundance estimates corrected with model-predicted availability to uncorrected estimates and to estimates that incorporated the average time the sharks were available for detection. The mean abundance (number of individuals) corrected with modelled availability was 15,320 (CV = 0.28) in 2015 and 11,001 (CV = 0.27) in 2016. Depending on the year, these estimates were ~7 times higher compared to estimates without the bias correction, and ~3 times higher compared to the abundances corrected with average availability. When the survey area contains habitat heterogeneity that may affect surfacing patterns of animals, modelling animals’ availability provides a robust alternative to correcting for availability bias and highlights the need for caution when applying “average” correction factors.

Marine aloricate ciliate red tides in a temperate Irish sea lough

Although red tides are typically formed by dinoflagellate blooms, aloricate ciliates in the genus Mesodinium also produce striking red blooms throughout the world. In mid-March 2015, we confirmed the occurrence of dense blooms of Mesodinium major in Lough Hyne Marine Nature Reserve, a fully marine sea lough in County Cork, SW Ireland. Daytime aggregations of these highly mobile ciliates occurred in the surface and subsurface waters of the lough, particularly along the western shore and in the Goleen. Fine-scale comparisons of dissolved oxygen (DO) and water temperature values indicated that the surface water supporting dense blooms was slightly but significantly more oxygenated and warmer than closely juxtaposed water without visible blooms. Coarse-scale comparisons, however, showed no significant difference in DO or temperature between bloom and non-bloom areas, although there were highly significant differences in the two parameters by water depth and location within the lough. Although this is the first formal report of red-water ciliate blooms for Lough Hyne and County Cork, it is not the first known occurrence; earlier spring red tides at the lough were assumed (probably in error) to be caused solely or primarily by dinoflagellates and/or loricate ciliates (tintinnids).

Nassariid whelks hitch-hiking on Cancer pagurus : phoresis, commensalism or fouling?

The behavioural responses of scavenging animals to mackerel ( Scomber scombrus ) baits were studied by short-term video photography in shallow water (16–18 m depth) at Lough Hyne, Ireland. Earliest arrivals (after seconds/minutes) at baits were small fish or swimming crabs ( Liocarcinus depurator ), followed by crawling portunid crabs. After tens of minutes, juvenile whelks 2–4 mm shell length ( Nassarius reticulatus and/or Nassarius incrassatus ) sometimes arrived to feed. They moved at a mean speed of 1.24 (SD 0.392) mm s −1 . After tens of minutes or hours, single large scavengers arrived, consuming most of the bait; the most common of these were Cancer pagurus that fed in a wasteful fashion, generating large quantities of mackerel scraps. Cancer pagurus moved into view at a mean speed of 48.7 (SD 16.9) mm s −1 (39 times the whelk speed). A single individual of C. pagurus (197 mm carapace width) arrived at a bait carrying 24 juvenile whelks on the dorsal surface of its carapace. No whelks were present on walking legs or chelipeds. The crab fed for 6.8 min and 3 whelks fell off before it departed. The nature of this crab/whelk association is discussed; on balance it appears that it is a previously unreported example of phoresy/phoresis. No whelks were observed being carried by other edible crabs or upon large numbers of scavenging portunid crabs.

Comparison of Inorganic and Organic Matter Sedimentation in a Natural Laboratory: A One-Year Study at Lough Hyne Marine Reserve, Ireland

Measuring sedimentation rates may provide useful information on the habitat preferences of marine organisms. To understand the effect of flow rates and meteorological conditions on sedimentation in the absence of other confounding factors, sedimentation of organic (OM) and inorganic (IOM) matters was measured at 6 sites in Lough Hyne Marine Reserve (a semienclosed marine lake) over the course of 13 months. During winter, both OM and IOM were imported to the Lough, peaking in December at Whirlpool, the site nearest to the Lough entrance, likely as a result of extreme weather conditions causing resuspension of matter outside the Lough. Highest inorganic matter (IOM) sedimentation occurred in December (47.36 gm−2d−1 at Whirlpool Cliff) and was related to November wind speeds (, ). Decreasing current speed also caused a decline in IOM sedimentation. Highest OM sedimentation occurred in December at Whirlpool (5.59 gm−2d−1), but was not related to meteorological conditions. No single environmental factor strongly influenced organic matter (OM) sedimentation. One-way ANOVAs on OM and log-transformed IOM data showed that sedimentation differed significantly amongst the six sites within the Lough. Increased plankton production in the Lough during summer led to increased OM sedimentation in areas of low current speed away from the entrance of the Lough.