Adaptations for cryopelagic life in the antarctic notothenioid fish Pagothenia borchgrevinki

Summary The cryopelagic circumantarctic notothenioid fish Pagothenia borchgrevinki lives near the undersurface of the sea ice in McMurdo Sound, Antarctica. When compared to closely related benthic species (especially Trematomus bernacchii), Pagothenia exhibited substantial morphological differences in a variety of organ systems. The values of the fineness ratio and the indices of trunk shape and flatness suggested streamlining and drag reduction, adaptations to life in the water column. Pagothenia also lacked substrate contact adaptations in the pelvic and anal fins. Silvery reflective layers (strata argentea) beneath the skin and in the iris and choroid of the eye provided camouflage when Pagothenia were viewed against a background of platelet ice. The retina had many cones indicating the eye was adapted to both diurnal and nocturnal vision. During the austral spring Pagothenia fed exclusively on nektonic organisms near the ice-water interface. Dietary diversity was low; copepods and amphipods were the most frequently occurring and amphipods were the most frequently occurring taxa. In conclusion, Pagothenia appear specialized for life in the water column.     

Heat tolerance and its plasticity in Antarctic fishes

The adaptive radiation of the Antarctic notothenioid ancestral benthic fish stock within the chronic freezing waters of the Southern Ocean gave rise to five highly cold adapted families. Their stenothermy, first observed from several high-latitude McMurdo Sound species, has been of increasing recent interest given the threat of rising polar water temperatures from global climate change. In this study we determined the heat tolerance in a geographically diverse group of 11 Antarctic species as their critical thermal maximum (CTMax). When acclimatized to their natural freezing water temperatures, environmental CTMaxs ranged from 11.95 to 16.17 °C, well below those of fishes endemic to warmer waters. There was a significant regional split, with higher CTMaxs in species from the more northerly and thermally variable Seasonal Pack-ice Zone. When eight of the Antarctic species were warm acclimated to 4 °C all showed a significant increase over their environmental CTMaxs, with several showing plasticity comparable in magnitude to some far more eurythermal fishes. When the accrual of heat tolerance during acclimation was followed in three high-latitude McMurdo Sound species, it was found to develop slowly in two of them, which was correlated with their low metabolic rates.     

Inducible heat tolerance in Antarctic notothenioid fishes

Significant increases in heat tolerance (time of survival at 14°C) were observed for some, but not all, species of notothenioid fishes collected from McMurdo Sound, Antarctica (77°51′S) following acclimation to 4°C. The increase in thermal tolerance was rapid in Trematomus bernacchii, developing within 1–2 days of acclimation to 4°C. Long-term (6–8 weeks) acclimation to 4°C led to greater heat tolerance in Trematomus pennellii than in T. bernacchii. Unlike its demersal congeners, the cryopelagic notothenioid Pagothenia borchgrevinki did not increase heat tolerance during warm acclimation. A deep-living zoarcid fish, Lycodichthys dearborni, also failed to increase heat tolerance, but survived significantly (> threefold) longer at 14°C than the notothenioids.     

Morphology of the brain and sense organs in the snailfish Paraliparis devriesi: Neural convergence and sensory compensation on the Antarctic shelf

The Antarctic snailfish Paraliparis devriesi (Liparidae) is an epibenthic species, inhabiting depths of 500–650 m in McMurdo Sound. Liparids are the most speciose fish family in the Antarctic Region. We examine the gross morphology and histology of the sense organs and brain of P. devriesi and provide a phyletic perspective by comparing this morphology to that of four scorpaeniforms and of sympatric perciform notothenioids. The brain has numerous derived features, including well-developed olfactory lamellae with thick epithelia, large olfactory nerves and bulbs, and large telencephalic lobes. The retina contains only rods and exhibits a high convergence ratio (82:1). Optic nerves are small and nonpleated. The tectum is small. The corpus of the cerebellum is large, whereas the valvula is vestigial. The rhombencephalon and bulbospinal junction are extended and feature expanded vagal and spinal sensory lobes as well as hypertrophied dorsal horns and funiculi in the rostral spinal cord. The lower lobes of the pectoral fins have taste buds and expanded somatosensory innervation. Although the cephalic lateral line and anterior lateral line nerve are well developed, the trunk lateral line and posterior lateral line nerve are reduced. Near-field mechanoreception by trunk neuromasts may have been compromised by the watery, gelatinous subdermal extracellular matrix employed as a buoyancy mechanism. The expanded somatosensory input to the pectoral fin may compensate for the reduction in the trunk lateral line. The brains of P. devriesi and sympatric notothenioids share well-developed olfactory systems, an enlarged preoptic-hypophyseal axis, and subependymal expansions. Although the functional significance is unknown, the latter two features are correlated with habitation of the deep subzero waters of the Antarctic shelf. J. Morphol. 237:213–236, 1998. © 1998 Wiley-Liss, Inc.     

Diversification of brain and sense organ morphology in Antarctic dragonfishes (Perciformes: Notothenioidei: Bathydraconidae)

In the subzero shelf waters of Antarctica, fishes of the perciform suborder Notothenioidei dominate the fish fauna and constitute an adaptive radiation and a species flock. The 16 species of dragonfishes of the family Bathydraconidae live from surface waters to nearly 3,000 m and have the greatest overall depth range among notothenioid families. We examined the anatomy and histology of the brain, retina, and cephalic lateral line system of nine bathydraconid species representing 8 of the 11 known genera. We evaluate these data against a cladogram identifying three clades in the family. We provide a detailed drawing of the brain and cranial nerves of Gymnodraco acuticeps and Akarotaxis nudiceps. Bathydraconid brain morphology falls into two categories. Brains of most species are similar to those of generalized perciforms and some basal notothenioids (Class I). However, brains of deep-living bathydraconids (members of the tribe Bathydraconini minus Prionodraco) have a reduced telencephalon and tectum that renders the neural axis visible - the stalked brain morphology (Class II). All bathydraconids have duplex (rod and cone) retinae but there is considerable interspecific variation in the ratio of cones:rods and in the number of cells in the internal nuclear layer. Retinal histology reflects habitat depth but is not tightly coupled to phylogeny. Although the deep-living species of Bathydraconini have rod-dominated retinae, the retinae of some sister species are photopic. An expanded cephalic lateral line system is also characteristic of all members of the Bathydraconini as exemplified by Akarotaxis. This morphology includes large lateral line pores, wide membranous canals, hypertrophied canal neuromasts, and large anterodorsal lateral line nerves, eminentia granulares, and crista cerebellares. The saccular otoliths are also enlarged in members of this tribe. Neural diversification among bathydraconids on the Antarctic shelf has not involved the evolution of sensory specialists. Brain and sense organ morphologies do not approach the specialized condition seen in primary deep-sea fishes or even that of some secondary deep-sea fishes including sympatric non-notothenioids such as liparids (snailfishes) and muraenolepidids (eel cods). The brains and sense organs of bathydraconids, including the deep-living species, reflect their heritage as perciform shorefishes.     

Sedimentation in McMurdo Sound, Antarctica: a disturbance mechanism for benthic invertebrates

A slumping event that occurred on permanent transect lines from 12- to 30- m depth located at Arrival Heights, McMurdo Sound, Antarctica in 1993, provided an opportunity to examine the effects of sediment-mediated disturbance on the benthic invertebrate fauna. The disturbance had a particularly significant impact on the soft coral Alcyonium paessleri, which resulted in 84% colony mortality downslope from the slump site compared to an average annual mortality rate of 14% on control transects. In contrast, anchor ice at the same site accounted for removal of 5% of the population in 1992. Laboratory experiments with A. paessleri colonies under conditions of periodic sediment resuspension indicate that the soft corals are susceptible to this form of disturbance. Our observations suggest they are capable of shedding fine silt in the laboratory, which might explain the presence of A. paessleri in soft-sediment sites around McMurdo Sound. However, scarring by larger gravel in laboratory assays was slow to heal and may account for much of the colony mortality we observed. Several invertebrate-barren rocky benthic regions in McMurdo Sound were suggestive of historical slumping events. Given the removal of the smaller grain size sediments from these areas – a typically slow process – it appears these communities are slow to recover. The long-term effects of sedimentation on the benthic communities are unknown, but the impact on A. paessleri, one of the most common and fastest growing species, suggests this disturbance mechanism could lead to significant restructuring of these communities. Received: 29 November 1996 / Accepted: 23 February 1997     

Evolution and Diversification of Antarctic Notothenioid Fishes

Antarctica supported fossil ichthyofaunas during the Devonian,Jurassic, Cretaceous and Eocene/Oligocene. These faunas arenot ancestral to each other, nor are they related to any componentof the modern fauna. About one hundred species of notothenioidsdominate a modern fauna of over 200 species of bottom fishes.This highly endemic perciform suborder is not representedinthe fossil record of Antarctica. Notothenioids may have evolvedin situ on the margins of the Antarctic continent while graduallyadapting to cooling conditions during the Tertiary. Cladisticstudies indicate that notothenioids are a monophyletic group,but a sister group has not been identified among perciform fishes.With relatively few non-notothenioid fishes in Antarctic waters,notothenioids fill ecological roles normally occupied by taxonomicallydiverse fishes in temperate waters. There are six notothenioidfamilies: Bovichtidae, Nototheniidae, Harpagiferidae, Artedidraconidae,Bathydraconidae and Channichthyidae. Aspects of theirbiologyare briefly considered with emphasis on the Nototheniidae, themost speciose family. Evolutionary diversification within thisfamily allows recognition of species which are pelagic, cryopelagic,benthopelagic and benthic.     

Spatial and temporal variations in the diet of nototheniid fish in McMurdo Sound,Antarctica

Specimens of 4 species of Antarctic fish were captured at different locations in McMurdo Sound during the early summer, and for one species also during late winter. Stomach contents were analysed to examine resource utilization across species, at different locations, and between late winter and early summer. The results are consistent with earlier findings that there is a gradation in resource utilization across these species.T. pennelli andT. bernacchii tend to take predominantly benthic crawling prey, though they also take prey from the water column.T. hansoni andT. nicolai tend to take more prey from the water column, a tendency which can be related to the visual feeding vector of these species. Substantial differences in diet for the same species captured in different locations indicated significant flexibility in prey selection which would allow utilization of spatial and temporal fluctuations in prey availability. Successful feeding byT. bernacchii in late winter is a further indication that this species can feed non-visually and supports the notion that non-visual feeding mechanisms are likely to be of importance in the biology of the Antarctic fishes.deceased     

PHOTOSYNTHESIS AND CELL DIVISION BY ANTARCTIC MICROALGAE: COMPARISON OF BENTHIC,PLANKTONIC AND ICE ALGAE1

Irradiance-dependent rates of photosynthesis and cell division of six species of microalgae isolated from the benthos, plankton and sea ice microbial community in McMurdo Sound, Antarctica were compared. Microalgae isolated from different photic environments had distinct photosynthetic and growth characteristics. For benthic and ice algae, photosynthesis saturated at 6 to 20 μE.m^?2.s^?1 and was photoinhibited at 10 to 80 μE.m^?2.s^?1 while for the planktonic algae, saturation irradiances were up to 13 times higher and photoinhibition was not detected. The slope of the light-limited portion of the P-I relationship was up to 50 times greater for the benthic algae than for either the ice or planktonic algae suggesting that benthic algae used the low irradiances more efficiently for carbon uptake. Cell division was dependent on the incubation irradiance for all but one microalga examined. The dependence of division rates on irradiance was however much smaller than for carbon uptake, suggesting that cell division buffers the influence of short term variations of irradiance on cellular metabolism.     

Parallel ecological diversification in Antarctic notothenioid fishes as evidence for adaptive radiation

Antarctic notothenioid fishes represent a rare example of a marine species flock. They evolved special adaptations to the extreme environment of the Southern Ocean including antifreeze glycoproteins. Although lacking a swim bladder, notothenioids have diversified from their benthic ancestor into a wide array of water column niches, such as epibenthic, semipelagic, cryopelagic and pelagic habitats. Applying stable carbon (C) and nitrogen (N) isotope analyses to gain information on feeding ecology and foraging habitats, we tested whether ecological diversification along the benthic–pelagic axis followed a single directional trend in notothenioids, or whether it evolved independently in several lineages. Population samples of 25 different notothenioid species were collected around the Antarctic Peninsula, the South Orkneys and the South Sandwich Islands. The C and N stable isotope signatures span a broad range (mean δ¹³C and δ¹⁵N values between ?25.4‰ and ?21.9‰ and between 8.5‰ and 13.8‰, respectively), and pairwise niche overlap between four notothenioid families was highly significant. Analysis of isotopic disparity‐through‐time on the basis of Bayesian inference and maximum‐likelihood phylogenies, performed on a concatenated mitochondrial (cyt b) and nuclear gene (myh6, Ptr and tbr1) data set (3148 bp), showed that ecological diversification into overlapping feeding niches has occurred multiple times in parallel in different notothenioid families. This convergent diversification in habitat and trophic ecology is a sign of interspecific competition and characteristic for adaptive radiations.     

Distribution patterns of benthic microalgal standing stock at McMurdo Sound,Antarctica

Summary During the austral summer of 1975–76 and winter of 1977 benthic and water column chlorophyll a and phaeopigments were measured at several sites along the east and west sides of McMurdo Sound, Antarctica. Estimates of in situ primary productivity were made at some McMurdo Sound locations. Additionally, water column samples were collected at 5 stations in the Ross Sea during January, 1976. Standing stock data are analyzed to identify seasonal and spatial patterns. Variability in algal standing stock was related to ambient light levels and appeared to be mediated by ice and snow cover whereby the highest algal standing stock was present under high light conditions (low ice and snow cover, shallow water, summer). Differences in published benthic invertebrate densities appear to be closely allied to differences in benthic primary production, and less so to in situ planktonic ice microalgal production.     

Contribution of sea ice microbial production to Antarctic benthic communities is driven by sea ice dynamics and composition of functional guilds

Organic matter produced by the sea ice microbial community (SIMCo) is an important link between sea ice dynamics and secondary production in near‐shore food webs of Antarctica. Sea ice conditions in McMurdo Sound were quantified from time series of MODIS satellite images for Sept. 1 through Feb. 28 of 2007–2015. A predictable sea ice persistence gradient along the length of the Sound and evidence for a distinct change in sea ice dynamics in 2011 were observed. We used stable isotope analysis (δ¹³C and δ¹⁵N) of SIMCo, suspended particulate organic matter (SPOM) and shallow water (10–20 m) macroinvertebrates to reveal patterns in trophic structure of, and incorporation of organic matter from SIMCo into, benthic communities at eight sites distributed along the sea ice persistence gradient. Mass‐balance analysis revealed distinct trophic architecture among communities and large fluxes of SIMCo into the near‐shore food web, with the estimates ranging from 2 to 84% of organic matter derived from SIMCo for individual species. Analysis of patterns in density, and biomass of macroinvertebrate communities among sites allowed us to model net incorporation of organic matter from SIMCo, in terms of biomass per unit area (g/m²), into benthic communities. Here, organic matter derived from SIMCo supported 39 to 71 per cent of total biomass. Furthermore, for six species, we observed declines in contribution of SIMCo between years with persistent sea ice (2008–2009) and years with extensive sea ice breakout (2012–2015). Our data demonstrate the vital role of SIMCo in ecosystem function in Antarctica and strong linkages between sea ice dynamics and near‐shore secondary productivity. These results have important implications for our understanding of how benthic communities will respond to changes in sea ice dynamics associated with climate change and highlight the important role of shallow water macroinvertebrate communities as sentinels of change for the Antarctic marine ecosystem.     

Comparative retinal anatomy in four species of elasmobranch

Using both light and transmission electron microscopy, we examined the retinal anatomy of four elasmobranch species with differing ecologies: the bull shark Carcharhinus leucas, Port Jackson shark Heterodontus portusjacksoni, epaulette shark Hemiscyllium ocellatum and pink whipray Himantura fai. Their retinas are typical of other vertebrates, having three nuclear and two synaptic layers, but are characterised by very large horizontal cells, low densities of ganglion cells (many of which are displaced to the inner nuclear and inner plexiform layers) and the presence of numerous myelinated axons within the nerve fibre layer. Carcharhinus leucas, H. fai and H. ocellatum have duplex retinas containing both rods and single cones. The peak ratio of rods to cones is much lower in C. leucas (4:1) and H. fai (3:1) compared to H. ocellatum (19:1), reflecting differences in diel activity patterns. No cones were observed in the retina of H. portusjacksoni, which is strongly nocturnal. The cones of H. fai lack a distinct myoid and their nuclei are located in a discrete layer sclerad to the external limiting membrane (ELM), whereas those of C. leucas and H. ocellatum have an obvious myoid, and their nuclei are located vitread to the ELM. No double/twin cones were observed in any species. Incorporating data from other studies, there is a clear correlation between rod outer segment volume and visual ecology in elasmobranchs, with smaller volumes found in partly diurnal pelagic species and larger volumes in benthic nocturnal species. This trend may reflect fundamental differences in visual temporal resolution between active and more sedentary species. J. Morphol., 2012. © 2011 Wiley Periodicals, Inc.     

半滑舌鳎仔、稚鱼视网膜结构与视觉特性

对1-50d半滑舌鳎仔、稚鱼视网膜和全长50mm的半滑舌鳎幼鱼视网膜结构和视觉特性进行了研究。结果表明:(1)3d仔鱼色素层形成,15d仔鱼没有显著的视网膜运动反应,25d时具有正常感受自然光的明视功能,43d半滑舌鳎稚鱼适应自然光的功能丧失;(2)半滑舌鳎仔鱼阶段感受细胞主要为高密度的单锥,视杆细胞和双锥细胞出现的较晚;单锥融合成双锥时,由于半滑舌鳎视锥细胞椭圆体细长,融合程度较差,尽管在视网膜横切面上能够看到双锥,但在切向切面上仍呈现单锥排列方式;随其生长发育,视锥和神经节细胞密度降低,视杆细胞密度增加,31d后视杆细胞数量显著增加;同时,外核层细胞核与神经节细胞的比值增大,网络会聚程度提高;相关数据表明,20-31d是视网膜结构和视觉特性发生明显变化的过渡时期,这是与半滑舌鳎从浮游生活到底栖生活生态环境的变化相适应的;(3)半滑舌鳎内核层结构特殊,50mm时只有1层水平细胞,属感光系统不发达类型,双极细胞和无长突细胞共4-5层,但不可分辨;内核层细胞层数的减少,基本上没有分化的水平细胞、双极细胞和无长突细胞,说明半滑舌鳎视网膜的光敏感性不高;(4)半滑舌鳎仔鱼浮游生活阶段视敏度较高,视觉在捕食行为中具有重要意义;底栖生活后,视敏度和光敏感性都较差,视觉在捕食行为中不可能具有重要作用     

Spectral sensitivity of mollies: comparing surface- and cave-dwelling Atlantic mollies, Poecilia mexicana

The visual pigments of cones and rods in three species of mollies, Poecilia mexicana , Poecilia latipinna and their asexual hybrid Poecilia formosa , were examined using microspectrophotometry. In P. mexicana , populations from extreme photic habitats were used: one population originated from a clear water habitat, one from a milky water habitat and another from a completely dark cave. Ultraviolet-sensitive cones were found in all species. Differences in the λ_max values of the visual pigments were small between species and among the three P. mexicana populations, but dark-reared cave fishes showed appreciably higher variance. The hybrid species P. formosa showed a highly variable long wavelength cone absorbance, ranging from 528·9 to 598·5 nm, suggesting multiple opsin expression or chromophore mixing.     

Buoyancy of sub-Antarctic notothenioids including the sister lineage of all other notothenioids (Bovichtidae)

The radiation of notothenioid fishes (Perciformes) in Antarctic waters was likely the result of an absence of competition in the isolated Antarctic waters and key traits such as the production of antifreeze glycoprotein and buoyancy modifications. Although notothenioids lack a swim bladder, the buoyancy of Antarctic species, ranging from neutrally buoyant to relatively heavy, corresponds to diverse life styles. The buoyancy of South American notothenioids has not been studied. Static buoyancy was measured in adult notothenioids (n = 263, from six species of the sub-order Notothenioidei, families Bovichtidae, Eleginopidae, Nototheniidae, and Harpagiferidae) from the Beagle Channel. Measurements were expressed as percentage buoyancy (%B). Buoyancy ranged from 3.88 to 6.96% (median, 4.0–6.7%), and therefore, all species could be considered benthic consistent with previous studies that found that neutral buoyancy in notothenioids is rare. Harpagifer bispinis, Patagonotothen cornucola, and Cottoperca gobio were significantly less buoyant than Paranotothenia magellanica. The buoyancy values of most species were concordant with known habitat preferences. These data, especially the data of C. gobio (sister lineage of all other nototehnioids) and E. maclovinus (sister lineage of the Antarctic clade of notothenioids), could be useful for understanding the diversification of this feature during the notothenioid radiation.     

Anchor ice and benthic disturbance in shallow Antarctic waters: interspecific variation in initiation and propagation of ice crystals

Sea ice typically forms at the ocean's surface, but given a source of supercooled water, an unusual form of ice--anchor ice--can grow on objects in the water column or at the seafloor. For several decades, ecologists have considered anchor ice to be an important agent of disturbance in the shallow-water benthic communities of McMurdo Sound, Antarctica, and potentially elsewhere in polar seas. Divers have documented anchor ice in the McMurdo communities, and its presence coincides with reduced abundance of the sponge Homaxinella balfourensis, which provides habitat for a diverse assemblage of benthic organisms. However, the mechanism of this disturbance has not been explored. Here we show interspecific differences in anchor-ice formation and propagation characteristics for Antarctic benthic organisms. The sponges H. balfourensis and Suberites caminatus show increased incidence of formation and accelerated spread of ice crystals compared to urchins and sea stars. Anchor ice also forms readily on sediments, from which it can grow and adhere to organisms. Our results are consistent with, and provide a potential first step toward, an explanation for disturbance patterns observed in shallow polar benthic communities. Interspecific differences in ice formation raise questions about how surface tissue characteristics such as surface area, rugosity, and mucus coating affect ice formation on invertebrates.     

Recruitment of Antarctic marine eukaryotes onto artificial surfaces

Activities related to Antarctic research stations have caused significant local impacts on the marine environment, potentially affecting the recruitment of benthic invertebrates. Herein, we report the community structure of recruiting marine eukaryotes onto artificial substrata using molecular techniques. Slides were deployed at three sites adjacent to McMurdo Station, Scott Base, and Cape Armitage in McMurdo Sound. Denaturing gradient gel electrophoresis (DGGE) analysis revealed complex and diverse eukaryotic communities had established on artificial surfaces deployed at a range of site and depth regimes after 12 months. Analysis of similarity results detected significantly greater variability in community profiles among sites than within sites. The nonmetric multidimensional scaling plot constructed from DGGE banding patterns revealed different benthic communities had established at 12 and 18 m depths. Despite this, the variation in community composition was greater among sites than between depths, especially at Cape Armitage and Scott Base. Sequence analysis of excised DGGE bands revealed a predominance of arthropod and dinoflagellate sequences at Cape Armitage. In contrast, a wide diversity of phyla including cnidaria, bryozoa, protozoa, dinoflagellates, arthropods, platyhelminths, and annelids were present adjacent to the two research stations. The abundance of diatoms detected in Cape Armitage benthic assemblages exceeded the abundance of diatoms from McMurdo Station and Scott Base by almost two orders of magnitude. The discovery that distinct eukaryotic communities recruit at different sites and depths is probably due to complex interactions between multiple factors including water quality, larval supply, and light. The detection of sessile phyla on slides at each of the sites indicates that the pollution profiles present at each site is not an impediment to successful recruitment of these species.     

Pleuragramma antarcticum (Pisces,Nototheniidae) as food for other fishes in McMurdo Sound,Antarctica

Summary Nine spcies of notothenioid fishes were captured near the southern limit of their range in ice covered McMurdo Sound, Antarctica. Stomach contents were examined using an occurrence method. Fishes were present in the diets of 8 of 9 species;Dissostichus mawsoni andGymnodraco acuticeps were predominantly piscivorous.Pleuragramma antarcticum was the most common prey fish consumed, being present in stomachs of 4 of 8 species.Pleuragramma was also partially piscivorous (22%) as well as cannibalistic (13%). As evidenced by their presence in the stomach contents of other fishes, all life history stages from 20 mm SL postlarvae to 160 mm SL adultPleuragramma were represented under the ice of the Sound.Pleuragramma was also a major food item for Weddell seals, birds and possibly invertebrates. As a widely distributed species in the pelagic zone,Pleuragramma may be an ecological substitute for euphausiids in the food web of the Sound.