LOSER: Antarctic Notothenioid Fishes

by: Priscilla Watson-Wynn

Antarctica• Fifth largest continent• The world’s most southern

continent• Surrounded by Southern

Ocean• 98% covered in ice sheet & 2%

barren rock• Highest average elevation• Water temperatures between -1.9° - 2°C• Ice temperatures between -28°

- 3°C• Desert environment• Cold adapted organisms - cold

yet thermally stable environment

- highly stenothermal

Antarctic Circumpolar Current

• Ocean current that flows clockwise isolating Antarctica from warmer ocean temperatures

• Allowed ice to form on land and surrounding sea• This current created the Antarctic Polar Front that reinforces the extremely

cold waters that surround continent• Has allowed 30 millions years of evolutionary adaptions for cold, arid climate

Climate Change and Antarctic Peninsula- Warming 5.4 times the

global average- Waters surrounding the

West Antarctic Peninsula are warming faster than the worlds other oceans.

- have risen ~ 1°C in the past 50 years - predicted to rise another 2°C in the coming century- Changes in marine

environment becoming evident

- such as species distribution and abundance which result in community and food web shifts

Ozone hole• Largest on record• Average thickness

is about 300 Dobson units

• Increased ultraviolet light can damage DNA of Antarctic organisms especially Antarctic ice fishes

Notothenioid= Antarctic ice fishes• Belongs to

perciform suborder Notothenioidei

• Channichthyidae family with no hemoglobin

• Dominant fish fauna in terms of species and biomass

• Unique in that they are the only known vertebrate that have no circulating hemoglobin, oxygen binding protein, as adults

- many species within family also don’t express myoglobin

Notothenioid fishes and evolution• Their success in Antarctic

environment due to special blood-borne antifreeze glycoproteins

- prevents freezing of body fluids by absorbing small ice crystals and inhibiting their growth• This novel ice binding protein

found to be evolved from pancreatic trypsinogen

• There is a small sequence divergence in the two genes which tells us that transformation of the gene happened 4-15 mya which correlates to the estimated time Antarctica started freezing

Protein evolution and organismal adaptationsto environmental conditions!

Chen et al., 1997

Nototheniod fishes adaptations to colder climate

• Larger and more extensive vasculatures, greater blood volumes, larger hearts, and more numerous cardiac mitochondria compared with similar sized red blooded notothenioids

• Combination of high- throughput circulatory systems, low absolute metabolic rates, and the well oxygenated waters of Southern Ocean allow these fish to get enough oxygen

… downside• Loss of hemoglobin has resulted

in higher energetic expense to the circulatory system

• Loss of myoglobin (in some species) has resulted in decrease in cardiac performance

• Oxygen carrying capacity of ice fishes is 10% less than that of red blooded fishes

• Lost genes to cope with higher temperatures like turn on heat shock proteins

As temperatures rise…

• Warmer water holds less dissolved oxygen, thus there will be less oxygen available to ice fish with no hemoglobin

• This will result in metabolism increase creating a mismatch between oxygen supply and demand

- aka hypoxia

Thermal Tolerance of Antarctic Notothenioid Fishes Correlates with Level of Circulating Hemoglobin ( Beers,J.,Sidell,B., 2011)

• Evaluate whether thermal tolerance limits correlate with readily accessible metrics of blood oxygen- carrying capacity (e.g., hematocrit) of both white and red-blooded species

• Assess the capacity of a notothenioid species (Notothenia coriiceps) to adjust thermal limits in response to 1 week exposure at a modestly increased environmental temperature of 4°C

Methods• Five species of Antarctic notothenioid fishes from Antarctic peninsula,

April-May 2007 and 2009 - Chaenocephalus aceratus, Chionodraco rastrospinosus, Notothenia coriiceps, Gobionotothen gibberisfrons, Lepidonotothen squamifrons• Thermal tolerance experiments -Temperature was elevated acutely from ambient temperatures at a constant rate of 3.6°C h-1

- CTmax defined as the temperature where animals lost righting response (LRR)

-exposed a group of N. coriiceps at 4°C for 1 week• Drew blood from fishes to determine plasma lactate concentration• Total RNA was extracted from brain, heart, and pectoral muscle tissue

of C. rastrospinosus and N. coriiceps - measure the mRNA levels for two hypoxia-inducible genes, HIF-1α and PHD2

Results: Thermal tolerance is directly correlated with hematocrit

-N. coriiceps one week exposure to 4°C had no effect on Ctmax indicating and inability to compensate for rising temperatures, at least under experimental conditions

Figure 1

• In previous research found that hematocrit is closely correlated to the expression of hemoglobin in these species

Results: Effect of acute temperature elevation on hematocrit and plasma lactate

Figure 2

Figure 3

Results: Effect of acute temperature elevation on mRNA levels of hypoxia-inducible genesFigure 4: red- blooded

N. coriicepsFigure 5: white- blooded C. rastrospinosus

Are Antarctic ice fishes “losers” of climate change?

• Results suggest that ice fishes are sensitive to temperature changes because of their lack of hemoglobin making them very stenothermal

• Insufficient supply of oxygen to tissues that results in increase in temperature may lead to limitations in cardiovascular physiology

• Will be vulnerable to effects of global warming which may have consequences in physiological performance, geographic distribution and species survival

• will act as a canary in a coal mine for climate change