Winter is Coming: Marine Intertidal Edition

 
Ice in the intertidal of Great Bay Estuary, NH in February 2013.  Photo credit: Jaimie Wolf

Ice in the intertidal of Great Bay Estuary, NH in February 2013.  Photo credit: Jaimie Wolf

 

The interface between land and ocean, known as the intertidal zone, is a harsh environment during the best of times.  As winter approaches, another challenge is added to the mix.  ICE.

Freezing in the Intertidal Zone

Along the shore line, freezing is a common occurrence during winter.  This freezing occurs in two forms: superficial freezing as the tide goes out, and melting as the time comes in; or the development of semi-permanent ice sheets, anchoring onto the shore in the supralittoral zone (the part of the intertidal zone that is only submerged at extreme high tides).  In the arctic and temperate zones of the northern hemisphere, freezing and ice formation is a regular yearly event.

Most intertidal organisms are ectothermic invertebrates.  This means that they don’t have the ability to regulate and maintain their internal body temperature like mammals do.  This difference is significant.  Humans, for example, maintain internal body temperature around 96 °F no matter if it is 110 °F our 20 °F outside.  Ectotherms, however, conform to the temperature of their surroundings; as temperatures drop, their metabolism decreases and they risk freezing.

A sea star caught frozen in the intertidal ice in Rhode Island.  Photo credit: Keryn Gedan

A sea star caught frozen in the intertidal ice in Rhode Island.  Photo credit: Keryn Gedan

So how do intertidal organisms cope with cold temperatures and freezing?

Most mobile organisms (such as crabs and snails) simply move out of the intertidal zone and into the ocean.  But what about all those organisms that can’t pick up and leave camp?  Surprisingly, the strategies used by invertebrates are not all that different to those used by trees (see Alena’s recent post on adaptations of trees to winter).

Senescence and Dormancy.  Just like many perennial and woody plants will die back over the winter, many sessile invertebrates (e.g. hydroids and bryozoans) will die back to a small overwintering form and wait for warmer temperatures to begin growing all over again.

A clump of blue mussels, Mytilus edulis, and a predatory dogwelk, Nucella lapillus.  Both of these organisms are found in the intertidal and display varying degrees of resistance/tolerance to freezing.  Photo credit: Sara Edquist  

A clump of blue mussels, Mytilus edulis, and a predatory dogwelk, Nucella lapillus.  Both of these organisms are found in the intertidal and display varying degrees of resistance/tolerance to freezing.  Photo credit: Sara Edquist
 

Resistance.  Similar to artic fish, some limpets (Patinigera polaris) and mussels (Mytilus edulis) generate an “anti-freeze” molecule that increases the range of temperatures they can tolerate by significantly reducing the temperature required to freeze their internal fluids (just like the anti-freeze in your car).  (See also Claire's post on a similar mechanism in salad greens.)

Tolerance.  Other species, such as barnacles, snails, and mussels develop mechanisms to tolerate freezing.  Some species, similar to what trees do, dehydrate their cells by shunting water from inside to outside their cells (learn how trees do it).  This decreases the chances of freezing occurring within the cells and bursting or otherwise damaging the cells.  Organisms such as the blue mussel Mytilus edulis, take this one step further and generate extracellular proteins that induce ice formation outside of the cells.  Some species can tolerate up to 80% of their tissues freezing due to this dehydration strategy!  Can you imagine being 80% frozen, thawing out, and continuing on with normal activity?!

Most of these strategies are used only in adult invertebrates.  Most invertebrate larvae are much more sensitive to harsh environmental conditions.  This is why most organisms reproduce during the spring and summer months, which allows their larvae time to hatch and develop during milder times before the onslaught of winter.

One intertidal organism displays an entirely different approach: the acorn barnacle, Semibalanus balanoides.

Acorn barnacles filter feeding under water.  Photo credit: wikimedia commons

Acorn barnacles filter feeding under water.  Photo credit: wikimedia commons

Acorn barnacle, Semibalanus balanoides, cemented to rock.  Photo credit: wikimedia commons

Acorn barnacle, Semibalanus balanoides, cemented to rock.  Photo credit: wikimedia commons

Adult barnacles encased in ice in Rhode Island.  Photo credit: Keryn Gerand

Adult barnacles encased in ice in Rhode Island.  Photo credit: Keryn Gerand

New settled and metamorphosed Semibalanus balanoides cyprid larvae.  Photo credit: Marinelarvae.org

New settled and metamorphosed Semibalanus balanoides cyprid larvae.  Photo credit: Marinelarvae.org

The adult acorn barnacle is a sessile organism found in the high intertidal in arctic and temperature North America and Great Britain, where freezing and ice is common during the winter.  The barnacle displays many of same tolerances to freezing as other intertidal organisms, as described above.  Unlike most other intertidal invertebrates, including other barnacle species, Semibalanus balanoides reproduces during the winter.  Their larvae are found swimming in the water column from January to March.  In the water, they are insulated from the threat of ice and freezing, but eventually they must settle on the hard rock substrate and metamorphose into adult barnacles.  At this late stage of their development the barnacle larvae are at risk for being frozen in ice.  And in fact they are often found frozen in blocks of ice collected from the shore.

Is freezing in a block of ice the kiss of death for these young barnacles? 

Semibalanus balanoides cyprid larvae frozen in ice collected from the intertidal zone during in southern New England.  Photo credit: Jesús Pineda

Semibalanus balanoides cyprid larvae frozen in ice collected from the intertidal zone during in southern New England.  Photo credit: Jesús Pineda

As is turns out, no!  Not only can some larvae survive being frozen, but they can continue their development into adult barnacles, with no apparent ill effects!  After two weeks of being frozen in a block of ice, up to 70% of the thawed larvae were active, would settle, and metamorphose.  When compared to larvae of the same age that were not frozen there was: NO difference in the survival to settlement, NO difference in successful metamorphosis, NO difference in the time it took the larvae to metamorphose, NO difference in the growth rate of the young barnacle, NO difference in the reproductive abilities after maturation.

The ramifications of this incredible adaptation for the barnacle population are huge.  Let’s consider just a few possibilities:

1.  Tolerance of Ice:  These barnacles have evolved a mechanism to allow their young to survive some of the harshest conditions. 

2.  Refuge from predators:  Larval survival may be increased because there are fewer predators actively feeding during the winter.  Not only does that mean that more larvae may survive their time in the water column, but they may also have more time to grow large before the mobile predators return to the intertidal zone when the waters warm again.

3.  Decreased competition:  Hard surfaces can be a limited commodity.  Many organisms rely on finding a hard surface on which to settle and live.  By reproducing in the winter, before most other organisms, these larval barnacles may encounter less competition for space, and thus increased survival to adulthood.

But beyond all of this, consider how fragile the young of any species are.  Consider how important early development can be for adult success for many organisms.  These barnacles have evolved a strategy to increase the hardiness of their young, and likely increase the success of the whole population.

References:

Aarset, Arne Vollan. "Freezing tolerance in intertidal invertebrates (a review)." Comparative Biochemistry and Physiology Part A: Physiology 73.4 (1982): 571-580.

Crisp, D. J., J. Davenport, and P. A. Gabbott. "Freezing tolerance in Balanus balanoides." Comparative Biochemistry and Physiology Part A: Physiology 57.3 (1977): 359-361.

Johnston, I. A., and A. Clarke. "Cold Adaptation in Marine Organisms [and Discussion]." Philosophical Transactions of the Royal Society of London. B, Biological Sciences 326.1237 (1990): 655-667.

Pineda, Jesús, Claudio DiBacco, and Victoria R. Starczak. "Barnacle larvae in ice: survival, reproduction, and time to post settlement metamorphosis." (2005).

 

Resources:

See great images of Semibalanus balanoides and read the original scientific research on cyprid larval freezing tolerance:  http://science.whoi.edu/labs/pinedalab/Subpages/larvaeinice.html


To explore more cold adaptations, see other posts in our "Winter is Coming" series:

Helen's Catchin Cabin Fever

Kenny's Microbe Edition

Claire's Salad Greens Edition

Alena's Tree Edition

To learn more about the intertidal zone see also:

Sara's History of the NH Rocky Intertidal

Sabah's Look in a NH Tide Pool