Current Research

Physiological Tolerances of an Invasive Clam

Broad physiological tolerances are known to be a factor in the ability of organisms to successfully invade new environments. Nuttallia obscurata is a recent invader from the western Pacific Ocean to the eastern Pacific and has quickly become one of the dominant bivalves in the intertidal sands of Oregon to British Columbia.  It is now found throughout the Strait of Georgia and into Puget Sound, and has reached densities of over 800 per m2.  Members of my lab (Rachel Allee and Zach Siegrist) are exploring physiological tolerances of this clam, and comparing them to other local (both native and non-native) bivalves.  We are focusing on tolerance to elevated temperature, low salinity, and anoxia.

We have found that N. obscurata has remarkably broad tolerances, especially to salinity, which may explain part of its ability to quickly colonize new habitats.  Using ciliary activity of gill tissue as an assay for tolerance, we found that tissue excised from N. obscurata and placed into flasks containing water of varying salinities showed no diminishment of ciliary activity after 24 hours, even at salinities as low as 1‰.  Furthermore, the gill tissue was capable of surviving at these extremely low salinities for several weeks.  This is in stark contrast to other local bivalves whose tissues quickly succumb at 10-20‰.  Our data suggest N. obscurata may have some of the broadest tolerances known for bivalves, making it an interesting model for studying both hypoosmotic and hyperosmotic adaptations.  This becomes particularly important as we try to understand how it may spread in Pacific Northwest habitats.


Phenotypic and Developmental Plasticity of Whelks in Response to Predators and Conspecifics

The whelk, Nucella lamellosa, is known for its phenotypic plasticity in the presence of predators.  Its ability to alter its shell morphology, in a matter of weeks, is well documented.  For example, in the presence of crabs N. lamellosa thickens the lip of its shell, reduces the size of its shell aperture, and forms small apertural teeth.  All of these responses make the shell thicker and less vulnerable to crab predation.
 
In collaboration with Dr. Ben Miner (WWU Biology Department), I am broadening our understanding of the ecology and evolution of this response by exploring the effects of seastar predators on adult snails and by investigating the metabolic and behavioral responses of these whelks to crabs.  We are also investigating developmental plasticity of Nucella embryos to crab and isopod predators.  Nucella encapsulates its embryos and the snails complete their entire development within the confines of tough capsules. We have shown that both predators delay the time to hatching in these marine snails.  This result is similar to data from amphibians and indicates that switching the timing of metamorphosis and hatching is an adaptation found in a wide variety of animals.  In a related experiment, we also found that the presence of adult conspecifics accelerated time to hatching.  Thus, these snails respond to multiple cues when hatching.  These results are especially interesting in that they are the first from a marine snail, a taxa ripe for investigation into this phenomenon given the variety of reproductive strategies involving egg masses.


Energetic Implications of Living in a Wave-swept Habitat  

Living in a wave-swept habitat is known to cause morphological changes in the organisms inhabiting this environment.  Work in my lab over the past few years has focused on the energetics of living in the wave-swept intertidal zone.  We hypothesize that exposure to hydrodynamic forces is metabolically expensive for animals since they must expend energy to resist being dislodged from the substratum.  This hypothesis was confirmed by work that I did in Dr. Harry Taylor’s lab at the University of Canterbury, Christchurch, New Zealand.  We completed a short study on the metabolic effects of wave forces on the abalone Haliotis iris.  We found that force had little effect on abalone heart rate, but significantly affected muscle (EMG) activity.  There was little EMG activity when no force was applied, but EMG activity significantly increased with increases in force at both low and high forces.  Oxygen consumption increased 10-20% with moderate force application and remained elevated throughout a five hour recovery period.

However, subsequent work in my lab indicates that living with hydrodynamic forces may not always be energetically expensive.  A recent grad student found that simulated wave force has no statistical effect on the aerobic metabolism of the keyhole limpet Diodora aspera, although there was a slight trend in which oxygen consumption increased from the resting rate when wave force commenced.  This indicates that living in a wave-swept environment is not as metabolically taxing as we had hypothesized, and that D. aspera may derive a metabolic benefit from living there by relying on water flow to enhance its respiratory gas exchange.  The cost of adhesion during wave exposure may be offset by the increased oxygen availability and an increase in aerobic metabolism, giving D. aspera more capacity for growth and reproduction.

Four grad students working in my lab, Chris May, Mike Thimgan, Scott Cowan, and Jonathan Robinson have investigated different aspects of this project.


Prior Research

Energetics of Gastropod Swimming
 There are three general forms of swimming in gastropods: parapodial flapping, lateral bending, and dorso-ventral undulating.  These experiments started when one of my Masters students, Sandra Caldwell, investigated the energetics of lateral bending in the Lion Nudibranch Melibe leonina.  More recently, with Dr. Tom Carefoot and Dr. Steve Pennings, I have investigated the energy expended during parapodial flapping and compared it to energy expended during crawling in the sea hare Aplysia brasiliana.  We found that although swimming and crawling require similar amounts of aerobic energy, swimming cost of transport is much lower than crawling cost of transport probably due to the fast, directional nature of swimming in this species.  During prolonged swimming bouts, A. brasiliana decreased parapodial beat frequency by approximately 10% after 4 h while swimming velocity decreased by 30%.  This demonstrates a loss of flapping efficiency with prolonged swimming and we observed that the parapodia did not overlap as completely during a stroke as the animals tired.  

I have also investigated dorso-ventral undulation in the nudibranch Tritonia diomedea with Beth Moore, a former WWU undergraduate and REU student at Shannon Point Marine Center.  In this case, we videotaped swimming animals and found that the number of body flexions per swim bout was dependent upon animal size, with smaller animals completing significantly more flexions per swim bout. The rate at which T. diomedea flexes its body was also dependent upon animal size, with smaller animals showing a faster flexion rate. Larger animals exhibited significantly farther distances traveled per individual flexion. Total swim time (49 ± 8 sec) was independent of animal size.

Swimming of Epibiont-encrusted scallops

Two local species of scallops, Chlamys hastata and Chlamys rubida, are regularly found heavily encrusted with the sponges Mycale adhaerens and Myxilla incrustans.  It is thought that this relationship is a mutualism since both scallops and sponges are less vulnerable to predation when they coexist.  However, the energetic implications of carrying sponges while the scallops are swimming are unknown.  Scallops are also found encrusted by balanoid barnacles, which are potentially more detrimental than sponges.  We investigated the impacts of sponge and barnacle epibionts on scallop swimming by 1) videotaping scallops swimming with and without epibiont encrustation to determine whether epibionts affect the distance the  scallops are able to swim, 2) measuring oxygen uptake to determine aerobic energy expenditure while swimming with and without epibiont encrustation, 3) measuring anaerobic metabolite buildup after swimming with and without epibiont encrustation to determine anaerobic energy expenditure during swimming, 4) determining morphological changes in shell dimensions and muscle mass with increased scallop size and epibiont encrustation, and 5) measuring the drag experienced by scallops encrusted with different epibionts.  Briefly, we found that 1) there were no apparent changes in swimming behavior with sponges although other animals (especially barnacles) have dramatic effects, decreasing the distance and height of swimming, 2) there were no differences in aerobic energy expenditure when scallops swam with and without sponge and barnacle encrustation, 3) scallops swimming with sponges produced the same amount of anaerobic metabolites as scallops swimming without sponges, but barnacle encrustation increased anaerobic energy expenditure, 4) scallop morphometry is not affected by epibiont encrustation but Chlamys do show intraspecific ontogenetic changes similar to other scallop species, and 5) sponge encrustation does not alter the drag experienced by swimming scallops but other epibionts such as barnacles and bryozoans do.  Thus, sponges do not appear to affect the swimming capability of scallops but barnacles increase drag, increase anaerobic energy expenditure, and decrease swimming distance and height.  This work was conducted with Dr. Brian Bingham at the Shannon Point Marine Center.
 

Swimming in the file shell Limaria fragilis

Swimming has been developed in only a few orders of Bivalves, including scallops (Pectinidae) and file shells (Family Limidae).  The mechanics and energetics of scallop swimming have been well studied.  Scallops exhibit a range of swimming abilities, from short-burst, "zig-zag" swimmers such as Chlamys to long-range, gliding swimmers such as Amusium and Placopecten.  Swimming ability in scallops is related to shell morphometry and the ability to produce power, and these vary amongst scallop species.  These also change intraspecifically with size since scallops must produce proportionately more power as they grow to compensate for increased mass.  For example, shells of long-swimming pectinids are comparatively thin  and relative thinning of the shell occurs as these scallops grow, making lift easier to generate with increasing mass.  As well, shell width is usually positively allometric with shell height in swimming pectinids (that is, shells become relatively broader as scallops grow), which increases the aspect ratio and makes swimming more efficient by decreasing drag.  Muscle mass is also positively allometric with shell height, increasing the relative power that can be generated by larger scallops.  In all scallops, swimming lasts a relatively short time (a few minutes) and is powered, to a large degree, anaerobically.  Scallops swim to escape predation, to position themselves in better habitat, and to migrate.
    
Swimming in Limidae is less well understood.  File shells, like scallops, swim by quickly adducting their valves and producing posterior propulsive jets of water.  This causes them to swim with their hinge hindmost.  The energetics of swimming in file shells have been well characterized.  Limaria fragilis is capable of swimming for extended periods (several minutes) and swimming is mostly aerobic, but with a substantial anaerobic contribution from arginine phosphate, octopine dehydrogenase, and ATP stores.  Their cost of transport is substantially higher than in other swimming invertebrates, possibly due to the cost of carrying a shell, no matter how light, and to swimming with the extensive mantle tentacles protruding into the water.  File shells typically have long tentacles that extend from the mantle and can not be withdrawn into the shell.  During swimming, these tentacles are capable of producing thrust by participating in a rowing motion and the thin shell is thought to decrease the sinking rate of the animal when it stops valve-clapping.
   
More recently, the behavior, morphometry and mechanics of swimming in Limaria fragilis were characterized and compared to the better understood scallops.  Absolute swimming speed (cm sec-1) increased linearly with increasing shell height, although relative swimming speed (body lengths sec-1) was independent of shell height.  The increase in absolute swimming speed was due to an increase in the distance covered during each valve clap as clap distance (cm clap-1) also increased linearly with shell height while clapping frequency (claps sec-1) was independent of animal size.  Limaria fragilis displayed a variety of morphological changes related to size.  Shell length was negatively allometric with shell height indicating the shell became proportionately slimmer in larger animals.  Dry shell mass was negatively allometric with shell height, while both dry adductor muscle mass and dry mantle + tentacle mass were positively allometric.  Autotomy of mantle tentacles significantly decreased clap distance by 13% without affecting clapping frequency or swimming speed.

These studies were conducted at Heron Island Research Station on Australia's Great Barrier Reef with Dr. John Baldwin and Dr. John Elias.


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