Limpets, littorines, barnacles, and mussels are common representatives of mid- to high-intertidal regions on the west coast and, of these, limpets are often found as high or higher than any other invertebrates.  Physical factors affecting their survival include desiccation, insolation, and wave impact. 

Topics relating to "life in the intertidal zone" for limpets include zonation & critical tide factors and temperature stress, considered here, and DESICCATION and WAVE FORCES found in other sections.

Early ideas about factors that influence zonation of limpets and other intertidal organisms, include regulation at the lower limits of distribution by competition for space and food, and regulation at the upper limits by biological factors, including uppermost distribution of algal foods, and physical factors, most notably, desiccation.  The idea of desiccation being important in delimiting distributions of limpets comes from an observation in Sunset Bay, Oregon that upper limits of distribution of 4 limpet species, Acmaea mitra, Lottia digitalis, L. scutum, and L. pelta are in close agreement with two critical tide levels, namely, LHHW  (lowest higher high water) and LHLW (lowest higher low water; see diagram on Left). The topic of zonation¹ of west-coast invertebrates is outside of the intended scope of the ODYSSEY, but perhaps a brief reference to critical tide levels is necessary before further discussing limpet distributions. 

The diagram above Right shows a typical day’s tidal pattern for the west coast, but with levels calculated for Sunset Bay, Oregon on a day in 1947. Note the semidiurnal pattern, with 2 high tides and 2 low tides, and mixed, that is, of unequal heights.  The critical levels for this 24-h tidal cycle are shown (HLW, HHW, LLW, and LHW).

If we now change this to a lunar day, which is approximately 28d in duration, we see the same pattern of tides and can identify 4 mean tidal levels as shown in the previous schematic - namely, MHLW (mean higher low water), MHHW, MLLW², and MLHW and the component tides that make up these means (only MLLW is indicated in the schematic).  With a bit of noodling the terminology will become clear.  The MHHW level, for example, includes the highest tide level of the month, namely, HHHW³ (highest higher high water) and also all the other daily HHW tides of the month, down to the LHHW.  The HHHW level, or the highest spring tide of the month, is thought to be critical because above this level an organism will theoretically not be wetted at all during a given lunar day (excluding waves and spray). 

Now, how does this relate to the Sunset Bay limpet species? LHHW is one of the critical tide levels designated for the Sunset Bay limpets, as it represents the highest level at which a limpet will be wetted on every day of the month, and this appears to set the upper limit of distribution for L. scutum and L. pelta, and also partially for L. digitalis.  Another level, thought to be critical for A. mitra, is LHLW, the level at which a limpet will normally be emersed for at least a few minutes each lunar day; however, at summer solstice when high tides in Oregon are generally lower than at other times of the year, the highest tide of the day will fail to reach it.  During a summer spring tide this exposure could be lethal. 

Does the concept of critical tide levels really really help explain distributional limits of limpets and other intertidal organisms?  Yes, but only when considered in the fullest context of all other physical and biological factors that may be operating at a particular time in a given area.  On the specific rocks at Sunset Bay inhabited by the limpets during the specific period of study (not specified in the paper, but probably summer), the author records a certain distributional pattern.  These distributions, however, are certain to be different in other nearby areas, ones with differing microhabitat conditions, including aspect to the sun, slope, food availability, and so on.  Such factors, in their myriad diversity, form the research basis for many hundreds of papers cited in the ODYSSEY. Shotwell 1950 Ecology 31: 647; charts of critical tide levels for Sunset Bay, Oregon adapted from Doty 1946 Ecology 27: 315.

NOTE¹  for a review of some of the older zonation references (up to 1975) see Carefoot 1977 Pacific Seashores Univ Wash Press, Seattle

NOTE²  MLLW (mean lower low water) represents Chart Datum or zero tide level on the U.S. system

NOTE³  this tide and LLLW are the spring tides of each month, when moon and sun are in alignment.  They are, respectively, the highest high tide of the month and the lowest low tide of the month.  In between are the monthly neap tides, when moon and sun are out of alignment, and these include the highest low tide of the month, HHLW, and the lowest high tide of the month, LLHW

Zonation on rocky shores in Barkely Sound, British Columbia

Not surprisingly, the intertidal height occupied by an organism has a significant effect on physiological rate.  This is shown in Lottia limatula collected from 2 intertidal levels (+1m vs. permanently submerged low-intertidal tidepools) at Palos Verdes, California.  Note in the accompanying graph that heart rates are consistently higher in the low-intertidal individuals regardless of experimental temperature.  Individuals reciprocally transferred to “opposite” intertidal heights exhibit rate-reversals within 4wk.  The authors conclude that temperature acclimatisation is the major factor influencing heart-rate differences in the high- and low-level limpets.  Segal et al. 1953 Nature 172: 1108. Photograph courtesy Scripps Institution of Oceanography, La Jolla, California.

NOTE  also included in the study is similar work on mussels Mytilus californianus, not included here

NOTE  counted by eye through a hole cut in the shell over the heart. The authors have plotted their data on heart-beat frequency and body mass on a log-log plot, but have selected to show the relationship in curvilinear form. Expectation from scaling prediction is that the relationship would be linear with a negative slope, so this is something that might be worth re-investigating

In a follow-up paper on Lottia limatula the same researcher expands on the effects of intertidal height on heart rate, with attention to temperature acclimation.  In the study area of Palos Verdes, California the species has a vertical distribution in the intertidal zone of about 1.5m.  At the highest levels, the limpets are air-exposed for about 50% of the time, and air temperatures in this part of the shore rise above, and fall below, those of the ocean (average sea temperature is about 7^OC).

Results show that individuals of the same live mass have lower heart rates in the high intertidal area as compared with individuals in the low intertidal zone, just as shown in Research Study 1 above.  This difference is maintained in the laboratory over a range of experimental temperatures (4-29^OC; see graph on Left). If low-level individuals are translocated to the high level, their heart rates slow so that after a month or so their rates are equivalent to those of high-level individuals at any given experimental temperature (see graph on Right; data shown here are for limpets at 4^OC, but results for experimental temperatures of 14 and 24^OC show a similar pattern).  Reciprocal transplants from high to low yield a similar pattern of results. Segal 1956 Biol Bull 111: 129.

NOTE  the author also includes information on gonad size in relation to intertidal height in L. limatula, but these data are not presented here

NOTE  the heart is exposed for viewing by trepanning a circular hole of 3-4mm diameter in the shell directly over it

In the Monterey area of California the limpets Lottia scabra and L. digitalis occupy roughly the same vertical range, from 0.5 to 3.0m above MLLW.  Our expectation would be that individuals at the high levels would tolerate temperature stress better than ones from mid- or low-intertidal levels.  Laboratory tests using slow temperature rise with immersed specimens show a tendency for this in both species, but perhaps more so for L. scabra than for L. digitalis.  The author suggests that the slightly greater tolerance for high temperature shown by L. scabra may owe to its tendency to inhabit horizontal surfaces that are affected more by sunlight than the more vertical, sometimes shady, surfaces occupied by L. digitalis.  Hardin 1969 Veliger (Suppl.) 11: 83.

NOTE  temperatures are raised by 1^OC every 5min

A study related to Research Study 2 above investigates acclimatisation to temperature in heart and respiration rates of limpets Lottia limatula collected from the Monterey Peninsula, California.  The author finds similar trends with intertidal height as noted in the earlier account, with the exception of lack of significance at 8^OC with respect to intertidal-height differences.  Other experiments on effects of starvation and acclimation show that L. limatula has the capacity to alter significantly its heart and respiration rates in face of changing environmental conditions. Markel 1974 Physiol Zool 47: 99.

NOTE  respiration data are similar in pattern to heart-rate data, and are not included here

NOTE  high-intertidal individuals are collected from the 1.5m level, while low-intertidal ones are collected from below 0.3m level

Over the past 2 decades heat-shock proteins (HSPs) have been extensively investigated in shore invertebrates.  HSPs are produced in response to high temperature and other stresses.  They function to bind to damaged proteins, thus preventing their aggregation into toxic clusters and/or degradation by cellular proteases, and to help refold them 3-dimensionally into their original functional shapes.  Their presence is generally indicative of greater tolerance to further heat, or other stress. Measurements of protein synthesis in mantle tissues of Lottia scabra and L. pelta over a range of incubatory temperatures reveal generally higher rates in the former species than the latter, with non-significant peaks in both species at about 29^OC. Note in the survivorship graph on the Right that L. scabra is much more tolerant to high temperatures than L. pelta.

Specific analyses for heat-shock proteins (HSPs) in the two species also show greater rates of synthesis of several types of HSPs by L. scabra as compared with L. pelta (data not included here).  Not only are rates of synthesis higher in L. scabra, which is subjected to more severe and variable thermal stresses than L. pelta, but L. scabra has more isoforms of, for example, HSP70 than pelta (not shown).  The authors note that while providing important comparative information on the physiological capabilities of the two species to tolerate thermal stresses, the data on rates of synthesis of HSPs provide no information on their actual intracellular concentrations. Sanders et al. 1991 Physiol Zool 64: 1471.

NOTE heat-shock proteins are considered elsewhere in the ODYSSEY: LEARN ABOUT MUSSELS: LIFE IN THE INTERTIDAL ZONE: HEAT-SHOCK PROTEINS and LEARN ABOUT ABALONES & RELATIVES: PHYSIOLOGICAL ECOLOGY: HEAT-SHOCK PROTEINS

Studies on heat-shock proteins in rocky shore marine invertebrates show that levels vary several-fold between microhabitats, intertidal zones, and seasons.  This is clearly shown in a study in Oregon where levels of expression of HSP70 (a commonly occurring type of HSP) in Lottia digitalis are significantly higher in high intertidal-level summer habitats than in mid-intertidal habitats or in winter/spring seasons, suggesting that these individuals may be experiencing the greatest thermal stress.  This work and the work of others confirm that heat-shock protein levels vary at all scales examined, including microhabitat, tidal height, site, and latitude.  In view of the sensitivity of these bioindicator molecules, the authors caution that care must be taken in assessing the scale of variation when interpreting heat-shock protein data. Halpin et al. 2002 Integ Comp Biol 42: 815.

NOTE  data for 2 habitats are presented by the authors, but only those for Strawberry-Hill habitat are presented here

Lottia scabra inhabits rocky areas of west-coast shores from mid-Baja California north to the Oregon border (see figure on Left).  At its northermost limits its abundance declines by over 100-fold over 300km distance approaching the Oregon border (see graph upper Right). What controls this decline?  Temperature is commonly implicated in the setting of poleward boundaries for a broad diversity of species, and the gradual decline in abundance shown here is suggestive of increasing physiological intolerance to some physical factor or another. 

In an attempt to answer this question for L. scabra, limpets from 2 source populations (S1 and S2) are transocated to each of 4 sites and their survival, growth, and reproductive state monitored over periods of 12-14wk.  Translocations are done in both summer and winter. The author's expectations are that survival will decrease in accordance with the density data already shown; that is, highest survival is expected at the southernmost translocation site (C1) and lowest at the northernmost site (N2).  Results show that survival is generally higher for winter translocations that for summer ones, but do not support the author's expectations (see graph lower Right). Other correlative measurements (not shown here) of air and water temperature and food supply at the translocation sites show that while these factors significantly influence survival, growth, and reproductive maturation, none explains the geographic abundance patterns.  In fact, in some cases translocated limpets are most successful at sites with the lowest natural abundances.  The study, a challenging one, is topical in its addressing of issues currently related to global warming, and is deserving of further research attention.  Gilman 2006 Oecologia 148: 270; see also Gilman 2005 J Biogeogr 32: 1583.

NOTE  the limpets are transported in cages and kept in these cages for the duration of the experiment.  To some extent this controls for biological differences of each new site (e.g., different numbers and types of predators).  Two transplants are done in 2 successive autumn/winters (Oct-Jan), and 2 are done in 2 successive spring/summers (Mar-Jul).  The author does not control for possible trauma during removal from scars and for possible increased vulnerability by the limpets being suddenly “scarless”, but the effects, if any, are the same for each new location.  The 4 locations are semi-protected outer coasts, and are similar in degree of wave exposure, beach slope, and community composition.  Limpets that die (some from handling stress) are replaced to the best extent possible to maintain consistent densities, but the deaths are not included in the survival and growth analyses

NOTE  only data for proportion surviving are shown here; data for growth and maturation are mostly not statistically significant

The temperature of an intertidal organism, such as a limpet, is controlled primarily by the rate of heat absorption from the sun, and the rates of heat loss by evaporation, convective transfer to the air, and conductive transfer to the substratum (see diagram on Left).  With a few exceptions¹, past investigations of temperature budgets of intertidal organisms have involved less-than-complete measurements over short time-frames, coupled with mathematical models that are too general.  Since the aim in such studies is to get as complete a record as possible over as long a time-frame as possible, resulting budgets have been found wanting.  What has been needed is a means to develop a heat-budget model using strictly meteorological parameters, which are comparatively easy to obtain.  This has been done, with remarkable success, for the limpet Lottia gigantea at the Hopkins Marine Station, Pacific Grove, California.  The authors record solar irradiance, wind speed, and temperatures of rock, the last using thermistors buried in thermally conducting paste in a 1mm-deep groove, and shaded air temperatures recorded 10cm above the rock every 30sec over  an 8-d period in September.  The model² is tested by comparing predicted temperatures with actual temperatures of 2 types of simulated³ limpets, and of live limpets.  Results show excellent agreement between predicted temperatures using the model and actual temperatures for all 3 objects despite, as noted by the authors, not taking into account evaporative cooling (see graphs on Right for one of the models and for live limpets). The authors comment that their model assumes that the limpet is always in thermal equilibrium with the environment which, after an appropriate test, is found to be true.   The authors note that the model, accurate to within a fraction of a degree Celsius for limpets, could readily be tweaked for organisms of different sizes, shapes, and perhaps motilities. However, they do advise caution when applying the model to larger organisms and, presumably also, to organisms that create less of a “conductive bond” with the substratum.  Finally, the authors suggest that their model could allow fine-scale resolution of differences in body temperatures of organisms with different morphologies over time and space, testing effects of thermal stress, and predicting effects of climate change on intertidal communities. Denny & Harley 2006 J Exp Biol 209: 2409.

NOTE¹  2 exceptions are heat budgets determined for the foliose red alga Mastocarpus papillatus and for the mussel Mytilus californianus

NOTE²  the model uses 29 equations with over 50 factors; evaporative cooling is not taken into account, but results of preliminary experiments suggest that its effect is likely to be minor

NOTE³  these are represented by 2 limpet-shaped objects: one, a silver-alloy cone, with a blackened exterior; the other, a shell of L. gigantea containing a silver-alloy body

In a companion article to Research Study 8 above the authors use their heat-budget model to predict lethal limits of temperature for limpets Lottia gigantea that might occur at hypothetical sites with differing aspects to the sun and differing intertidal heights.  Interestingly, input into the model of 5yr of air-temperature and wind-speed data measured on the shores around Hopkins Marine Station, Pacific Grove, California predicts no body temperatures above 37.5^oC.  This suggests that other factors such as desiccation, ecological interactions, or combinations of sublethal effects must be operating to set the species’ upper limits of distribution. By manipulating factors such as intertidal height and substratum orientation in the model, the authors show that lethal temperatures would theoretically have been experienced only 3 times in the past 5yr at sites with a variety of combinations of factors.  Even if one were “on the ground” and knew what to look for, such a combination could be easily missed in field measurements. Implicit in these observations is the requirement that data on lethal limits be known from laboratory experiments, and the authors highlight the need for more empirical data on a species’ thermal limits and effects of sublethal stress.  The authors note that a tool for predicting acute thermal stress in an intertidal species may be especially useful in a future threatened by warming air temperatures.  Denny et al. 2006 J Exp Biol 209: 2420. Photograph courtesy Jackie Sones, Bodega Marine Laboratory, California.

NOTE experimental temperatures in excess of 38^oC are shown to kill all L. gigantea (see graph)

NOTE  these include intertidal height, aspect, annual air and sea temperatures, ocean-wave heights, wind speed, and so on  

As these accounts show, limpets are popular subjects for research on thermal stresses and tolerances on rocky intertidal shores.  Investigation by a researcher at Bodega Marine Laboratory, California of a mass mortality of limpets Lottia scabra resulting from unseasonably hot temperatures in mid-March shows that even small-scale differences in orientation to the sun may be critical to survival.  The incident in question occurred in the Bodega Marine Reserve during a single mid-day exposure at low tide, with limpets facing directly to the sun being killed, but not ones on rock surfaces angled more than 45^o away from the sun.  Substratum temperatures in the limpet zone during the event ranged up to 35^oC, depending upon angle of solar incidence (see graph).  Interestingly, nearby sea mussels Mytilus californianus were not killed.  On another extremely hot day that occurred a month later the reverse occurred, with many sea mussels being killed, but not limpets.  Shore ecologists have long known that orientation of the substratum is an important factor in determining body temperature and mortality of intertidal invertebrates, and the present study shows that it may be as important as intertidal height.  Harley 2008 Mar Ecol Progr Ser 371: 37.

NOTE  air temperatures are recorded at the Laboratory, while rock-surface temperatures are recorded by miniature temperature loggers embedded in glue in shallow depressions chiseled into the rock

Investigators of thermal stresses in owl limpets Lottia gigantea  at Hopkins Marine Station, California monitor levels of heat-shock protein 70 as indicators of sublethal stress, and measure mortality rates over the same temperature range.  Peak expression of Hsp70 occurs at 32^oC, and lethal limits at 30-42^oC depending upon length of exposure and humidity (see graph upper Right for mortality data).  A comparison of these results with field surveys of distribution of owl limpets shows, as predicted from heat-budget models, that thermal stresses are highest on high-level southwesterly facing slopes and on horizontal surfaces, and lowest on low-level northerly facing slopes and on vertical surfaces (see illustration on Right), and that owl limpets are distributed accordingly.  The authors discuss the usefulness of integrating detailed physiological-performance data in computer-simulation models for predicting future climate-change-induced effects on marine communities.  Miller et al. 2009 Functional Ecol 23: 756.

NOTE  the heat-budget model used is described in Research Study 8 above