title for learn-about section on whelks & relatives in A SNAIL'S ODYSSEY
  Physiological ecology
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Temperature & light effects

  Topics in this section on physiological ecology include temperature & light effects, considered here, and TRAIL-FOLLOWING, GAS EXCHANGE, and HEAT-SHOCK PROTEINS considered in other sections.
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Research study 1

graph showing growth rates of embryos of whelks Nucella emarginata in Alaska and southern CaliforniaLatitudinal compensation for temperature is seen commonly in physiological and other studies of invertebrates. Whelks, Nucella spp., inhabit rocky shores of Alaska and southern California, and seasonal seawater temperatures are greater by 6-10oC in the southern habitats. Most scientists would predict that growth of embryos of Nucella emarginata would thus be faster in the warmer waters of the south, although not so fast as the temperature differences would suggest because of of such latitudinal compensatory adaptation. It is surprising, then, that growth measurements actually show the reverse, with rates about 9 times faster in Alaska than in southern California (see graph). The reason for the difference photograph of hatchling whelks Nucella ostrina courtesy Louis Gosselin, Thompson Rivers University, British Columbiais not known.  Dehnel 1955 Physiol Zool 28: 115. Photograph courtesy Louis Gosselin, Thompson Rivers University, British Columbia.

NOTE  we now know that the experiments were likely done on different species of Nucella: lima or ostrina in Alaska and emarginata in southern California.  Still, this is unlikely to have accounted for the large differences shown

Hatchlings of Nucella ostrina from Barkley Sound, British Columbia 50X

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Research study 2

graph showing oxygen uptake for whelks Nucella lamellosa when immersed and emersed over a temperature rangeIn Lummi Island, Washington, Nucella ostrina lives about 0.5m higher on the shore than N. lamellosa.  Both species are often openly exposed to solar irradiation and, as a result, tissue temeratures may be much higher than air temperatures. The authors note that lower humidities at higher tidal heights may aid in cooling through greater evaporative water loss.  Both species take photograph showing a single whelk Nucella ostrina foraging amongst a selection of barnacle speciesup oxygen when emersed but, as shown here for N. lamellosa, at rates about 3 to 4-fold less than when immersed (see graph). Bertness & Schneider 1976 The Veliger 19: 47. Photograph courtesy Dave Cowles, Walla Walla University, Washington www.wallawalla.edu.

NOTE  data are presented here only for large-sized N. lamellosa, but data for large-sized N. ostrina show similar differences


Nucella ostrina forages amongst prey barnacles Balanus glandula, Semibalanus cariosus, and Chthamalus dalli 1X

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Research study 3

photograph of shell-less whelks Nucella lamellosa, courtesy Koy 2007 J Shellf Res 26: 267.An unusual behaviour in whelks Nucella lamellosa is described by a researcher at Friday Harbor Laboratories, Washington.  The behaviour involves loss of the shell a few days to weeks after collection and transport to the laboratory.  The shell-less individuals crawl about and appear to exhibit normal behaviours, including, in 2 of 7 instances of shell loss out of a collection of several hundred, the drilling and eating of prey mussels and barnacles.  Although the author discusses the possibility that the autotomy is defensive, along the lines of limb loss in crustaceans or arm loss in sea stars, she acknowledges that it is more likely to be a response to stressful conditions, such as temperature or oxygen deprivation. Koy 2007 J Shellf Res 26: 267.

Two shell-less whelks
Nucella lamellosa.

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Research study 4

photograph of whelk Nucella canaliculata courtesy Linda Schroeder, Pacific Northwest Shell Club, Seattlemap showing collection sites for whelks Nucella canaliculata for study of thermal tolerancesWhat is the geographic variation in thermal limits of a marine snail?  This is investigated in whelks Nucella canaliculata from 7 similar mid-intertidal sites ranging from Oregon to central California (see map).  By rearing eggs in capsules to maturity from each of the 7 populations under standard conditions at the Bodega Marine Laboratory, California, then mating up to 28 non-sibling pairs within each population, the researchers are able to produce test hatchlings minimally influenced by potential past field-acclimatisation and other non-genetic effects. 

histogram comparing thermal tolerances of whelks Nucella canaliculata from sites in Oregon and CaliforniaResults of thermal-or lethal-tolerance (LT50) assays on the F2 progeny reveal that hatchling snails from central California are, surprisingly, less heat tolerant than conspecifics from Oregon (see histogram; capital letters indicate statistical homogeneity). The authors conclude that the differences in upper thermal limits existing among the populations of N. canaliculata are likely genetically based.  As to explanation for the differences, we have to conclude that Oregon whelks are exposed to higher potential thermal stresses than central California whelks.  Kuo & Sanford 2009 Mar Ecol Progr Ser 388: 137. Photograph courtesy Linda Schroeder, Pacific Northwest Shell Club, Seattle, Washington PNWSC.

NOTE the temperature at which 50% of the test subjects are killed

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Research study 5

Studies of temperature effects on feeding in intertidal animals are common, but it is rare for an investigation simultaneously to include rates for an organism both emersed and submersed.  Researchers at Friday Harbor Laboratories, Washington measure feeding rates of whelks Nucella photograp of whelk Nucella ostrina feeding courtesy Emily Carrington, Friday Harbor Laboratories, Washingtonostrina on barnacles Balanus glandula at different and varying temperatures.  Results show, interestingly, that while feeding and growth over a 20d experimental period are greatest at higher submersion temperatures of 13oC as compared with 11oC, they are actually lowest at higher emersion temperatures of 28oC as compared with 20oC or 12oC.  Thus, warm weather may lead to greater predation on the barnacle population, but is significantly released if air temperatures become too warm.  The authors suggest that at the highest experimental air temperatures the whelks may be so physiologically stressed that feeding becomes secondary to seeking shelter within their shells or in cooler microhabitats, or in devoting needed energy to cellular maintenance and repair.  Yamane & Gilman 2009 Mar Ecol Prog Ser 393: 27. Photograph coutesy Emily Carrington, Friday Harbor Laboratories, San Juan Island, Washington CARRINGTON LAB.

NOTE  temperature regimes imposed are in the range that the whelks normally experience during summer in San Juan Island, Washington

A whelk Nucella ostrina feeds on
a barnacle Balanus glandula 1X

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Research study 6

If you live in Alaska it’s hard to avoid freezing temperatures in winter, and even harder if you are a whelk Nucella lima living intertidally in Lynn Canal, Alaska where -0oC air temperatures are common during October-April.  Individuals in the upper part of the intertidal zone will photograph of a whelk Nucella lima courtesy Gerald and Buff Corziexperience more than twice the daily exposure to freezing temperatures than individuals in the lower part (7 vs. 3h, respectively).  Behavioral mechanisms to minimize freezing include cessation of feeding, hiding in crevices or beneath boulders, and burrowing into sediments during periods of tidal emersion.  Physiologically, the snails can supercool to almost -5oC but, as the researchers record several incidents of air temperatures during intertidal exposure below this during Dec-Feb (to -13oC), it is evident that freezing of tissues must occur and is tolerated by the snails.  When a snail’s temperature falls below the supercooling point, ice forming in the extracellular-fluid compartments will draw water from the intracellular compartments thus protecting the cells from damage.  In this regard, tolerance to freezing may owe in large part to the seasonal winter increase in hemolymph concentration of total free-amino acids, including most notably taurine and glycine.  The authors suggest that upper limits of intertidal zonation of N. lima may be set by their freeze tolerance to emersion during winter low tides.  Stickle et al. 2010 J Exp Mar Biol Ecol 395: 106. Photograph courtesy Gerald & Buff Corzi, and the California Academy of Sciences CALPHOTOS

NOTE  seawater temperatures in the Canal range seasonally from 1-15oC

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Research study 7

schematic showing latitudinal compensation for temperature stress in whelks Nucella ostrinaLatitudinal compensation for temperature stress is common in adult intertidal invertebrates, but is it present in larval stages?  This is investigated by researchers at the University of California, Santa Barbara for veliger larvae of whelks Nucella ostrina obtained from capsules collected at 7 sites from northern Washington to central California. The authors determine LT50 values for mature veligers and, as expected, find a significant latitudinal trend (see graph and map).  Note that first to die are veligers from Cattle Point, Washington Gulf Islands and the last, from 2 sites in central California. Zippay & Hofmann 2010 Mar Biol 157: 707.

NOTE  for data on temperature effects on growth of N. ostrina embryos, see Research Study 1 above

NOTE  this is the temperature at which 50% of the larvae are killed by heat treatment.  Different samples of veliger larvae still in their capsules are exposed for 1h periods to a range of temperatures from 13-34.5oC.  Only if the veligers upon examination afterwards are in an advanced stage of development (i.e., shell, foot, operculum, eyespots) are the data used in analysis 


The small letters above each datum
point indicate statistical similarity

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Research study 8

graph showing effect of light intensity on distribution of horn snails Cerithidea californica on beaches in CaliforniaAn investigation of horn snails Cerithidea californica in Mugu Lagoon and Goleta Sloughby researchers at the University of California, Santa Barbara reveals that light plays a strong role in their distribution.  After observing that densities seem greater in lighted areas of the shore than in shaded areas (see graph), the researchers experimentally manipulate light regimes by clipping vegetation and installing shade structures.  Within a few days, snail densities in areas of the shore with higher light levels increase significantly.  The authors hypothesise that shading reduces the numbers of surface-inhabiting diatoms on which the snails feed and the snails soon move away.  Lorda & Lafferty 2012 J Exp Mar Biol Ecol 432/433: 148.

NOTE confirmed in other experiments

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Research study 9

photograph of mesocosm set-up for use in study on temperature responses in whelks Nucella ostrinaA study by researchers at Friday Harbor Laboratories, Washington investigates temperature effects on foraging and growth of whelks Nucella ostrina from the standpoint of possible sex differences.  While the motivation to look for sex differences in this particular whelk species is unclear, the results are interesting.  Instead of conducting their experiments in the field the researchers use temperature-regulated mesocosms in an outdoor laboratory setting.  These are upside-down terracotta pots bearing prey barnacles (Balanus glandula) on the upturned base, and with a “thermal refuge” (a portion of PVC pipe near the base of the pot; see photograph) into which the snail can crawl when it gets too hot.  Heat lamps above each pot are controlled by thermisters.  Snails are monitored for foraging times and durations during simulated low-tide periods by simple visual counts.   Results from 30d monitoring sessions show that males and females exhibit similar temporal patterns of foraging that are little affected by elevated “low-tide” air temperatures, and that females forage more than males.  Most interesting is the finding that females are more “risk-takers” than males, and will venture out even when the risk of thermal stress is high enough to lead to loss of body mass after several days of exposure to higher temperatures.  Such risk-taking appears not to be related to greater nutritional needs of the female during the reproductive cycle because the study is done in June, apparently too early for gonads to begin growing.  As is almost de rigueur during this time of climate change, the authors include a summary comment about possible long-term implications of such sex-specific temperature responses to survival of the species in an “increasingly warm world”.  Vaughn et al. 2014 Mar Biol 161: 75.

NOTE  foraging by these predators occurs commonly during mid-day low-tide periods in summer, especially during late morning.  Experimental temperatures vary from a “control” level of 20oC to a “heat” level of 28oC, in various patterns of exposure

NOTE  the study is done in June, outside of the period of gonadal growth, but wouldn’t it have been interesting to have done it later in the season when the gonads start growing, especially from the standpoint of this enhanced thermal risk-taking of the females?  September/October can sometimes be warm in the San Juan islands

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Research study 10

photograph showing biomimetic sensors used in study of temperature interactions in whelks NucellaThe extent to which whelks Nucella spp. could potentially ameliorate summer temperature stress in intertidal rocky habitats by selective use of different microhabitats is examined by researchers at Friday Harbor Laboratories, Washington using a series of biomimetic thermal sensors (see photograph). Forty-two of these thermal sensors are moved between 11 different microhabitats within a 10x10m square area on a rocky shore of San Juan Island over 3 successive spring/summers (May-Aug). Temperatures are recorded from the sensors at 15min intervals over periods of several weeks-to-months during each of the 3yr. Results show, as would be expected, significant temperature differences among the microhabitats at low tide depending upon aspect to the sun, shading from algae, open rock or crevice, time of year, and intertidal height. With respect to the last, the authors remark that Nucella ostrina could theoretically halve its thermal stress by moving relatively short distances between different sun-exposed and shaded locations at the same tidal height, or by crawling as little as 0.5m down the shore during particularly hot days. Just shifting from open rock to a crevice or algal-shaded habitat could reduce body temperatures by 2oC or more. The authors provide considerable graphical information on different temperature-habitat interactions, which while informative, begs the more interesting question of the extent to which snails actually do undertake migrations to ameliorate thermal stresses in the field. Gilman et al. 2015 Mar Ecol Progr Ser 536: 77. Photograph courtesy the authors.

NOTE species modelled include the predatory whelks Nucella lamellosa and N. ostrina, and their prey barnacles Balanus glandula. Only the whelks are considered in this summary

NOTE the biomimetic structures are constructed of empty shells filled with epoxy adhesive, that together match the thermal characteristics of the model snails. Each contains a thermocouple sensor linked to a central data-logger. Thermal characteristics, compared between mimetics and live snails in a wind tunnel simulation with fans and incandescent heat lamps, reveal a mean difference of about 2oC

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Research study 11

The research question posed in the foregoing Research Study regarding whether whelks Nucella ostrina modify their behaviour in the field to reduce temperature stresses is addressed in a companion study by the same research group at Friday Harbor Laboratories, Washington. The experiment involves placing cinder blocks in the intertidal zone oriented so that one side faces east and the other west (in the directions of morning and afternoon sunlight, respectively). Barnacles growing on mussel shells are then attached to each side of each block along with temperature loggers1 (see photographs below). Snails are added to each block (number2 not specified). Over an 8wk period during summer, counts are made during low-tide periods of snails feeding or sheltering and of barnacles being consumed on each side of a block, and the data later related to substratum temperatures. Results show that foraging is closely associated with the tide cycle and with the substratum face that is most cool (temperature differences between sides vary with the tide cycle, but on average are about 4-8oC). Thus, on days with a morning low tide the snails tend to feed on the shady or west side, while on days with an afternoon low tide they favour the shady or east side. As the low-tide period advances through its 2wk lunar cycle, so the proportion of snails feeding on one side or another shifts in synchrony. In general, the snails feed more during neap tides (mean substratum temperatures of 17oC) than during spring tides (31oC). Optimal foraging3 for the snails is therefore when exposure to temperature stress is minimised. Hayford et al. 2015 Mar Ecol Progr Ser 518: 165. Photographs courtesy the authors.

NOTE1 dataloggers may slightly overestimate body temperatures of the snails owing to the snails experiencing a certain degree of evaporative cooling

NOTE2 while the authors report proportion of snails feeding at different times, they seem not to provide the total number of snails maintained on each cinder block (more than 5, though, because at any count less than this the researchers comment that new snails are added to restore numbers to original starting values). In addition to “natural” deaths (not reported), snail losses may partly owe to escapees over the wall, and partly to predation from red-rock crabs Cancer productus which apparently enter the compounds during nighttime high tides

NOTE3 given the sensible nature of this comment, one wonders why most foraging by the snails in summer is not done at night. In fact, the researchers would have had all the data necessary to determine extent of nighttime foraging, but appear not to have done so. Perhaps the snails themselves are inhibited from feeding by presence of predatory crabs, themselves foraging for snails at nighttime. The authors should look into this

  photographs of whelk habitats for study of temperature effects on foraging of whelks Nucella ostrina
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