title for learn-about sections for chitons in A SNAIL'S ODYSSEY
  Adaptations to intertidal life
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Gas exchange

  This hodge-podge selection of topics relating to intertidal life in chitons includes gas exchange, considered here, and pH & OCEAN ACIDIFICATION, WAVE EXPOSURE & TENACITY, TOLERANCE OF FRESHWATER & OSMOREGULATION, and LIGHT, DESICCATION, & TEMPERATURE STRESS, Considered in other sections.
Research study 1

photograph of lined chiton Tonicella lineataGas exchange in chitons occurs in ctenidia that hang freely into the pallial groove on either side of the body. Although it is something that might be expected, gill numbers may not be identical on either side of a chiton, at least not according to counts done on museum-preserved specimens of Tonicella lineata in California.  These show that individuals of 2-4cm in length have 24-32 ctenidia in the right pallial groove and 26-29 in the left pallial groove.  The means are about the same at 28, but whether there is any biological significance in the variability is not known.  Johnson 1969 Veliger 11: 272. Photo of Tonicella courtesy Ron Long, Simon Fraser University, Burnaby, British Columbia.

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Research study 2
  photograph of ctenidia of a gumboot chiton Cryptochiton stelleri drawing showing water flow through the pallial groove of a gumboot chiton Cryptochiton stelleriInvestigations at Friday Harbor Laboratories, Washington show that adult gumboot chitons Cyptochiton stelleri have about 75 ctenidia per side, while juveniles have about 50 per side.  Each ctenidium has about 100 filaments, providing a relative surface area for gas exchange that is notably large for a mollusc. Water is moved through the pallial cavity by ciliary action and flows from front to back.  In addition to irrigating the ctenidia, the flow as it moves along picks up urinary discharge from the kidney openings, reproductive products from the gonopores and, near the end of its route, feces from the anus.  

drawing to show counter-current flow arrangement in the ctenidium of a chiton Cryptochiton stelleriGases move across the ctenidial epithelium by diffusion in response to concentration gradients.  The authors demonstrate the existence of a counter-current exchange system in the ctenidial filaments.  Thus, hemolymph moves in one direction through the filaments, while seawater moves in the opposite direction. This means that oxygen-poor hemolymph entering the ctenidia first meets oxygen-depleted seawater exiting the filaments.  By the time the hemolymph leaves the filament it is richer in oxygen, but is now meeting seawater with maximum content of oxygen. The counter-current system ensures maximum concentration gradients between the two fluids along the width of each filament.  The gradients for exchange of carbon dioxide operate in reverse, but are likewise maximal. When exposed to moist air when the tide goes out, Cryptochiton may expose its ctenidia, apparently to facilitate aerial gas exchange.  However, measurements of oxygen uptake show rates in air only about one-quarter that in water, even at experimental temperatures in air (17-20oC) almost twice that in water (10oC).  Even when immersed, Cryptochiton often raises its girdle to maximise exchange of seawater within the pallial cavity.  Petersen & Johansen 1973 J Exp Mar Biol Ecol 12: 27.

NOTE the authors term this “blood”, but blood is defined as a tissue that circulates within closed systems of vessels and that usually contains cellular material involved in gas transport and internal defense.  Hemolymph is found in molluscs and arthropods, circulates in large, open (i.e., not enclosed in vessels) hemocoelic spaces, and carries few, if any, cellular elements.  A gas-transporting pigment hemocyanin is present in chitons, but is in solution and not contained within cells; see also Heath 1905 Biol Bull 9 (4): 213 for a detailed account of the excretory and circulatory systems in C. stelleri

NOTE  this behaviour may explain why some individuals are found lying upside-down during low-tide periods, possibly having fallen off rocks while adjusting their position for ctenidial exposure

Research study 3

photograph of chiton Nuttallina californica courtesy Ron Wolf, CaliforniaWhat modifications in morphology and functional mechanics of the ctenidia and pallial cavity are associated with increased air exposure in chitons?  If this parallels what is seen in branchial-cavity morphology and functioning in crabs with increasing terrestriality, then we would expect adaptations such as:

1) fewer ctenidia relative to body size
2) smaller volume of individual ctenidia
3) greater structural support for the ctenidia
4) vascularisation of the pallial groove
5) larger volume of the pallial groove.

So, what do we find in chitons?  A comparison of ctenidial and pallial-groove morphology in 2 species of chitons at Hopkins Marine Station, Pacific Grove, California, one of which, Nuttallina californica, inhabits the mid- to high-intertidal region, while the other, Tonicella lineata, lives mostly in the subtidal region, reveals the following:photograph of lined chiton Tonicella lineata

1) Nuttallina of about 5cm length has 30-48 ctenidia on either side versus 22-29 in Tonicella of about 2-4cm length 
2) Nuttallina has more filaments per ctenidia than Tonicella, which, although not mentioned in the study, may represent a greater relative surface area for gas exchange in Nuttallina
3) Nuttallina has somewhat stouter ctenidia than Tonicella, possibly providing more support for the ctenidia in air
4) there is no evidence of vascularisation of the pallial cavity in either species
5) Nuttallina is capable of considerably more expansion of the pallial cavity than Tonicella, and does so during times of air exposure as long as the air is moist

So, 3 characteristics of Nuttallina identified in blue numbers in the above list support the notion of ctenidia/pallial cavity adaptations for more terrestrial life in chitons, while the other 2 don't. Is this enough, however, to suggest that the gas-exchanging capability in air of the high level-inhabiting Nuttallina is potentially greater than that of the low intertidal/subtidal-inhabitiing Tonicella?drawings showing different girdle/mantle orientations in chitons living subtidally (Tonicella lineata) and intertidally (Nuttallina californica)

Nuttallina’s girdle is additionally thick and muscular, and can be closed tightly over the ctenidia or raised up high, depending upon humity conditions (see drawings on Right).  This behaviour is also suggestive of an aerial oxygen-exchanging capacity.  Measurements of oxygen consumption in air in the 2 species show non-significant differences between the 2 species. Both species consume significantly less oxygen in air than in water.  The study is an interesting one and should repay further investigation.  Robbins 1975 Veliger 18(Suppl): 98.


photograph of a "duppy crab" Cardisoma guanhumi from BarbadosNOTE  in crabs the functionally analagous condition is known as “ballooning”, where the branchial chamber in terrestrial species has become greatly expanded in size.  All of the adaptations listed above for crabs increase the surface area available for gas-exchange in air

Caribbean "duppy crabs" Cardisoma guanhumi
show "ballooning" of the carapace surrounding
the branchial chambers, indicative of an
ability for aerial uptake of oxygen 0.3X

Research study 4

histogram comparing oxygen uptake and scaling exponents in 6 species of chitons Katharina tunicata, Cyanoplax dentiens, Mopalia lignosa, M. muscosa, Tonicella lineata, and Placiphorella velata An interesting contribution to the concept of metabolic scaling in marine ectotherms is made by researchers from Queen’s University Belfast and University of British Columbia.  Metabolism as reflected by oxygen consumption is generally thought to follow the classical two-thirds rule1 when dealing with a single ectothermic species, where slope b of the regression of metabolic rate to body mass equals 0.67 and, when dealing with interspecies comparisons, where slope b becomes closer to 0.75.  Why this latter should be is never very clearly explained, but the scaling exponent of 0.75 is commonly used in multi-species comparisons or in studies at a community level.  When experimentally measured values deviate significantly from theoretical expectation, researchers are likely to shrug them off as being caused by imprecise measuring instruments, poorly controlled experimental conditions, or other kinds of “noise” (e.g., bacterial and other micro-organismal  contamination).  The present authors set out to determine scaling exponents for oxygen consumption against body mass in 6 species of chitons, using as carefully controlled conditions as possible (including nutritional status, bacterial contribution and, to a lesser extent, activity level in the respirometer).  Results for the 6 scaling exponents range from 0.64-0.91, equating to an all-species value of 0.73 (not significantly different from 0.75), but with 5 of the 6 species2 differing significantly from it.  Rather than accepting their results as de facto support for the ¾-power rule, the authors attempt to identify possible reasons for the significant differences measured.  Their conclusion is that variations from the ¾ rule are real, and stem from species-specific differences3 in activity levels and general lifestyles related to different microhabitats occupied.  Their ultimate conclusion is the large natural variation in scaling exponents shown by chitons (and other species) adds to the growing evidence against acceptance of a universal scaling law.  Carey et al. 2013 J Exp Mar Biol Ecol 439: 7.  

NOTE1  this is based on the scaling ratio of surface area to volume of a 3-dimensional object

NOTE2 the species include Katharina tunicata, Cyanoplax dentiens, Mopalia lignosa, M. muscosa, Tonicella lineata, and Placiphorella velata

NOTE3  most telling is that the 6 species separate into 2 statistically homogenous groups, with the 2 mopalids Mopalia muscosa and M. ligosa in one group (b = 0.64), and the remaining 4 species in the other (b = 0.75)

Research study 5

photograph of black-leather chiton Katharina tunicatagraphs showing relationship of metabolic rate and temperature/pH in chitons Katharina tunicataA later study by the same research group from Queen’s University Belfast compares effects of temperature and pH on oxygen consumption in 3 chiton species at Friday Harbor Laboratories, Washington. The aim here is to measure the metabolic response of these invertebrate grazers to increased temperature and decreased pH as might be expected during impending climate change, with specific attention to body-size scaling effects. Results show, in fact, that oxygen uptake scales with body size differently in response to temperature and pH. This is shown most clearly for K. tunicata, where smaller individuals are more responsive to warming than larger ones (see graph on upper Right), while larger ones (graph lower Right) are more responsive to decreased pH, especially at the lower temperature of 9oC. In both graphs the natural range of slopes between 0.67-1.0 (see Research Study 4 above) are shown by shaded areas. The authors briefly discuss the possible significance of these asymmetric responses to temperature and pH in different size/age groups, with regard to metabolic function in predicted warmer, more acidic future conditions. Carey & Sigwart 2014 Biol Lett 10 (8): xx.

NOTE Katharina tunicata, Mopalia muscosa, and Tonicella lineata

NOTE 3 temperatures are used (9, 13, and 17oC) and 2 pHs (8.0=control and 7.5)