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Intertidal distribution of six trochids atPortobello, New ZealandC. P. Mitchell a ba Portobello Marine Laboratory , University of Otago , P.O. Box 8,Portobello, New Zealandb Fisheries Research Laboratory , Ministry of Agriculture &Fisheries , P.O. Box 951, Rotorua, New ZealandPublished online: 29 Mar 2010.

To cite this article: C. P. Mitchell (1980) Intertidal distribution of six trochids at Portobello,New Zealand, New Zealand Journal of Marine and Freshwater Research, 14:1, 47-54, DOI:10.1080/00288330.1980.9515842

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New Zealand journal of Marine & Freshwater Research, 1980, 14 (1): 4 7 - 5 4

Intertidal distribution of six trochids at Portobello, New Zealand

C. P. MITCHELL*

Portobello Marine Laboratory, University of Otago, P.O. Box 8, Portobello, New Zealand

The vertical distribution of the trochid topshells Diloma nigerrima (Gmelin, 1791), D.zelandica (Quoy & Gaimard, 1834). D. subrostrata novazelandiae (Anton, 1839), D. bicana-liculata (Dunker, 1844), D. lugubris (Gmelin, 1791), and D. arida (Finlay, 1927) and of thelittorinid Littorina cincta (Quoy & Gaimard, 1833) was studied on rocky shores in OtagoHarbour. The upper temperature tolerance while submerged and exposed, weight loss underlow and high relative humidities, and survival under constant submergence were determinedfor each species. Vertical distribution was not directly related to resistance to high tempera-tures and desiccation but to the conditions likely to be experienced during low tide within themicrohabitat occupied by each species. No lethal physical factor was found that would pre-vent any of the species from occupying subtidal levels. Behavioural responses of each speciesto high temperatures and desiccation also reflected the environment in the species' micro-habitat at low tide.

KEYWORDS: Gastropoda, Intertidal distribution, Trochid topshells, Desiccation, Thermalstress, Behaviour, Portobello.

INTRODUCTION

The intertidal zone is differentially exposed to theterrestrial environment during the tidal cycle andcan be subdivided into faunal zones on this basis(Morton & Miller 1968). For marine life, stressimposed by the retreat of the tide must be greater athigher levels on the shore and the zonation of plantsand animals which is displayed in the intertidalzone may be determined by their ability to resist theeffects of exposure. Two of the most obvious prob-lems that an exposed intertidal animal must face atlow tide are desiccation and heat stress.

A variety of intertidal trochid gastropods are foundliving up to the supralittoral fringe of New Zealandshores (Powell 1976). This study attempts to relatethe resistance of six such species to desiccationand heat stress in both air and water to their ver-tical distribution on the shores of Otago Harbour.Survival under the converse stress of constant sub-mergence is also compared. Littorina cincta (Quoy& Gaimard, 1833) is included for comparison asit occurred higher on the shore than any othergastropod and was assumed to be the most resistantintertidal gastropod.

METHODSFIELD METHODS

The vertical zonation of six trochid species and L.cincta was determined by transects on the rockysheltered shores near Portobello Marine Laboratory,

Otago Harbour, New Zealand (NZMS1 64/271774).Each transect consisted of a continuous strip of1 m2 quadrats from the upper limit of Hormosirabanksii (MLWN) to the upper limit of Verrucarialichens (MHWS). Levels of MHWS, MHWN,MLWN, and MLWS were determined by visits tothe shores at the appropriate times (Marine De-partment 1971). Snails visible on the surface andthose beneath the rocky substrate were recorded andobservations were made of the habitat occupied byeach species.

LABORATORY METHODS

RESISTANCE TO DESICCATION. Freshly collected L.cincta and the six trochid species were divided intotwo groups containing 20 individuals of each species.One group was maintained at low relative humidity(24-27% RH) in a desiccator over silica gel. Theother group was maintained at high relative humid-ity (80-82% RH) induced by open containers ofwater in a sealed 10-L container. Temperatures were5-6°c throughout—comparable to June-July localsea and air temperature (Records of the PortobelloMarine Laboratory). Animals were weighed to± 0.002 g ?t irregular intervals for 41 days. Cleanedand dried shells were then replaced in the experi-mental containers to equilibrate water content, andthe resulting shell weights were subtracted from totalweights to express the results as changes in wetflesh weight.

Received 28 March 1978; revision received 6 August 1979Fisheries Research Division Publication 391

•Present address: Fisheries Research Laboratory, Ministry of Agriculture & Fisheries, P.O. Box 951,Rotorua, New Zealand

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48 New Zealand Journal of Marine & Freshwater Research, 1980, 14 (1)

RESISTANCE TO THERMAL STRESS IN SUBMERGED

ANIMALS. Twenty specimens of each species wereplaced in 5-L containers filled with fresh, con-tinuously aerated seawater at 10-14°c. The tempera-ture was raised l°c per 5 min (Newell 1970) untilthe test temperature was reached and was thenheld constant for 120 min. The animals were thenremoved and left for 12 h in shallow dishes of seawater at 10-14°c before mortalities were recorded.When a test animal failed to retract rapidly afterbeing lightly touched with a fine metal probe andwhen no tentacle movement could be seen, theanimal was classed as irreversibly heat damaged(Sandison 1967). This method was repeated for eachspecies at l°c successively higher test temperatures.The temperatures at which all animals lost theirgrip on the substrate and at which they went intoheat coma (Sandison 1967) were recorded.

RESISTANCE TO THERMAL STRESS IN EXPOSED ANI-

MALS. Twenty specimens of each species weresealed in a 2-L chamber which was then submergedin a water bath at 10-14°c. Air, temperature-equili-brated by passage through a coil immersed in thewater bath, was continually pumped through thechamber. The temperature was raised in the sameway as with submerged animals. Limitations of thissealed apparatus meant that the temperatures atwhich loss of attachment to the substrate occurredwere recorded in a less thermally stable, glass-fronted incubator. Glass plates, to which the ani-mals had initially adhered, provided an artificialsubstrate inclined at 45°. Humidity levels in theincubator were kept high with open containers ofwater.

RESISTANCE TO CONSTANT SUBMERGENCE. Twenty

specimens of each species were kept under con-tinuously flowing sea water in 20-L containers withsubsurface covers of nylon grit gauze to preventthe animals gaining access to the atmosphere. Thecontainers were examined for mortalities at 2-3-dayintervals. Three experiments were run for 28, 49,and 74 days respectively.

RESULTS

FIELD RESULTS

L. cincla was found further up the shore than anyother gastropod and was most abundant in andaround crevices on rock surfaces as found in Trans-ect A (Fig. 1). Animals on exposed surfaces duringfine weather were usually inert and attached by afilm of dried mucus between the anterior shellmargin and the rock; the close-fitting operculum wasfurther sealed with mucus. Diloma nigerrima(Gmelin, 1791) was recorded higher on the shore

than any of the other trochid species, co-occurringwith L. cincta in shaded places where large amountsof drift algae (Macrocystis pyrifera) were washedup (Transect B). Diloma zelandica (Quoy & Gai-mard, 1834) and Diloma arida (Finlay, 1927) bothreached peak densities between MHWN and MLWN,although D. zelandica was confined to the undersideof large, relatively stable rocks. D. arida occurredboth exposed on upper surfaces and underneathstones, and was the dominant species where thesubstrate was of small, readily moveable stones(Transect C). Diloma lugubris (Gmelin, 1791) wasclearly the dominant gastropod both above andbelow rocks and stones from between MHWN toMLWN in all transects. Diloma bicanaliculata (Dun-ker, 1844) and Diloma subrostrata novazelandiae(Anton, 1839) were both relatively uncommon. D.bicanaliculata appeared restricted to the undersideof large boulders in damp places around the lowerrange of D. zelandica. D. s. novazelandiae is mostabundant on the upper reaches of tidal flats insheltered sites (Clark 1968, Logan 1976), but smallnumbers were present near MLWN on these rockyshores.

LABORATORY RESULTS

RESISTANCE TO DESICCATION. Fig. 2 shows relativerates of weight loss expressed as a percentage ofthe initial weight for the seven species. An obviousfeature is the apparent superior ability of D. niger-rima to maintain weight in a humid atmospherecontrasted with a rate of weight loss similar to theother trochid species when kept under low humidity.D. bicanaliculata appeared to have the lowest resis-tance to weight loss of all the species and during thefirst 5-7 days lost weight relatively rapidly and ata similar rate under both high and low humidities.

RESISTANCE TO THERMAL STRESS. The effects ofelevated temperatures on the seven species areshown in Table 1. All species released their grip onthe substrate at higher temperatures when exposed,possibly due to the cooling effect of evaporatingbody fluids (Newell 1970). The initial response ofexposed animals to rising temperatures was to be-come quiescent. The anterior shell margin was thenoriented upslope followed by the shell lifting awayfrom the substrate so that the mantle cavity gaped.A further temperature increase caused the animals torelinquish their grip, the foot 'peeling' away fromanterior to posterior. Not all L. cincta behaved inthis manner; some secreted a continuous sheet ofmucus from the anterior portion of the body on tothe substrate and the anterior shell margin. Theanimal then withdrew into the shell and as theoperculum moved to seal the aperture the posteriorof the shell was lifted. Finally, the aperture and

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Mitchell: Distribution of Topshells 49

Transect A n=661

12-

10-

8-

6-

4-

2-

0-

Transect B n=556

16

14

10-

S'

6-

4-

2

0J

14-

12-

10-

8

6-

4-

2-

0

Transect C /;=414

20

Under cover =

-2Q

OcCO

ci

-S9>

Ci

= Exposed

MHWS

MHWN

MLWN

MLWS

•MHWS

•MHWN

MLWN

MLWS

•MHWS

•MHWN

•MLWN

MLWS

Fig. 1.

Number per m2as percentage of totalVertical distribution of intertidal gastropods on the shore at Portobello, New Zealand.

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50 New Zealand Journal of Marine & Freshwater Research, 1980, 14 (1)

operculum were sealed with mucus, leaving an inertanimal hanging on the substrate by a film of driedmucus. This response appears better directed to-wards reducing water loss than to the avoidance ofhigh temperatures. Those L. cincta which had re-leased their grip on the substrate sealed the oper-culum and remained passive. In contrast, the Dilomaspecies did not attempt to close the operculum butmade righting movements which quickly declined invigour and frequency.

The 50% mortality temperatures of the sixtrochids lie within a 3°c range, but L. cincta cansurvive exposure to temperatures over 5°c higherthan D. zelandica, the most resistant trochid (Fig.3). An average difference of 0.18°c between the50% mortality temperatures in water and air forall species suggests that there is no essential dif-ference in the cause of heat death when submergedor exposed.

RESISTANCE TO CONSTANT SUBMERGENCE. Three

separate experiments, terminated after 28, 49, and74 days respectively, did not show any definitetrends (Table 2). Mortality during long periods offorced submergence was very low for all the species.

DISCUSSION

Of the gastropods examined in these experiments, thespecies found on the upper shore should be themost resistant to elevated temperatures and desicca-tion. However, comparison between the two speciesfound in the supralittoral zone showed a consider-able variation in tolerance. L. cincta was clearly themost resistant to elevated temperatures; the50% lethal temperature was over 7°c higher thanfor D. nigerrima (which was one of the least tol-erant species), but D. nigerrima was found to losewater at the lowest rate of any species when keptunder humid conditions. These results appear toreflect environmental conditions within the micro-habitat occupied by each species. D. nigerrima wasrestricted to shady situations of high humidity

(usually beneath stones or drift seaweed), wherethe animal is protected from the effects of directinsolation, but an ability to resist water loss wouldbe vital during neap tides. L. cincta occurred withD. nigerrima but was also common on open rocksurfaces where temperatures up to 45°c have beenrecorded (J. Jillett, Portobello Marine Laboratory,pe»"s. comm.).

The two trochids of the upper mid-littoral zone,D. zelandica and D. arida, were less resistant todesiccation than the gastropods from higher up theshore. The tolerance of D. zelandica to elevated tem-peratures and, conversely, the greater resistance ofD. arida to water loss were not reflected in theirobserved distributions; D. zelandica occurred be-neath stones and D. arida was found both on exposedsurfaces and beneath stones. D. lugubris, D. s. nova-zelandiae, and D. bicanaliculata attained levels ofmaximum abundance within the lower mid-littoralzone and all displayed a low resistance to desicca-tion, but it was again apparent that resistance tostress does not directly reflect vertical distributionas D. lugubris and D. s. novazelandiae were amongthe three trochids most tolerant to elevated tempera-tures. Periods of exposure in the lower mid-littoralwould never exceed 6 h so that desiccation is un-likely to become a major problem for these gastro-pods, although insolation could raise temperaturesappreciably for exposed animals. D. bicanaliculatawas found to be the least resistant to desiccationand thermal stress. This is consistent with a distribu-tion restricted to the damp microhabitat foundunderneath large boulders.

The stress imposed by constant submergenceshould be greatest for animals living in the uppertidal range, but none of the species in this studywas found to be an obligate air breather. Thehigh survival of all seven species during enforcedsubmergence conflicts with results reported for com-parable animals; 6 days for L. littoralis (Colgan1910) and 23-28 days for L. littorea (Gownalock *Hayes 1928). Micallef (1966) demonstrated that

Table 1. Temperature (°c) at which 7 species of in :ertidal gastropods lost their grip on substrate, enteredheat coma, or died while exposed to atmosphere or submerged in seawater (-, no data).

SpeciesLittorina cinctaDiloma nigerrimaD. aridaD. lugubrisD. zelandicaD. s. novazelandiaeD. bicanaliculata

Grip on substrate lostExposed

35343736363536

Submerged34333634333535

Heat comaSubmerged

44373837383837

50% mortality after150 min exposure

Exposed43.736.937.7373838.335.6

Submerged43.736.537.338.738.237.735.8

100% mortalityafter 5 minexposure

Submerged

4841434242

41

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Mitchell: Distribution of Topshells 51

Relative humidity 24-27%Temperature 5-6 °C

70-

60-

50-

40-

30-

20-

10

A Littorina cinctao Diloma nigernma* D. arida* D. lugubriso D. zealandica• D. s. novazelandiae* D.bicanaticulata

Relative humidity 80-82%Temperature 5-6 °C

0— i —10 15

— I —20 25 30 35 40

Time (days)

Fig. 2. Relative rates of weight loss for seven species of intertidal gastropod at two levels of relativehumidity.

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52 New Zealand Journal of Marine & Freshwater Research, 1980, 14 (1)

100

90

80

70

60

50

40

30

20

10

~ 33

Submerged

34 35 37 38 39 40 41 42 43 44 45

33 34 35 36 37 38 39 40Temperature (°C)

41 42 43 44 45

Fig. 3. Percentage mortality of intertidal gastropods subjected to elevated temperatures. Symbols for speciesas in Fig. 2.

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Mitchell: Distribution of Topshells 53

constant submergence was stressful to high-level,facultatively air-breathing gastropods, and Micallef &Bannister (1967) found that dependence on aquaticor aerial respiration may vary between speciesaccording to their levels of maximum abundanceon the shore.

The inclusion of all trochid species used in thisstudy within the genus Diloma (Powell 1976, Cer-nohorsky 1977) suggests that the species have a re-cent common ancestor which has been able to exploitsix distinct niches within the intertidal zone. Cer-tain limitations of the basic trochid design are ap-parent when a comparison is made with the littor-inid species, a gastropod type shown to have greaterresistance to both heat stress and desiccation. Waterloss is the factor towards which littorinid morphologyand behaviour appears to be directed and the shellaperture is the most obvious point of water loss. Thesubstantial operculum of L. cincta, sealed withmucus, is apparently an efficient water conserva-tion system. In contrast, the trochid operculum is athin, spirally coiled, chitinous disc which warpedafter prolonged drying. This may be an importantfactor in the restriction of D. nigerrima, the onlytrochid to have invaded the upper shore, to habitatsof obvious high humidity. If we consider how evolu-tionary radiation has occurred to integrate the tol-erance of each species to the physiological demandsof a niche, it is apparent that a simple shorewardgradient of increasing tolerance cannot be discerned.Possibly the metabolic 'cost' of producing stresstolerance over a wide range of conditions is suchthat selection favours individuals most closely adapt-ed to the environmental demands of the niche micro-habitat.

Physical stress which does not reach lethal valuesmay be important in controlling the distribution ofthese species through behavioural responses. Forexample, the first response of all trochids and manyL. cincta to rising temperatures was to release theirgrip on the substrate. In nature this could result inanimals dropping off inclined surfaces to reach lower,possibly cooler, levels. Exposed individuals of L.

Table 2. Mortality among 7 species of intertidalgastropod kept constantly submerged in seawater.(n = 60 for each species).

SpeciesLittorina cinctaDiloma nigerrimaD. aridaD. lugubrisD. zelandicaD. s. novazelandiaeD. bicanaliculata

0

0000000

Time submerged28

0001100

49

00

nl201

(days)74

1101533

cincta were commonly found clustered together increvices where they may collectively reduce thetemperature and rate of water loss. Rapid upwardmovement by all species when the gauze covers wereremoved for cleaning during constant-submergenceexperiments indicated that exposure was preferredafter constant submergence (Luckens 1974). Bark-man (1955) described behaviour in L. littoralis andsuggested that negative geotactic movement untilhalted by desiccation was the response by whichoptimal shore levels are attained.

These results provide a basis for comparison ofresistance to physical stress factors, but the absolutevalues measured do not allow for acclimatisation.Other intertidal species have been shown to havetolerances which vary with latitude and season(Edney 1961), and with shore height, aspect, andtopography (Smith 1975).

ACKNOWLEDGMENTSi thank Dr John Jillett, Acting Director of Porto-bello Marine Laboratory, both for making the facili-ties there available to me and for his continued in-terest, advice, and encouragement.

REFERENCESBARKMAN, J. I. 1955: On the distribution and ecology

of Littorina obtusata (L.) and its subspecificunits. Archives Neerlandaises de Zoologie 11-1:22-86.

CERNOHORSKY, W. O. 1977: The taxonomy of somemolluscan species reported from New Zealand.Records of the Auckland Institute & Museum14: 87-104.

CLARK, W. C. 1958: The New Zealand species ofMelagraphia Gray and Zediloma Findlay(Mollusca, Gastropoda). Transactions of theRoyal Society of N.Z. 85(4): 659.

COI.GAN, N. 1910: Notes on the adaptability of cer-tain littoral Mollusca. Irish Naturalist 19: 127-33.

EDNEY, E. B. 1962: Some aspects of the temperaturerelations of fiddler crabs (Uca spp.). Bio-meterology 1: 79-85.

GOWANLOCK, J. N.; HAYES, F. R. 1926: The physicalfactors, behaviour and intertidal life of Littorina.Contributions to Canadian Biology 3: 133-66.

LOGAN, S. J. 1976: Ecology of Diloma novaezelandiaeat Portobello, New Zealand. N.Z. Journal ofMarine & Freshwater Research 10(4): 699-714.

LUCKENS, P. A. 1974: Removal of intertidal algaeby herbivores in experimental frames and onshores near Auckland. N.Z. Journal of Marine& Freshwater Research 8(4): 637-54.

MARINE DEPARTMENT 1971: New Zealand NauticalAlmanac and Tide Tables for the Year 1972.Government Printer, Wellington.

MICALLEF, H. 1966: A biochemical factor in thezonation of marine molluscs. Nature 211(5050):747.

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MICALLEF, H.; BANNISTER, W. H. 1967: Aerial andaquatic oxygen consumption of Monodonta tur-binata (Mollusca, Gastropoda). Journal of Zoo-logy 151: 479-82.

MORTON, J.; MILLER, M. 1968: The New ZealandSea Shore. Collins, London & Auckland.

NEWELL, R. C. 1970: Biology of Intertidal Animals.Logos Press, London.

POWELL, A. W. B. 1976: Shells of New Zealand. 5threvised ed. Whitcoulls, Christchurch.

SANDISON, E. E. 1967: Respiratory responses to.temperature and temperature tolerance of someintertidal gastropods. Journal of ExperimentalMarine Biology & Ecology 1: 271-81.

SMITH, S. 1969: “Distribution and abundance ofsub-iittoral grazing molluscs on rocky shores.”Unpubl. MSc thesis, University of Auckland,N.Z.

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