Winter 1963 RESPONSES OF THE GENERA 73 Hathaway, R. R. and K. D. Woodburn. 1961. Studies Patten, B. C. 1962. diversity in net phyto• on the crown conch, Melongena corona Gmelin. Bull. plankton of Raritan Bay. ]. Mar. Res. 20: 57-75. Mar. Sci. Gulf and Carib. 11: 45-65. Pilson, M.E.Q. and P. B. Taylor. 1961. Hole-drilling Hutchinson, G. E. 1959. Homage to Santa Rosalia or by octopus. Science 134: 1366-1368. Why are there so many kinds of ? Am. Nat. Robertson, R. 1961. The feeding of Strombus and re• 93: 145-159. lated herbivorous gastropods. Notulae Naturae 343: Kohn, A. J. 1959. The ecology of Conus in Hawaii. 1-9. Ecol. Monogr. 29: 47-90. Sanders, H. L., E. M. Goudsmit, E. L. Mills, and G. E. Lindeman, R. L. 1942. The trophic-dynamic aspect of Hampson. 1962. A study of the intertidal fauna of ecology. Ecology 23: 399-418. Barnstabk Harbor, Massachusetts. Limn. Ocean. 7: 63-79. MacArthur, R. 1955. Fluctuations of popula• Scheltema, R. S. 1961. Metamorphosis of the veliger tions, and a measure of community stability. Ecol• larvae of Nassarius obsoletus () in response ogy 36: 533-536. to bottom sediment. Bioi. Bull. 120: 92-109. -- and J. W. MacArthur. 1961. On bird species Stehouwer, H. 1952. The preference of the slug diversity. Ecology 42: 594-598. Aeolidia papillosa (L.) for the sea anemone M etridium Magalhaes, H. 1948. An ecological study of of senile (L.). Arch. Neerl. Zool.10: 161-170. the Busycon at Beaufort, North Carolina. Ecol. Tate, M. W. and R. C. Clelland. 1957. Nonparametric Monogr. 18: 377-409. and short-cut statistics. Danville, Ill: Interstate Margalef, R. D. 1958. Information theory in ecology. Printers and Publishers, Inc. General Systems 3: 36-71. Turner, H. J. 1951. Fourth report on Investigations Menzel, R. W. 1955. Annotated check-list of the ma• of the Shellfisheries of Massachusetts. Comm. Mass., rine fauna and flora of the St. George's Sound• Dent. Conserv., Div. Mar. Fish. Apalachee Bay Region, Florida Gulf Coast. Florida --. 1955. How clam drills capture razor clams. State Univ. Ocean. Inst. 61: 1-78. Nautilus 60: 20-22. --and F. E. Nichy. 1958. Studies of the distribu• --. 1958. The effect of nutrition on the color of the tion and feeding habits of some oyster predators in callus of Polinices duplicatus. Nautilus 72: 1-3. Alligator Harbor, Florida. Bull. Mar. Sci. Gulf and Wells, H. W. 1958a. Predation of pelecypods and Carib. 8: 125-145. gastropods by Fascia/aria hunteria (Perry). Bull. Mar. Paine, R. T. 1962. Ecological diversficahun in sym• Sci. Gulf and Carib. 8: 152-166. patric gastropods of the genus Bus)•com. Evolution 16: ---. 1958b. Feeding habits of .Uurex fulvescens. 515-523. Ecology 39: 556-558. --. In press. Feeding rate of a predaceous gastro• Willcox, J. 1895. The habits of Florida littoral mol• pod, Pleuroploca gigantea. Ecology. lusks. Nautilus 8: 79-80.

COMPARISON OF TEMPERATURE AND MOISTURE RESPONSES OF THE SNAIL GENERA AND ONCOMELANIA1

HENRY VANDER ScHALIE AND LowELL L. GETZ Museum of Zoology, University of Michigan, Ann Arbor, and Department of Zoolog)' and Entomology, University of Connecticut, Storrs

INTRODUCTION (1948), Abbott (1948), and others stressed the The relationship between amnicolid snails be• need for basic studies of amnicolid snails and espe• longing to the American genus Pomatiopsis and cially species in the genus Pomatiopsis. Berry and the Oriental genus Oncomelania has been known Rue ( 1948) found that P. lapidaria could be in• for a long time. Increased interest in the latter fected with the Chinese strain (personal communi• group was stimulated when they were recognized cation) of Schistosoma japoniwm; van der Schalie as the hosts for the Oriental blood fluke, S chisto• and Basch (unpublished data) found development soma japonicum. It was somewhat later that ac• to the sporocyst stage in one of 25 P. cincinnatien• tive work on the American Pomatiopsis was ini• sis, which had been exposed to miracidia of the tiated, particularly at the close of the war when Japanese strain of S. japonicum. Extensive work service men, as well as dogs which had been loaned has been done on Oncomelania in such centers as to the Armed Forces, returned to the continental the 406th Medical General Laboratory in Japan United States from Pacific regions infected with (Hunter III, Ritchie, Williams, et al.), the Philippine 9 team in Palo, Leyte (Pesi• schistosomiasis. Stunkard ( 1946), Berry and Rue W.H.O. gan, Hairston, et at.), and in other laboratories. 1 This work was sponsored by the Commission of Para• There is general agreement as to the need better sitic Diseases, Armed Forces Epidemiological Board, and supported by The Office of the Surgeon General, Depart• to understand the life history and ecology of the ment of The Army. Oncomelania snails. 74 HENRY VANDER SCHALIE AND LOWELL L. GETZ Ecology, Vol. 44, No. 1 Intensive work with both local speciesof Poma- is consideredwith respect to its normal zoogeo- tiopsis (P. lapidaria and P. cincinnatiensis) was graphic range. begun in the laboratory of the senior author about 6 years ago. For referencewe were fortunate in TEMPERATURE RESPONSES havingavailable an excellentstudy of the amnicolid Preferences snails of Michigan by E. G. Berry (1943). In A temperaturegradient was establishedusing addition, some unusually good colonies of both equipment similar to that described by Getz speciesof Pomatiopsisare available in the vicinity ( 1959). The apparatus consisted of a trough of Ann Arbor. With this large reserve of local (made of 1/10 inch tinned-copper) 1 X 1 X 24 material and with facilities for culturing Oncome- inch, with a 1 X 1 X 2 inch water-tight compart- lania (only a few specimensof 0. hupensiswere ment at each end. Each compartmentwas pro- available for use, however), a wide variety of vided with an inlet and an outlet tube. The bot- studies has been possible. Several investigations tom of the trough was covered with wet blotter have centered on P. cincinnatiensis dealing with paper marked into 24 sectionsof 1 inch. A glass its distribution, ecology and life history (van der cover, held in place by a series of flanges, was Schalie and Dundee 1955, van der Schalie and placed 3/8 inch above the floor to keep the snails Getz, in press), its morphology (van der Schalie on the sameplane so as to avoid vertical tempera- and Dundee 1956), its egg-laying habits (van der ture gradients. The top of the trough was covered Schalie and Walter 1957), and the comparative with a piece of plate glass which was in turn difference in moisture requirementsbetween the covered by opaquepaper. Nine thermister ther- young and adults (van der Schalie and Getz mometerswere taped to the bottom of the trough 1961). Likewise, studies of P. lapidaria to date (under sections 1, 3, 6, 9, 12, 15, 18, 21, and 24) centeredon its ecology, morphology and distribu- to determinetemperatures along the trough. The tion (Dundee 1957, van der Schalie and Dundee entire trough was packed in a box of cotton (to 1959). insulate it againsttemperature influences from the Many difficulties were experiencedin culturing outside). species of Oncomelania and Pomatiopsis in the To create a gradient, water heated by passing laboratory. \Vhile efforts were made to duplicate through a coil in a beaker of boiling water was as nearly as possible the conditions observed in circulated through the compartmentat one end, the field for each species, there were no data while water cooled by passagethrough coils in a available to indicate the range of tolerance to chest of crushed ice circulated through the other. variables of such conditions as temperature,mois- The temperature of water going through each ture of air and substrate, or ability to tolerate terminal compartmentwas varied by increasingor drowning or desiccation. It was observedthat the decreasingthe rate of flow through each coil and species varied in their reactions to the environ- compartment until a uniform gradient between mental conditions, but few data were available to suitable extremeswas producedalong the experi- determine the parametersto ecological conditions mental chamber. Once such a gradient was at- for the several species. Without such knowledge tained ( 36-6o C), an experiment was conducted it is difficult to culture certain of the speciesand by placing snails of one species in the 3 central sections. The one cannot interpret behavior in an effort to com- 2 glass covers were then put back in place and the box was pensatefor unfavorable conditions. P. cincinna- darkenedto avoid any possible influence of light. After 6 hours the tiensis proved to be most difficult to maintain; numbers of snails in each section were recorded. hence it received more attention (van der Schalie Two species of Pomatiopsis, P. lapidaria and P. and Getz 1961 and in press). It was found that cincinnatiensis,and 4 speciesof Oncomelania, 0. P. lapidaria was most similar in its responseto quadrasi, 0. nosophora, 0. formosana, and 0. moisture conditions to the 4 species of Oncome- hupensis, were tested. The mean temperatures lania. It is also similar in that it is a biennial preferred by the 6 speciesvaried from 21 oc for species, while P. cincinnatiensis has been shown P. cincinnatiensis and 0. hupensis to 26oC for to be an annual. In the experimentsthat follow, 0. quadrasi (Figure 1). The range of tempera- the data indicate several striking differences be- ture selectionwas mainly between12°C and 30°C tween the ecological tolerancesof the 2 speciesof for most species excepting a few isolated snails Pomatiopsis; it is also evident that each of the in the lower ranges; 0. quadrasi showeda second species of Oncomelania and Pomatiopsis tested peak of distribution at 18°C, probably indicating has rather definite toleranceranges which tend to that the individuals in question were chilled to a identify the species. In somecases, the optima are point where they were unableto move back toward different from what one might expectif the species the warmer end of the gradient. This inability to Winter 1963 RESPONSESOF THE SNAIL GENERA 7S

(/) ..J c:t z (/)

3634 30 26 22 IS 14 10 36 34 30 26 22 18 14 10 36 34 30 26 22 18 14 10

I.J.. 0 26 24

22 EcmcmnotrenSJs 20 20 18 16 14 12

3634 30 26 22 18 .. 10 6

TEMPERATURE GRADIENT FrG. 1. Temperaturepreferences of Oncomelania and Pomatiopsis. Distribution of individuals after 6 hours in a temperaturegradient of 36•c-6•c. The arrow indicates the mean temperaturepreferred. move was confirmed by using another,more grad- 3 layers of wet filter paper in a 15 em petri dish ual gradient, ranging between l7°C and 33°C, and the dish was placed in a freezer at -5°Cfor thus giving the snails a chance to retreat before 3 hours. One day later the number of snails still becoming immobilized. 0. quadrasi in both tests alive, in decreasingorder of tolerance, were as was aligned between20° C and 30°C, with a mean follows: P. lapidaria, 17; P. cincinnatiensis, 17; of 26°C (Figs. 1 and 2). 0. hupensisalso showed 0. nosophora,14; 0. formosana, 12; 0. quadrasi, a somewhatrestricted range of temperaturepref- 18 erence. This observation of restriction in range may be related in part to fewer data; a rather definite avoidance of temperaturesabove 26°C !!!. "6 14 appearsto occur, however. Although the remain- c: ing speciesall had a similar range of temperature (/) 12 Q. quadrasi preferences,fewer P. cincinnatiensismoved above 0 10 ~ 28°C than did the other species, while 0. for- Q) .0 8 mosana appeared to avoid temperaturesbelow E l4°C to a greaterextent. z::J 6 Tolerances 4 Low temperature 2 A measurefor the toleranceof low temperatures was obtainedby 2 methods: ( 1) a short exposure 29 27 25 23 21 19 17 to extremelylow temperature( -S°Cand -7°C), Temperature (°C) and (2) a longer exposure to temperaturesof Frc. 2. Temperaturepreferences of Oncomelaniaquad- rasi at a gradient more gradual than that used in Fig. 1, aroundooc and of soc. In the first experimentSO after 6 hours. The arrow indicates the mean temperature snails of each of the S speciesused were placed on preferred. 76 HENRY VANDER SCHALIE AND LOWELL L. GETZ Ecology, Vol. 44, No.1 5. A 3-hour exposureto -7°C resulted in the dish removed. The procedureof raising the tern- deaths of all individuals of each speciestested. peratureby 1oc and removing a dish every half For longer exposureto low temperature,50 in: hour was continued up through to 48°C. The dividuals of each of the 6 specieswere placed in snails were checked18 hours later and again after a petri dish, as above, and maintained at -2°C 30 hoursto determinethe numberstill alive (Table to +1 oc for 120 days. In this test, again, P. 1). lapidaria was best, and 0. quadrasi least, able to TABLE I. Survival of Oncomelaniaand Pomatiopsissnails toleratethe low temperature(Figure 3). A simi- 18 and 30 hours after cumulative exposuresto tempera- lar procedure, using 5 species, was followed to tures increased by l"C, from 34"C to 48"C, every 30 determine survival at soc. During this experi- minutes

KEY NUKBBR OP SNAILS OUT or 5 SURVIVING A.ITBR EXPOSURII +-+0.-il ••••• 0 ...... 0. 0. 0. P. cincin- P...... __ _ -·-0.- Hours after quadraai no•ophora formooafiiJ naliemia lapidaria expoaure ', -·--P.-0.-- -- P. lapiobia 18 30 18 30 18 30 18 30 18 30 40 ' ' -.... _, ------... Tomporature•a > ' ', 40• ...... 5 5 5 5 5 5 5 5 5 5 :J 30 c ' ' 41...... 6 4 5 5 5 5 5 4 4 2 ' 42 ...... 5 4 5 5 5 5 4 2 2 0 Ill: ' ' ... ' 43 ...... 3 2 5 5 5 5 3 2 1 0 ~ zo ' ' ' ' 44 ...... 2 0 3 3 4 4 2 I I 0 ii! 45 ...... 3 2 3 1 2 I 0 0 0 0 46 .•...... 0 0 2 0 2 I 0 0 0 0 47 ...... 0 0 0 0 0 0 0 0 0 0 48 ...... 0 0 0 0 2 0 0 0 0 0

15 30 45 10 75 tO 105 120 • No mortality between34°C aod 40"C, ineiUBive. DAYS FIG. 3. Survival in days of Otu:omelaniaand Pomatiop- mortalities ranged between 41 sis maintainedat a temperaturefluctuating between-2"C The onset of oc and +1"C. and 44o C for different species, total mortalities occurred between 44o C and 48o C. P. lapidaria ment, the filter paper lining the bottom of the was least able to tolerate higher temperaturesof petri dish was replacedand the disheswashed once the speciesexamined. In the order of the least a week. Thesedishes were inspectedperiodically to the greatest,the relative ability of the remaining for 40 days; the numbersof snails still alive at the speciesto toleratehigh temperatureswas recorded end of this time, in decreasingorder of tolerance, as follows: P. cincinnatien-sis, 0. quadrasi, 0. were as follows : P. lapidaria, 50; 0. formosana, nosophora,and 0. formosana. 0. formosanawas 50; 0. nosophora, 48; P. cincinnatiensis,45; 0. only slightly more tolerant than 0. nosophora. quCJdrasi, 28. Tolerance to longer exposures at 30°C and It appearsfrom these tests that 0. quadrasi is 35°C was also determined. Fifty individuals of markedly less able than the other speciesto toler- a specieswere placedin a petri dish, as in previous ate low temperatures,while P. lapidaria is at the tests. The filter paperwas changedand the dishes other end of the scale. washed at weekly intervals. The dishes were placed in constanttemperature chambers and in- High temperature spected periodically to determine the number of The tolerance of high temperaturesof 5 snail animalsstill alive. 0. formosana was markedly specieswas determinedby 2 methods: ( 1) short more tolerant to prolonged high temperature exposuresto high temperatures( 34o C to 48o C), (35°C) than any of the other speciestested (Fig- and (2) longer exposuresto less extremetempera- ure 4). While somewhatmore tolerant than the tures (30°Cand 35°C). To determinetolerance remaining species,0. nosophorawas considerably for short exposuresat high temperatures,5 indi- less so than 0. formosana. Both P. lapidaria and viduals of each specieswere placed on wet filter P. cincinnatiensisare relatively intolerant to high paper in a stendor dish (with covers in place). temperatures,P. lapidaria slightly less so than P. For each species15 such disheswere placedin an cincinnatiensis. 0. quadrasi appearsintermediate oven and the temperatureset at 34°C. The ani- between the Pomatiopsisand the other Oncome- mals were maintainedat that temperaturefor 30 lania in ability to tolerate prolonged high tem- minutes, then 1 dish was removed and the oven peratures(Fig. 4). Tests at 30°Cfor the 4 less temperatureraised to 35°C. This temperature resistantspecies confirmed this order of longevity was again maintainedfor 30 minutes and another (Figure 5). Winter 1963 RESPOXSES OF THE SNAIL GENERA 77 7 KEY -P.- P cincinnotiensis- ~ 40 -- P.lapiclaria ..... o .,._i. O.quodrosi ------/\ 1&1 -·- o...... 6 > -•-0...... 0. formoso ~50 no...... I \ 1.. ------J II \l a:: I l 1&1 -5 I \ ~ 20 I \ :::1 e z u II 'I 10 - I I I \ -5i4 I \ I \ E I \ 5 10 15 20 25 50 55 40 ~ DAYS ~3 II '\ I \ FIG. 4. Survival in days of Oncomela11ia and Poma- I • \ tiousis maintainedat a temperatureof 35"C. I . \ \. '' I : ' 50 ~----~.~--r·-·-·, I i \ ', .. ""··~·. J.-- ·-·-· ...... I ! \ ', ·... ~ l',, ,) i '\. " .... 40 'Il ', ,, i \ > ·.'·.' ::::i ·.' KEY <( ·.'·., I " ...... J \ ...... , a:: 30 ·., - P. cincinnationsis I ...... P'· ·., ..... 0. quadrali IIJ ., , ...... ,... I I I I I m -- p. lapidaria 0 :::E 5 10 15 20 25 30 35 'r. -·- O.nosophora i 20 •..... Temperature (°C) I •, I •, FIG. 6. Movement in relation to temperature. Aver- .. age distances covered by Oncomelania and Pomatiopsis .I ·•, 10 I •, (10 individuals each for 10 min) under exclusion of light. \ ··· .... I ••• ••• 0 movement dropped off. P. cincinnatiensishad a 0 10 20 30 40 DAYS wider range. It displayed a considerableamount FIG. 5. Survival in days of Oncomela11ia and Poma- of movementat temperaturesas low as 10°C; its tiopsis maintainedat a temperatureof 30"C. greatestmovement was recorded at 30°C and it was still high at 35°C. This speciesand also 0. Movement quadrasi showed greater activity than the others. Data were obtained on 10 individuals of each species;2 snails at a time were placed in the cen- Moisture Responses ter of a dry petri dish. The dish, which had been Preferences previously conditioned to the temperatureused in To determinepreferences for substratemoisture the experimentfor at least 30 min, was placed in the snails were placed on a gradient ranging from a constanttemperature cabinet for 10 min. The saturation to approximately 20% of saturation. snails were then removed and talc sprinkled into Such a gradient was establishedby placing 15 the dish to reveal the trails left by the snails. ( 1~ X 1 inch) pads ( 10 thicknessesof paper These trails were measuredwith dividers. The toweling) in a long tin box ( 24 X 1 X 1 inch) ; a same individuals were exposed, in sequence,to gap of approximately 1/3 inch was left between temperaturesof 5, 10, 15, 20, 25, 30, and 35°C. the pads. To establish a moisture gradient, 10 The temperaturechambers were darkenedand all drops of water were placed on the center pad and had relative humidities of 80 to 85% except the the amount increasedby 5 drops per pad, pro- 35°C chamber, which had a relative humidity of gressively,toward both ends. Th,is method estab- 95%. Betweenthe testing periodsthe snails were lished a gradientof 10 through 45 drops from the placed in distilled water (25°C) for 5 minutes center to each end. The resulting percentagesof and the shells dried with a cloth before the start saturationranged from approximately100 at each of the next trial. end to 20 at the middle. Five individuals of each Of the 6 speciestested, all except P. cincinna- of the 6 species tested were placed on each pad tiensis displayed the same general pattern (Fig- and the box was coveredwith a glass plate sealed ures 6 and 7). In the other 5 specieslittle move- with petrolatum; a dark doth cover eliminatedthe ment occurredup through 20°Cwith' most move- possible influence of light. After 24 hours the ment taking place at 25°C, while at 30 and 35°C distribution of the snails on the padswas recorded. 78 HENRY VANDER SCHALIE AND LOWELL L. GETZ Ecology, Vol. 44, No. 1 trough and had not yet reoriented themselves) ; P lopidorio ---- the others also were distributed in a way that in• 4 0. hupensis ------dicated an avoidance of the higher moisture condi• 0. nosophoro ...... tions. Tolerances Immersion All 6 species were tested. Two individuals of a given species were placed in a one dram vial closed with a metal cap punctured by 8 small holes. The vials were filled with distilled water and then immersed in a shallow dish of distilled water at 2JOC. Ten individuals were utilized for 0. formosana and 0. hupensis and 30 for all other species. The average survival times in hours, arranged in the order of increasing lon• gevity, are as follows: P. cincinnatiensis, 65; P. lapidaria, 85; 0. nosophora, 130; 0. quadrasi, 140; 0. hupensis, 140; 0. formosana, 150. In addition to the above experiment, 2 others were made to determine differences between P. Since the method of establishing a moisture lapidaria and P. cincinnatiensis. The first con• gradient was rather crude, the data have been sisted of placing 30 individuals of each species in used to compare the moisture preferences of the 6 vials as described above, but maintained at ooc species rather than to obtain absolute preferences instead of 27oC. for each species. All 6 species avoided the satu• P. lapidaria had an average survival time of rated pad; 0. quadrasi, 0. hupensis, and P. lapi• approximately 500 hours, while P. cincinnatiensis daria appeared to be equally distributed over the survived only 365 hours. In the second experi• remainder of the gradient while the remaining 3 ment, one individual of each species was placed in species appeared to avoid the moist half of the a corked, 34-dram vial of distilled water at 27°C. gradient (Figure 8). P. cincinnatiensis had the Air bubbles were eliminated with a small pin. most narrow range of preference and also tended Twenty individuals of each species were utilized. to avoid the higher moisture conditions more than The survival times were SO hours for P. lapidaria did any other species. 0. hupensis had the widest and 20 hours for P. cincinnatiensis. spread over the gradient. All species tended to There is, therefore, a marked difference in the avoid the 100% pads (those P. cincinnatiensis ability of the genera Pomatiopsis and Oncome• that were found on the 100% pads probably repre• lania to withstand immersion in water; all 4 spe• sented individuals that encountered the end of the cies of the latter are more tolerant of submergence

0 . nosophoro 0. quadrosi 0 formosano 0. hupensos P. lap1dario P. cincinnatienSis

(/) .....1

0::: IJJ III :::!; z:::>

SUBSTRATE MOISTURE (PERCENTAGE OF SATURATION) FIG. 8. Substrate moisture preferences of Oncomelania and Pomatiopsis. Distribution after 24 hours, under exclusion of light. Winter 1963 RESPOKSES OF THE SNAIL GENERA 79 than either of the former. P. cincinnatiensis is KEY FEMALES much less resistant to drowning than is P. lapi- - • - 0. nosophoro .... - •- 0. formosona daria. :I: • • • • • • 0. quodrosi ~tOO --- P. lopidaria - P. cincinnatiensis 3: 90 ~·~ Desiccation '\.,. -:::~::::.-.-. Two methodsof desiccationwere used on the 5 ~ 80 g 70 ··-~-~-~-~-·---.:::.:._·-·-·-·-·-·-·-·-· speciesof snails tested at a constanttemperature -·-·- ;;J. 60 o "'"'·~... ·-·-·- of 25 C. ( 1) Fifty snails of each species were ;!;~ placedin a petri dish in which dry filter paper was ;;: 40 "'0 ···~-~-~-~.~------·-~-~-~·-·-·-·-·-·-·- used as a desiccant. The dish was then main- u..30 --- 0 20 ---- tained at a relative humidity of 30 to 35%. The .... --- it 10 snails were examineddaily to determinethe num- ·········· o+----.---2--~-3---.--.--~~--.-~6--~~-. ber that remained alive ; the specimens judged living were thosethat showedmovement of viscera DAYS FIG. 10. Tolerance to desiccation. Loss of weight of or heart. (2) Ten males and 10 females of each female Ollcomelmlia and Pomatiopsis at 0-5% relative species, in an open 9-cm petri dish (no filter humidity at 25 • C. paper),were placed in a desiccatingchamber with 0 to 5% RH. They were weighed at frequent in- KEY MALES tervals to determinethe rate of desiccation. -.- 0. nosophoro .... -,- 0. formosono :I: --- P. lopidorio Both experimentsindicate the order of tolerance lO ;;jiOO • • • • · · 0. quodrosi - P. ClnClnrlO!IeflSlS to desiccationto be, from least to greatest,as fol- 3: 90 lows: P. cincinnatiensis,0. quadrasi, P. laJpidaria, ~~ ...... ~80 ...... ;.;:::-·-·-. 0. formosana, and 0. nosophora (Figures 9-11). g 70 '-. -·-·- The deaths of the last survivors among the first ;;J_eo ' .... -·-·-· ·-·-. 4 speciestested in the first series ranged from 6 ;!;~ -·,·-·-·-·-.::_-,·--.·- "'0: 40 ·-·-·· to 30 days while some 0. nosophora were still 0 --- -·-·-· ... 30 --- ,,_ alive on the 42nd day. In the 2nd series, loss in 0 --, 20 ...... body weight on the last day of observation (7th) ';;! 10 ...... rangedfrom 40 (females) and 60 (males) %, ap- ol_---,r-r--.--~-.r-.r-o-_;=:;=~6==~~==, proximately, to more than 95%. In Oncomelania DAYS the rate of desiccation was greater for the males FIG. 11. Tolerance to desiccation. Loss of weight of than females,up to the 4th day in 0. quadrasi and male Oncomelaniaand Pomatiopsisat 0-5% relative hu- 0. formosana, and increasingly the 5th to 7th midity at 25·c. day in 0. nosophora (Figures 10 and 11); there the use of salt solutions. Humidities were checked was no sexual difference in the rates of desicca- with Serdexlaboratory hygrometers. Two snails tion of P. lapidaria or P. cincinnatiensis. were placed in the center of a clean 9-cm petri Movement dish and the dish placed on a wire floor above the Relative humidities of 95, 85, 75, 65, and 259'o salt solution in the aquaria. A plate glass cover (at 26°C) were establishedin covered aquariaby (sealed with petrolatum) was opened only wide enough to insert the dish so that the air in the chamber would not be influenced too greatly by KEY - P. cincmot.ensis the room air. After the cover was replaced the -- P. lapidcrio ~0 :~.:_:-·-·-· ...... '...... 0.- entire aquarium was covered with an opaque - • - 0. formosano '~ ·, -·,., -. - 0. nosophono cloth. Each trial lasted 10 min. The movement ·: \ 40 . ·...... of 10 individuals ( 5 males and 5 females) of each \ w I·. species was determined for each of the above > :J 30 ""\.-' ~ ...... ' humidities. The amount of movementwas meas~ .. ... ', \ •• I \ ' ured by powderingtalc into the bottom of the dish ·. \ . \ at the end of a run. The slime deposit marking \ \ \, ·,...... \ \ ·,~ ·-· ...... eachsnail's trail thus becamevisible and was meas- : I \ ...... ured with dividers. 10 ~- \ ·, ·, ···· ...'\ ·...... , ·-· ...... To interpret the data relating to movementthe o+---~.----'~,·~~----.----·'T·-'~·=-~·~----~---. following assumptionswere made concerningthe 12 18 24 30 36 42 behavior of thesesnails. At the higher, favorable DAYS humidities individuals will display a moderate FIG. 9. Toleranceto desiccation. Survival of Oncome- lania and Pomatiopsisin days at a relative humidity of amount of movement. As the humidity decreases 30-35% at 25°C. a percentageis reachedthat is unfavorable. At 80 HENRY VANDER SCHALIE AND LOWELL L. GETZ Ecology, Vol. 44, No. 1 that point the snail is stimulated and begins mov• Since there were marked differences in the ing about; the humidity is still high enough, how• moisture requirements of the species of Oncome• ever, so as not to hamper movement. Hence, one lania and Ponwtiopsis, a study was made of the would expect the greatest amount of movement gill structure of these species to see if such differ• at the point at which the humidity becomes un• ences might be related in part to their mode of favorable. At lower humidities stimulation may respiration. also take place, but the animal is less able to move Gills were dissected from individuals of all 6 and less movement occurs. Eventually a point is species. The number of gill filaments was counted reached at which the animals withdraw into their and the shape of the giils also noted. In dissection shells and become inactive. the snails were relaxed with nembutal, fixed in The results of these tests indicate that the 6 Bouin's solution (which also removed the shell), species fall into 2 groups (Figure 12). The first and the animals preserved in SO% alcohol. The results are given in Table II. KEY • • • • • 0. quodrusi TABLE II. Number of gill filaments in relation to size in - 0. hupensis Oncomelania and Pomatiopsis - P. c:incmat- -·- 0. naoophoro -- P. tapdario INDlVJDUALS AVERAGE NUMBER OF -•- 0. lormosona ------Species ------Filament.. Number Size in mm Pairs gill permm filaments ------length 0. hupen•i• . . 5.7 49 8.6 0. formosana ...... 5.1 49 9.6 0. nosophora. 6.4 54 8.4 4.5 34 7.5 3.4 32 9.3 2.3 29 12.6 0. quadrasi ...... 8 4.6 42 9.1 2 1.6 22 13.5 RELATIVE HUMIDITY P. lapidaria ...... 6.0 25 4.2 FIG. 12. Movement in relation to humidity. Average P. rincinnatiensis ...... 5.5 17 3.1 distances covered by Oncomelania and Pomatiopsis (10 4.5 15 3.3 individuals each for 10 min) under exclusion of light. 20 3.5 14 4.1 II 2.5 14 5.6 I 1.5 9 6.0 group, comprising 0. nosophora, 0. quadrasi, and P. lapidaria, has a more restricted tolerance range; a relative humidity of 85% already appears to be All species of Oncomelania have a larger num• unfavorable, as maximum movement takes place ber of gills than the 2 species of Pomatiopsis at that range; activity then falls until no movement studied. 0. quadrasi and 0. nosophora, of which occurs at 25%. The other group, P. cincinnatien• young were available for study, appear to have a sis, 0. hupensis, and 0. formosana, is not yet relatively smaller gill system in the adults than in adversely affected by humidities of 857o; the the young, as was also observed in P. cincinna• greatest movement occurs at 75%. There was tiensis. Since the young of these 2 species are still considerable movement at the lower limit of known to live in water, an increase in the impor• the experiment (257o). These 3 species, there• tance of pulmonary respiration in the adults may fore, appear to be more tolerant to lower hu• be indicated. It was observed that P. lapidaria midities. has a relatively small giii system, but it also shows a preference for more moist situations. Hence, a Comparison of Respiratory Systems correlation does not appear to exist between the It was found earlier (van der Schalie and Getz habitats of the various species and the development 1961) that there appeared to be a relationship of pulmonary respiration. between development of the gill system (number of gill filaments) and the moisture requirements DISCUSSION of young and adult P. cincinnatiensis. In the The 2 species of Pomatiopsis were characteris• younger, smaller individuals there were more gill tically more tolerant of low temperatures and less filaments per unit of body mass than in the larger tolerant of high temperatures than were the 4 spe• ones. Since the larger animals were found to re• cies of Oncomelania. P. lapidaria was less able quire less moisture, it was assumed that there was to survive exposure to high temperatures than was a transfer from gill to pulmonary respiration in P. cincinnatiensis. Although P. cincinnatiensis this species, the change coming about as individ• showed a more marked preference for a lower uals approach adult size. temperature than did P. lapidaria, it lives in a Winter 1963 RESPONSES OF THE SNAIL GENERA 81 relatively exposed situation in nature and must Since it occupies the driest habitat of any of the frequently encounter high temperatures (when the species studied, one would anticipate such a pref• sun shines on the bank), but usually only for short erence as well as a tendency to be less able to with• periods. P. lapidaria inhabits a more sheltered stand drowning and perhaps also to be better able situation and normally would not be exposed to to tolerate desiccation. The 2 former conclusions excessively high temperatures. During the winter were shown to be true; however, the desiccation P. cincinnatiensis hibernates (aestivates) under experiments indicated that this species was the leaf litter or dormant grassy vegetation above the most susceptible to drying, even more so than 0. river banks (van der Schalie and Dundee 1955). quadrasi, which, in nature, is found in an almost The temperatures in such situations normally do aquatic situation. It is evident, therefore, that not go much below freezing for extended periods. P. cincinnatiensis requires a habitat which affords The seepage areas in which P. lapidaria occurs are an optimum substrate moisture at all times. This normally frozen for extended periods during the animal cannot tolerate protracted fluctuations in winter. The moist soil and decaying vegetation moisture conditions. The river banks upon which freezes during the winter and, owing to the insu• it lives usually meet these requirements. Regard• lation of the dead vegetation covering the surface, less of the degree to which the river fluctuates, remains frozen. The ability of P. lapidaria to with• there usually is a zone on the bank which has the stand low temperatures better probably reflects the proper moisture. Observations indicated that differences in temperatures in the habitats of these these snails move up the bank to avoid extended 2 species. periods of flooding. Their inability to cope with That the species of Oncomelania are less toler• conditions that lead to drowning, compared with ant to low temperatures may be a reflection of the P. lapidaria, also .serves to emphasize some of the situations in which these species occur in nature; differences in the habitats of the 2 species of i.e., these animals are not subjected to extremely Pomatiopsis. Consequently, P. lapidaria, which low temperatures. The relative ability of each inhabits low, marshy situations, can withstand of the 4 species to tolerate low temperatures cor• extended periods of inundation, as shown by its responds to the range of latitude of their geo• resistance to drowning. graphic distribution. 0. nosophora and 0. hupen• Among the species of Oncomelania, 0 quadrasi, sis, the most northern species, are most tolerant which was shown to prefer very moist situations, to low temperatures, while 0. quadrasi, from the was most susceptible to desiccation. On the other Philippines, is the least; 0. formosana, from Tai• hand, 0. nosophora, which also lives in a moist wan, is intermediate. situation, proved to be very tolerant of desiccation. The degree of tolerance to high temperatures This characteristic permits it to withstand ex• among the species of Oncomelania shows no such tended periods of drying without appreciable mor• pattern. If one uses the same line of reaspning tality. and considers the natural distribution pattern, 0. It has been established that the aquatic pulmo• quadrasi, the southern most species, should be nate snails which carry other human schistosome most tolerant to high temperatures; however, it species are able to lose their infection under cer• is less tolerant than either 0. formosana or 0. tain conditions of chilling or desiccation; the snails nosophora (data are not available for 0. hupen• are thus rid of the parasite without being killed sis). Evidently, there must be modifying factors themselves. It would, therefore, be of interest to in the habitat of 0. quadrasi so that it actually learn what influence the variations in tolerances inhabits situations in which temperatures seldom of the amnicolid snails to ecological conditions go as high as those encountered by the more have upon the S. japonicum parasites they carry. northern species. Its inability to tolerate ex• To a certain extent the parasites are undoubtedly tremes of temperature was also reflected in the adapted to the stresses of desiccation and variations experiments designed to permit these species to in temperature. It seems possible that such an select the temperature preferred. 0. quadrasi had adaptation to the varying physiological environ• the narrowest range of preference of any of the ment within the Oncomelania species from differ• 6 species examined. It appears, therefore, that ent regions may account, in part, for the strain 0. quadrasi lives in a habitat in which there is differences encountered in S. japonicum from dif• relatively little fluctuation of temperature and ferent countries. which is particularly shielded from high tem• The Oncomelania used in the present study peratures. were, to the best of our knowledge, not parasi• Pomatiopsis cincinnatiensis had the most re• tized. The reactions to the several factors, such stricted range of moisture preference ; it also se• as temperature, humidity, substrate moisture and lected a drier substrate than the other 5 species. desiccation were those of healthy, normal adults. 82 HENRY VANDER SCHALIE AND LOWELL L. GETZ Ecology, Vol. 44, No. 1 Studies of tolerances of infected snails to factors drowning than the Oncomelania; P. cincinnatiensis in their environment would be of interest. was less tolerant than P. lapidaria. The order of toleration to desiccation, from the SuMMARY least to the greatest, was as follows: P. cincinn/11- tiensis, 0. quadra:si, P. lapidaria, 0. formosana and A study was made of the temperature and mois• 0. nosophora. The male Oncomelania were more ture responses of the 2 American species of Poma• tolerant to desiccation than tiopsis (P. lapidaria and P. cincinnatiensis) and the females; no dif• the 4 nominal Oriental species of Oncomelania ferences were observed among the sexes of Ponw• ( 0. nosophora, 0. formosana, 0. quadrasi and 0. tiopsis. hupensis). Movement of the 6 species was measured When subjected to a temperature gradient rang• through a range of 5 relative humidities (95, 85, ing from 6°C to 36°C, the mean temperatures 7 5, 65, and 25%) at 26 o C. Three species ( 0. preferred by the 6 species tested varied from 21 oc nosophora, 0. quadrasi and P. lapidaria) were less for P. cincinnatiensis and 0. hupensis to 26°C for tolerant of the lower humidities, while P. cincin• 0. quadrasi. The range of selection was between natiensis, 0. hupensis and 0. formosana remained 12°C and 30°C. When the animals were tested active in the lowest range tested. for their ability to tolerate low temperatures, i.e., a short exposure to extremely low conditions AcKNOWLEDGMENTS ( -5°C and -7°C), the order of response from ln order to carry out a program involving comparisons the least tolerant to the most was, as follows : ( 1) of Oriental snail species with related forms in Michigan, 0. quadrasi; (2) 0. formosana; (3) 0. n-oso• it was necessary to have stocks of the foreign species sent phora; ( 4) P. to us. It was both helpful and encouraging to receive cincinnatiensis; and ( 5) P. lapi• assistance in obtaining stocks from staff in the following daria. All were killed by a 3-hour exposure to centers: Mr. James Williams of the Medical General -7°C. In exposures to high temperatures (34°C Laboratory ( 406) in Japan (supplied Oncomelania noso• to 48°C) the onset of mortalities came between phora); Dr. Robert E. Kuntz of the U. S. Naval Medical Research Unit No. 2 (supplied Oncomelania formosana); 41 o C and 44 o C with P. lapidaria least able to tol• and Mr. Bonifacio C. Dazo and Mr. Ricardo Moreno, erate high temperatures ; the remaining species members of the W.H.O. Philippine 9 team (supplied were less tolerant in the following order: P. cin• Oncomelania quadrasi). In the course of the work, Mr. cinnatiensis, 0. quadrasi, 0. nosophora and 0. Dazo gave generously of his expert assistance in main• taining and culturing these stocks. Mrs. Anne Gismann formosana. When the animals were exposed for assisted in the preparation of the manuscript; Mrs. Stan• longer periods to less extreme temperatures (30°C lee Lonsdale drew the graphs. This work would not have to 35°C), both the Pomatiopsis species were quite been possible without the assistance of each of them; we are grateful for sensitive with P. lapidaria slightly more so than their interest and help. P. cincinnatiensis; 0. nosophora was much less tolerant than 0. formosana; 0. quadrasi was in• REFERENCES termediate between the Pmnatiopsis and the other Abbott, R. T. 1948. A potential snail host of oriental schistosomiasis in North America (Pomatiopsis lapi• Oncomelania. daria). Proc. U. S. Nat. Mus. 98 (3222): 57-68. Movement was studied in relation to tempera• Berry, E. G. 1943. The Amnicolidae of Michigan: ture (at 5, 10, 15, 20, 25, 30, and 35°C). In all distribution, ecology, and . Misc. Publ. species excepting one, little movement occurred Mus. Zoo!., Univ. Mich., No. 57. before 20°C was reached; most movement oc• -- and R. E. Rue. 1948. curred at 25°C. The exception, P. cincinnatiensis, (Say) an American intermediate host for Schistosoma japonicum J. Paras. suppl. 34: 15. displayed considerable movement at temperatures Dundee, D. S. 1957. Aspects of the biology of Poma• as low as 10°C and it was still very active at 30°C tiopsis lapidaria (Say) (: Gastropoda: Pro• and 35 o C. This adaptation is a necessity for a sobranchia). Mus. Zoot. Univ. Mich., Misc. Pub!. snail subject to wide extremes of temperature in 100: 1-37. the late fall when it must find its way to the top Getz, L. L. 1959. Notes on the ecology of slugs: Arion circumscriptus, Deroceras reticulatum. and D. of the river bank where it hibernates. laeve. Amer. Midi. Nat. 61: 485-498. To determine substrate moisture preference, a Stunkard, H. W. 1946. Possible snail hosts of human gradient ranging from 20 to approximately 100% schistosomes in the United States. J. Paras. 32: 539- of saturation was established. All the species 560. avoided the region of the highest saturation; P. van der Schalie, H. and D. S. Dundee. 1955. The dis• tribution, ecology and life history of Pomatiopsis cin• cincinnatiensis had the narrowest range of prefer• cinnatiensis (Lea), an amphibious, operculate snail. ence and tended to prefer a drier substrate. Trans. Amer. Micr. Soc. 74: 119-133. The species of Pomatiopsis were less resistant to --. 1956. The morphology of Pomatiopsis cincinna- Winter 1963 LIFE HISTORY OF TROUT-PERCH 83 tiensis (Lea), an amphibious prosobranchsnail. Occ. moisture requirements. Trans. Amer. Micr. Soc. 80: PapersMus. Zoo!., Univ. Mich., No. 579. 211-220. --. 1959. Transectdistribution of eggs of Pomatiop- --. (in Press) Distribution and natural history of sis lapidaria Say, an amphibious prosobranch snail. Pomatiopsiscincinnatiensis. Amer. Midi. Nat. Trans. Amer. Micr. Soc. 78: 409-420. --and H. J, Walter. 1957. The egg-layinghabits of --and L. L. Getz. 1961. Comparisonsof adult and P omatiopsiscincinrwtiensis (Lea). Trans. A mer. Micr. young Pomatiopsis cincinrwtiensis (Lea) in respect to Soc. 74: 404-422.

SOME PHASES OF THE LIFE HISTORY OF THE TROUT-PERCH1

JOHN J. MAGNUSON2 AND LLOYD L. SMITH, JR. Department of Entomology,Fisheries and Wildlife, University of Minnesota, St. Paul

INTRODUCTION ( 130 to 160 ppm). There are no bays, and all The trout-perch,Percopsis omiscomaycus (Wal- shorelines are exposed to heavy wave action. baum), is one of the more abundantforage fishes Beachesare mostly sandy except in a few boulder in the larger lakes of midwestern United States areas along PonemahPoint and the south shore. and central Canadawhere walleye, Stizostedionv. The bottom soil is predominantlysand from shore vitreum (Mitchill), yellow perch, Perea ftavescens to a depth of 17 to 20 ft where it blends into an ( Mitchill), and coregonids predominate. It has organic muck. Aquatic vegetation is absent in been suggestedthat it may have considerableeffect shallow water on the east shore, but the north, on perch and walleye populations of these lakes. south, and west shoreshave bands of Scirpus sp. The present study describesgrowth, food habits, SO to 100 ft off the beaches. Outside of and population structure,year-class strengths, and re- mingled with the Scirpus, there are scatteredbeds productive capacity of the trout-perch in relation of Potamogetonsp. The depth of water increases to its population dynamics in lower Red Lake, gradually with a steep drop-off occurring between Minnesota. The physical characteristicsof Red the 8- and 15-ft contours. The 6-ft contour is at Lake and the ecology of commercial species are least 600 ft off the beachon most shorelines. describedby Smith and Krefting ( 1954), Pycha Trout-perch were sampled in June, July, and and Smith ( 1955), Van Oosten and Deason August, 1949-57. Quantitative samplesconsisted ( 1957), and Smith and Pycha ( 1961). of 346 bag-seinehauls from the lake in August Lower Red Lake, locatedin Beltrami and Clear- of 1955 and in the summers of 1956 and 1957, water Counties in north-central Minnesota (Fig- 108 otter-trawl tows in 1956 and 1957, and 57 ure 1) has an area of 255 mi2 and a max1mum seine hauls from Mud Creek in 1956. From 1949 through 1954, 134 additional non-quantitativeseine hauls were made. Shore sampleswere collected ~---- with 30- to SO-ft straight and bag seines6 ft deep with ,74-inch netting. After 1952 the 6 by 6-ft bag was lined with fine netting ( 10 meshes to the inch). To collect fish in water 4 to 20 ft in depth, a 10-ft otter trawl lined in the cod end with Ys-inch nylon bobbinet was towed at 3 mijhr. ' Four seining stations (Figure 1) were established ~~· on the south, east, west, and north shores of the \_ -· lake. Trawling stations were outside the seining stationson the north, east,and south shores. Ran- ---~, .... - dom subsamplesof fishes were saved from the ------seine hauls and all forage fishes were saved from the trawl tows. FIG. 1. The Red Lakes. This study was supportedin part by the U. S. Fish and Wildlife Service and the National Sci- depthof 35ft. The lake is isothermal,is subjectto ence Foundation. strong wind currents, and is moderately alkaline 1 Paper No. 4749, Scientific Journal Series, Minnesota GROWTH Agricultural Experiment Station, St. Paul 1, Minnesota. • Presentaddress: U. S. Bureau of Commercial Fish- Analysis of age and rate of growth was made eries, P. 0. Box 3830, Honolulu 12, Hawaii. from adult trout-perch taken on the beachesdur