lThis work received support from Grant no. RR-08125from the Haumana Biomedical Program, MBS Program,DRR/NIH. Manuscript accepted 24 September 1980.

2 Pacific Biomedical Research Center, Kewalo MarineLaboratory, 41 Ahui Street, Honolulu, Hawaii 96813.

THE NATIVE LAND SNAILS of the HawaiianIslands are rapidly becoming extinct, thevictims of a host of human-related distur­bances (van der Schalie 1969). Destructionof the snails' habitat and especially the nativevegetation by logging, grazing, and com­petition with introduced exotic plants, theintroduction of numerous predators, and ex­travagant removal by collectors (some ofthem scientists) have all taken their toll. Thestylommatophoran subfamily Achatinel­linae (family Achatinellidae), endemic to theHawaiian Islands, was represented on theisland of Oahu by 41 species of the genusAchatinella (Cooke and Kondo 1960, Pilsbryand Cooke 1912-1914). Now, fewer thanhalf of these species survive and even thesehave become rare (Hart 1978, Kondo 1970).

Massive monographs have been writtenon shell variation in the achatinellids (Gulick

Pacific Science (1980), vol. 34, no. 4© 1981 by The University Press of Hawaii. All rights reserved

A Field Study of a Vanishing Species, Achatinella mustelina(Gastropoda, Pulmonata), in the Waianae Mountains of Oahu1

MICHAEL G. HADFIELD2 and BARBARA SHANK MOUNTAIN2

ABSTRACT: A population of Achatinella mustelina occupying four treeswithin a 5 x 5-m quadrat on a ridge in the Waianae Mountains of Oahu,Hawaii, was studied by mark-recapture techniques. Between September 1974and December 1975, 222 snails were individually marked and measured.Recapture analyses indicate that the standing population consisted of about220 snails, of which an average of 40 percent were large enough to be sexuallyreproductive. Growth of A. mustelina was found to be slow, averaging about 2mm increase in length per year from a birth size of 4.50 mm to a size atterminal growth of 18.44 mm. Maturity is estimated to occur at an age of 6.9yr. During the course of the study, snails belonging to the introducedpredatory species Euglandina rosea were found progressively nearer the studysite. In August 1979, shells of E. rosea were abundant in and about the studyarea and no living specimens of A. mustelina or any other arboreal snailspecies could be found. We conclude that E. rosea was responsible for thedestruction of the population under study and that species with life historiessimilar to that of A. mustelina stand little chance of surviving the ravages ofsuch introduced predators.

1905, Pilsbry and Cooke 1912-1914, Thwing1907, Welch 1938, 1942), and their repro­ductive systems have been extensivelystudied, primarily for taxonomic reasons(Cooke and Kondo 1960, Pilsbry, Cooke,and Neal 1928). However, there is not asingle study of these animals alive in theirnatural habitat, and only a single recentreport discusses growth of animals main­tained in the laboratory (Severns, in press).Even shell-size ranges in the large museumcollections are missing from the concholo­gical monographs. Thus, these snails, so ad­mired by early adherents of Darwinism fortheir number of endemic species, are vir­tually unknown as biological entities.

The current study was undertaken toprovide data on growth rate, age at re­productive maturity, size/age-frequencydistribution, and such other demographiccharacteristics as might be learned from afield investigation of a population of Acha­tinella mustelina in the Waianae Mountainsof west Oahu. We hoped that field-collectedpopulation data would contribute to anunderstanding of the reasons for the high

345

346

extinction rates of Achatinella and suggestmeans for reversing them. At least the formergoal was achieved.

The data presented were obtained viamark-recapture studies extending over a3-yr period commencing in 1974. Few snailswere removed from their habitat because ofour conviction that even a small samplingprogram could lead to further populationcollapses.

METHODS

Study Site

The Achatinella mustelina populationstudied was located in small trees at anelevation of about 2400 ft near the trail toPuu Kanehoa on the eastern side of theWaianae Mountains, Oahu, Hawaii. Thisridge contained one of only two relativelydense populations of A. mustelina seenduring a fairly intense reconnaisance of theirformer wide range in the Waianae Moun­tains. The study site, a gently sloping, 5 x5-m area, is near those designated asKaluaa-Manuwaielelu ridge by Welch(1938). Snails were found here mainly ontwo Osmanthus sandwicensis and less fre­quently on a Gouldia sp. and an ohia lehua(Metrosideros polymorpha), the only trees inthe quadrat. These trees were 5-7 m tall andsomewhat sparse. Snails were located by vis­ual searches of trunks, limbs, and leaves.Middle heights of the trees were searched byclimbing; special care was taken to look forvery small specimens. The highest parts ofthe trees could not be searched due to fragil­ity of the limbs, and snails in these heightsescaped collection. Ground cover in thestudy area consisted principally of leaf litterwith some small scattered tufts of grass.Passion fruit vines were present on theground and in some of the trees.

Species Studied

It is assumed here that all the snails ob­served can be assigned to the major WaianaeMountain species Achatinella mustelina Mig-

PACIFIC SCIENCE, Volume 34, October 1980

hels, 1845. Many subspecies have been des­cribed from these mountains (Welch 1938),but for present purposes such designation isunimportant. A second species, A. concavo­spira, has been described from lower eleva­tions on west Oahu, and some specimensfrom the current study site had characteris­tics of this species. However, given that theanimals were sympatric, even to the treelimb, and no differences were seen in growthof animals belonging to these two potentialspecies, all data are here considered together.

Marking and Measurement

The snails were assigned individual codenumbers by cleaning a small area of theupper shell with cloth, applying a numberwith india ink, and, after the ink had dried,coating the number with a layer of clear,fast-drying lacquer (Decophane). Many ofthe numbers were clearly legible more than2t yr after their application.

Achatinellids were removed from thetrees, measured (length, width, and spireheight above the aperture), assigned a codenumber, labeled, and, after all snails weremeasured, returned to the trees. Because re­tracted snails will not stick to limbs, animalswere returned by putting them in small, openbags which were hung well up in the trees.Later recapture data indicate that the snailsreadily dispersed from these bags and nonewere ever found remaining in the bags onreturn visits to the study site.

Beginning in September 1974, all speci­mens of Achatinella mustelina found in thestudy area were marked and measured. Onnearly monthly visits to the study site for thefollowing 15 months, all snails recapturedwere identified and remeasured and all pre­viously unmarked snails found were mea­sured and labeled. Subsequent visits weremade to the study site in September 1976,January 1977, and August 1979, and allmarked animals found were remeasured; nonew snails were marked on these visits. Datawere thus obtained on both individual growthrates and population size-frequency distri­butions at all seasons.

When animals were collected and marked,

Field Study of a Vanishing Species-HADFIELD AND MOUNTAIN 347

other notations were made on color pattern,whether the animal better fit the apellationAchatinella concavospira, and whether theshell aperture possessed a thickened callus or"lip." Such a lip appears to indicate the endof growth in an achatinellid and probablyalso signifies the onset of sexual maturity(Pilsbry, Cooke, and Neal 1928).

Migration

The specific tree within the study area onwhich each snail was found was recorded atthe time of collection. Because all snails werereturned after each collection to a specifictree, it was possible to determine the fre­quency of migrations of snails from tree totree. The data were examined to determinewhether migration frequency was a functionof time between recaptures or snail size.

Birth

Attempts to determine fecundity andother reproductive characteristics of Acha­tinella mustelina were limited by our reluc­tance to remove living animals from theirnative habitat. In September 1976, ten snailswere collected near, but from outside, thestudy site and taken to the laboratory. Theywere kept in perforated plastic boxes underconditions similar to those utilized by Mur­ray and Clarke (1966) for the culture ofPartula spp. from Moorea. Freshly collectedbranches and leaves of Osmanthus sandwic­ensis and bark of ohia lehua were added toprovide the epiphytic fungi upon which thesnails feed. The specimens of A. mustelinasurvived well, and seven produced offspringwithin a month of collection.

Data Analyses

Altogether, 222 snails were measured andmarked at the Kanehoa trail study site. Ofthese, 137 were recaptured at least once, themaximum number of recaptures being 11.Analysis of the population's size-frequencydistribution was carried out by first collatingthe number of snails measured in each milli­meter size class at each of 12 visits to the

study site between 15 September 1974 and 20December 1975 (Table 4). Then the percen­tage of the total number of snails repre­sented by each size class was calculated andthese were averaged across all 12 samples.The resultant histogram (Figure 3) thus rep­resents the average percentage distributionof size classes over the major IS-monthstudy period. Minimum and maximum sizeswere also derived from these measurementsand utilized to designate size at birth andmaximum/reproductive size.

The size of the population of Achatinellamustelina was estimated in two ways fromthe mark-recapture data. First, the LincolnIndex (Poole 1974) was determined on thebasis of the first mark-recapture set, where­in the estimated population size, i, is thequantity found by dividing the product ofthe number of animals marked on the firstvisit, a, and the total number found on thesecond visit, n, by the number of markedanimals recovered on the second visit, r:

A anX=­

r

The variance for i is calculated as:

A a2n(n - r)Var(x) = 3

r

The second estimate was arrived at by alinear regression of the percentages ofmarked snails caught at each visit againstthe total number of snails marked prior toeach successive visit (Figure 4). Determiningthe value of 100 percent marked from theregression equation provided an estimate oftotal animals in the population.

Growth rate was analyzed in two ways. Inthe first method, data on the growth of tensnails for which six or more growth intervalswere measured, representing the range ofsizes of growing individuals of Achatinellamustelina, were subjected to regression ana­lysis. The calculated slopes were averaged toarrive at a mean slope, expressed as milli­meter increase per day, which is also a meangrowth rate.

In the second method, all nonoverlapping

348 PACIFIC SCIENCE, Volume 34, October 1980

A8• •

I:• A= •AJOO

~

8

18

16

14

-E 12E A10

..s:-Clc:Q) 10-I

6

J J A SON D J1974

F M A M J J A SON D1975

FIGURE I. Growth curves for ten marked snails. Code numbers given for each snail are those used in themarking studies; regression slopes for these growth curves are presented in Table 1.

growth interval data for all snails were util­ized to calculate growth rates. Thus, if oneanimal was measured twice, with an inter­vening time of 6 months, the growth rateover that 6-month period provided a singleutilizable statistic. Other snails, measured upto eight times, with intervals of differentdurations, provided up to eight such ratemeasures. In calculating mean growth rates,the rate contributed by anyone interval wasweighted by multiplying it by the duration ofthe interval divided by the mean duration ofall intervals so that short rapid bursts orbrief lapses of growth were averaged out infinal calculations. Because interval growthrates varied enormously, even for single indi­viduals, it was considered better to handlethe data in this manner than to calculate

summary growth rates based on averages forindividuals.

Growth was examined as an individualfunction and as a size function. From thecalculated growth rates, ages were attachedto size groups, and the age at reproductivematurity was extrapolated.

RESULTS

Growth

Growth curves for ten snails, chosen torepresent a range of sizes among snails forwhich six or more intervals were measuredand which did not have or develop a shell lipduring the study, are presented in Figure l.

Field Study ofa Vanishing Species-HADFIELD AND MOUNTAIN 349

TABLE I

REGRESSION ANALYSIS OF GROWTH IN TEN Achatinellamustelina

Mean slope: 5.14 mm x 1O- 3/day (SO = 1.8J)Annual growth rate: 1.88 mm

It is noteworthy that animals of all sizes ap­pear to be growing at about the same rate.To determine whether this was indeed thecase, a linear regression slope was calculatedfor each of the snails in Figure 1 (Table 1).As can be seen, there was no apparent corre­lation between slope and size. The meanvalue of the slopes gives a daily growth rateof 5.14 x 10-3 mm, or 1.88 mm/yr (SD =0.66). From the data, it was concluded thatthe rate of growth in Achatinella mustelina isrelatively constant throughout the growingportion of the life of the snail. Because this isunusual-most gastropods showing rapid

early growth and a decreased rate of growthas size increases (Wilbur and Owen 1964)­further analyses of growth rate were carriedout.

The second analysis of the pattern ofgrowth consisted of entering all growth in­terval pairs for all animals in a simple linearregression model of growth rate versus meansize during the growth interval; 209 pairswere entered. The slope obtained did notdiffer significantly from zero.

Finally, all growth interval data were di­vided into three groups based on the meanlength of the snail during the interval meas­ured: below 10 mm; 10-15 mm; and greaterthan 15 mm. This segregation provided 24snails (53 intervals) in the smallest size class,27 snails (73 intervals) in the intermediatesize class, and 32 snails (83 intervals) in thelargest size class. Rates for each intervalwere weighted by the duration of the inter­val, and mean growth rates with standarddeviations were calculated for each class.The results are presented in Table 2. Studentt-tests show no significant differences amongthe mean growth rates of the three sizeclasses. These statistical analyses provide anaverage growth rate of about 2.04 mm/yr forAchatinella mustelina of all sizes, a figureclose to the one predicted for growth rate byregression analysis (l.88 mm/yr). Hence­forth, an average growth rate of 2 mm/yr isassumed.

The smallest specimen of Achatinella mus-

7.93 6.78.33 2.5

10.54 5.412.49 6.113.48 5.215.365 8.615.22 5.014.89 3.717.22 5.317.34 2.9

MIDLENGTH SLOPE(mm) (mm x 1O- 3 /day)SNAIL NUMBER

A879AIO72A78A73AI6A69A64AIOO

TABLE 2

GROWTH RATE VERSUS SIZE IN Achatinella l11ustelina

ANIMAL LENGTH(mm)

NUMBER OFGROWTH

INTERVALSNUMBER OF

SNAILSAVERAGE GROWTH RATE

(mm x 1O- 3/day)STANDARDDEVIATION

< 10.0010.00-15.00> 15.00

537383

232731

5.655.335.77

6.175.605.95

Mean growth rate (all sizes):Annual growth rate:

5.595 mm x 1O- 3/day2.042 mm/yr

NOTE: Mean growth rates were determined by multiplying all individually measured growth rates (all possible intervals used for all animals) by aweighting factor consisting of the duration of the individual interval divided by the mean duration of all intervals measured. The mean growth rates, withtheir standard deviations, are calculated from the weighted interval rales.

350 PACIFIC SCIENCE, Volume 34, October 1980

BIRTH SIZES OF SNAILS IN THE LABORATORY

TABLE 3

NOTE: Data on offspring of len snails (L1-LIO), collected on 4September 1976.

Mean size at birth:

Attainment of maximum size in achatinel­las is marked by the formation of a thick­ened lip on the outer shell aperture (Pilsbry,Cooke, and Neal 1928). Animals with athickened lip found in the present studyvaried in length from 16.69 to 20.40 mm(Figure 2). Snails that formed lips on theirshells during the course of the study grewlittle or not at all after the formation of thelip, even though growth had been measuredin these same individuals up to the time oflip formation. It was noted that a lip wasdeveloping in 27 animals during the study;mean length of these snails was 18.43 mm(SO = 0.755).

4.54 18.835.35 19.964.30 18.274.08 19.843.27 18.924.21 18.573.28 18.44

4.15mm

BIRTH SIZE PARENT(mm) (mm)

9 September9 September

II SeptemberII September18 September23 September

5 October

BIRTH DATESNAILNUMBER

LIL2L3L8L4L7LIO

telina found in the field measured 4.52 mmin length. Animals brought into the labo­ratory produced young measuring between3.27 and 5.35 mm in length (see Table 3).Because laboratory conditions may inducepremature birth (the smallest snails invari­ably died soon after birth), it is assumed thatthe smaller observed birth sizes in the labo­ratory do not reflect the normal situation.We thus take 4.50 mm as a better estimate ofthe average birth size of A. mustelina in thefield (this figure is close to the mean size oflaboratory-born juveniles, 4.15 mm; seeTable 3).

It should be noted that the growth datacited refer to shell length, probably a poormeasure of increase in animal mass. As anestimate of mass change with age, the length­to-width ratio (L/W) of 20 snails for each ofthree length classes « 10 mm, 10-15 mm,> 15 mm) was calculated. The mean L/Wwas determined for each class and thesemeans were compared by using t-tests. Theresults show highly significant differences:L/W for snails under 10 mm in length is1.345; for snails 10-15 mm in length, 1.405;and for snails greater than 15 mm in length,1.574. Since width of the shells does notaccrue as rapidly as length, then neither doesshell volume nor, presumably, mass. A nega­tive exponential curve would probably betterdescribe growth in weight of Achatinellamustelina.

Age

An age at maturity can be determined byapplying the average growth rate determinedabove; that is, the average size of snails witha shell lip, 18.43 mm (n = 52; SO = 0.78),minus the size at birth, 4.50 mm, gives a lifegrowth of 13.93 mm. At a growth rate of 2.0mm/yr, maximum size would be achieved in6.9 yr. This age is also assumed to be that ofanimals at first reproduction.

Figure 3 presents the mean size-frequencydistribution data for specimens of Acha­tinella mustelina in the study area. Agegroups are also indicated. Age determina­tions are extrapolated as described above. Arelatively even age distribution of snails upto a peak of abundance in the maximum sizeclasses, apparent in Table 4, suggests contin­ual reproduction (i.e., there are no apparentannual age groups) and a grouping ofseveral years' progeny in the largest sizecategory. There are suggestions of season­ality in the monthly distribution of occur­rences of smallest animals, but the data aretoo meagre to make this clear (Table 4).

An examination of the recapture datashows that five marked animals with shelllips were present in the study area for atleast 2 yr, and three lipped snails were pres­ent at collections spanning 28 months.Added to an estimated age at lip formationof 6.9 yr, we see a potential life-span exceed­ing 9* yr.

Field Study of a Vanishing Species-HADFIELD AND MOUNTAIN 351

FIGURE 2. Shells of Achatinella mustelina chosen to illustrate the relative changes in shape that occur duringgrowth from birth (the shell on the left) to maturity (the shell on the right). The length/width ratios of the five shellsare, left to right, 1.16, 1.21, 1.25, 1.48, and 1.53. The largest shell bears a thickened lip, indicating terminal growth.Note that the shell in the middle is dextrally coiled, a character without taxonomic significance in this species. (Thescale is graduated in millimeters.)

Population Size

The size of the population of Achatinellamustelina in the study area was not great.The number of snails seen there, located oneach visit when exhaustive collecting wasattempted, varied from 33 to 58 with a meanof 44 (Table 4). Of these, an average of 69percent (range 27.6-90.5 percent) were re­captures and the remainder were animalsmeasured for the first time. The lowestnumber of recaptures was on the second visitto the study site. On the single visits to thestudy site in 1976 and 1977, no new snailswere marked. The number of recaptures, 33and 24, respectively, suggests that the popu­lation was at about the same density as ithad been throughout the more intensive partof the study. However, on the visit to thestudy site in August 1979, no living snails(marked or unmarked) were found in, oranywhere near, the study site, and the popu­lation was judged to be extinct. Seventy-fourempty shells were collected beneath the trees;

15 of these bore evidence of our numbering,and 14 shells showed breakage of the sortattributed to rat predation.

The first estimate of the size of the popu­lation of Achatinella mustelina in the studyarea was based on the Lincoln Index, usingfirst mark-recapture data (Table 4):

x = 58 ~6 58 = 210.25

VarianceoU = 582(58~~38 - 16) = 2000.66

The standard deviation is found by takingthe square root of the variance. The estimatefor the population size is thus 210 ± 45snails.

A second population estimate based onlinear regression of the percentage of markedsnails recaptured versus the total number ofsnails marked is shown in Figure 4. Extra­polating the percent marked to 100 gives anestimate of 234 animals in the population, or

352

c lS.~-.2:::lQ.0

Q....100

~

Ii><

S

PACIFIC SCIENCE, Volume 34, October 1980

FIGURE 3. Size-frequency distribution in the study population of Achatinella mustelina. Sizes are expressed asmillimeter class marks; ages are estimated from growth rate data. Each size class is shown as the average percentageof the total population it represented between September 1974 and December 1975. The monthly data are presentedin Table 4.

215 if the last, somewhat anomalously low,recapture percentage (66.7 percent) isdropped. These estimates agree well withthat obtained by the Lincoln Index. Esti­mates of the population based on the triple­catch method (Begon 1979) and Jolly'sstochastic multiple-recapture method (Poole1974) were far less than the number of snailsseen in the study and were thus discounted.

During the study, the portion of the popu­lation judged to be potentially reproductive(i.e., a lip was present on the shell) variedfrom 24.4 to 48.5 percent (on nine visitswhen lip data were recorded), with the meanpercentage being 37.3 (SO = 8.73). Imma­ture, prereproductive animals thus alwaysformed a majority of the population. Only

26 snails measuring less than 6.50 mm inlength and judged to be newborn or less thanI yr old were seen in the course of the study.The number of snails seen with a shell lip,and thus judged to be sexually mature, was68.

If our data accurately predict a real re­lationship between the number of yearlingsnails and the number of sexually matureanimals, then the population exhibited avery low annual fecundity of 26/68, or about0.4 offspring per adult per year. The fact thatonly 4 of 26 snails less than 6.50 mm inlength were ever seen a second time suggestseither a very high mortality in this age groupor, possibly, that our search efficiency waslow for the smallest snails.

TABLE 4

NUMBER OF Achatinella mustelina COLLECTED MONTHLY BY SIZE CLASS

SIZE CLASS(mm) 15 Sep 1974 2 Oct 1974 6 Nov 1974 24 Dec 1974 2 Mar 1975 6 Apr 1975 15 Jun 1975 27 Jul 1975 30 Aug 1975 5 Oct 1975 5 Nov 1975 20 Dec 1975

4.50-5.49 2 I I 0 0 0 0 1 2 2 2 65.50-6.49 1 I 0 2 1 3 0 0 0 0 0 26.50-7.49 1 0 2 4 1 0 2 I 2 1 0 37.50-8.49 5 3 2 4 3 3 0 3 2 J I 08.50-9.49 0 2 2 3 2 1 2 2 4 4 2 09.50-10.49 3 I 4 I I 0 0 I 2 0 0 0

10.50-11.49 0 0 0 I I 3 5 4 3 1 0 011.50-12.49 0 I 2 2 0 I 2 2 1 4 0 412.50-13.49 2 4 5 2 1 0 I 0 0 I 0 013.50-14.49 3 5 3 2 4 2 1 0 2 I I 214.50-15.49 3 I 2 I 0 2 3 1 2 1 2 315.50-16.49 9 10 4 3 0 2 0 2 2 2 6 316.50-17.49 6 10 2 5 5 7 6 4 6 4 3 317.50-18.49 8 10 6 8 5 6 6 6 14 15 14 1218.50-19.49 13 7 5 3 9 8 5 9 10 10 7 919.50-20.49 2 2 2 0 0 0 I I I 2 1 I

Total 58 58 42 41 33 38 34 37 53 49 42 48Number

recaptured 16 24 25 20 30 28 28 39 41 38 32Percentage

recaptured 27.6 57.1 61.0 60.6 78.9 82.3 75.7 73.6 83.7 90.5 66.7

NOTE: Sampling sessions of 25 January 1975 and 13 May 1975 are not included here, because due to weather conditions, collections were incomplete.

354 PACIFIC SCIENCE, Volume 34, October 1980

. ".B215 ..···· ,,".' "..... """ A234

,,",,"

A: y = 16.78 +0.355 x (r =0.861)

B: y= 8.74+0.425x (r =0.952)

/"fit'

.,.-:.~.',"" ...,,"" .', .''" ..­, .', .'

-', ., ........

100

20

80

" 60~:::I-a.ouQ)

0::

~

o 30 60 90 120 150

No. Snails Marked180 210 240

FIGURE 4. Percentage of marked snails recovered versus total numbe~ of snails marked (solid line) andregression analyses of the data (broken lines), including (A) and not IncludIng (8) the last recapture count. Thenumbers of snails estimated to be present at 100 percent markIng are 234 and 215.

Migration

Twenty snails for which four or moregrowth intervals were measured were ran­domly selected for analysis of their migra­tion frequency. In the 100 recaptures of these20 snails, 51 were in different trees thanthose in which they had been placed aftertheir prior capture and measurement. Whenthese snails were examined for frequency oftree-to-tree migration as a function of inter­val duration between recaptures or size ofthe snail, no correlations were found. Pilsbryand Cooke (1912-1914: xxxv) had suggestedthat "young shells wandered more widelythan the adults." The trees in the study areawere close together and the snails could havemoved across intermingled branches ratherthan across the ground.

DISCUSSION

The data presented here strongly supportthe conclusion that the rate of growth in

shell length is constant throughout the grow­ing part of the life-span of an individual ~f

Achatinella mustelina. The reasons for thISare probably twofold. First, achatinellids a~e

very large at birth, being over 4 mm III

length, and their entire life's growth the~e­

after thus results in less than a fivefold Ill­

crease in length. A logarithmic phase ofgrowth, characteristic of most very. y~)Ung

animals, probably is passed in utero III Juve­niles of Achatinella mustelina, if it occurs atall. A second factor contributing to constantrate of length increase up to terminal size isthat reproductive maturity occurs after ~ax­imum size is achieved. Because there IS nomajor energetic cost due to reproductionuntil after the shell aperture callus is formed,the end of each snail's growth phase occursvery abruptly, without a lengthy period ofasymptotic growth. However, as noted abo~e,

the proportions of the shell do change ~Ith

growth in these snails, and the rate of weIghtincrease may well vary with age, decreasingas animals get older.

Field Study of a Vanishing Species-HADFIELD AND MOUNTAIN 355

The rate of growth observed in Aehatinellamustelina is very slow as compared withgastropods in general and pulmonates inparticular. The giant African snail Aehatinafuliea grows at rates in excess of 24mm/month during its phase of maximumrate and has an average lifetime growth rateof about 10 mm/month (Kondo 1964).Cepaea nemoralis grows considerably moreslowly, at perhaps 2 mm/month (Cain andCurrey 1967). However, growth is inter­rupted by aestivation in these snails and thegrowth is measured in diameter rather thanlength. Data on age at maturity for twospecies of Partula, land snails from theSociety Islands, reared in captivity suggestgrowth rates of 10-20 mm/yr (Murray andClarke 1966). Some young, tropical marinegastropods studied by Frank (1969) grew atrates of about 5-10 mm/yr, while others,Cerithium nodulosum and Strombus gigas,studied by Yamaguchi (1977) and Berg(1976), respectively, grew at rates of 2.7-6.6and 5-10 cm/yr.

Severns (in press) measured growth in 32specimens of Aehatinella lila in captivity for81 days. Measuring growth along the sutureline (i.e., added to the growing shell margin),Severns showed a declining rate of lipgrowth as shell length increased. Our dataon increasing length/width ratios with in­creased length are in agreement with hisdata. Severns calculated that animals of 17­mm shell length are 5.27 yr old. This figure isless than our prediction by nearly 2 yr, andmay indicate a species difference. However,it does reinforce the fact that achatinellidsare slow growing and late maturing.

Reasons for the slow growth rate seen inAehatinella mustelina can only be specula­tive. It may be related either to limited quan­tities or low nutritional value of the resourceon which these snails feed, epiphytic fungi(Pilsbry and Cooke 1912-1914), and to theirrestricted nocturnal feeding habits. It ispossible that calcium for shell growth is onlyslowly acquired in the snail's diet. It hasbeen suggested (Welch 1938) that feedingmay not occur during exceedingly dry peri­ods, and such periods are not infrequent inthe Waianae Mountains. However, when weexamined our data for evidence of season-

al variation in growth rate, we found none.The result of a life history pattern such as

that seen in Aehatinella mustelina is wellknown. Low motility-at least relative tocrossing geographical barriers such as val­leys and plains-led to great numbers ofspecies arising and the establishment of nar­rowly localized varieties. More than 200species were originally described on the basisof relatively consistent morphs. A more re­alistic count of about 41 species was theresult of later revision (Pilsbry and Cooke1912-1914).

Another result of the life history patternobserved is the vulnerability of populationsof achatinellids to predation and habitatdestruction. Because of low geographic mo­tility, small isolated populations are readilyeliminated. However, a more long-rangeeffect of predation results from the removalof animals during the extended prereproduc­tive phase of their lives. More than 60 per­cent of the population of Aehatinella mus­te/ina studied was composed of prereproduc­tive individuals. If predation is random,more than half of the animals removed in agiven time period will never have repro­duced. Under these conditions, if predationis constant and sufficiently intense, the preypopulation will eventually die off.

The data presented on the low occurrencesof 4.50-6.50-mm juveniles in the study areastrongly suggest a low rate of fecundityfor the adult individuals of Aehatinellamuste/ina-less than one offspring per adultper year. While no observational data areavailable on the rate of release of offspringby individuals of any species of Achatinella,published notes that uteri of adult snailsnever contain more than two large embryos(Cooke and Kondo 1960, Pilsbry and Cooke1912-1914, Pilsbry, Cooke, and Neal 1928),and more frequently only one, allow someextrapolation of reproductive rate. If therate of growth of ova from a fertilized size of0.75-mm diameter (Solem 1972) to a hatch­ing size of 4.50 mm is similar to that ofjuvenile snails (about 2 mm/yr), then fecun­dity would be maximally two offspring peradult per year. Doubling or tripling thegrowth rate still gives very low fecunditypredictions. Presumably, in the native state

356

the low annual rate of fecundity was offsetby a lengthy reproductive life.

Carlquist (1970: 185) notes that "the ach­atinellas probably had no active predatorsin prehuman times, although the thrushPhaeornis may have eaten a few." The snailswere able, apparently, to form dense popu­lations, although it is nearly impossible toarrive at any estimates of density from studyof older works based on many thousands ofcollected specimens. In an undated manu­script, Emerson refers to Achatinella "dup­locincta" in the "Apex family": "From thisone tree about three score of this rare shellwere picked." The tree was an ahakea(Bobea elatior), a bushy form not exceeding20 ft in height. By comparison, it seemscertain that the population we studied wasgreatly diminished at the start of our in­vestigation. Consisting of about 220 snails infour trees in a 5 x 5-m quadrat, it was as­suredly less dense than those from whichdozens of snails were once taken at frequentintervals (Welch 1938).

While our data indicate fairly frequentmigration of snails from tree to tree, allpublished reports on achatinellas suggest thatmigration occurs too slowly to significant­ly replenish rapidly depleting populations.

One change that may have occurred be­tween the time of collection of Welch's(1938) specimens and the present was a de­cline in the mean size of mature snails. Snailsfrom the same ridge system seen by Welchaveraged 20 mm or greater in length. Themature snails we saw averaged under 18.5mm in length. There is no obvious reason forthis decline.

The life history pattern of Achatinellamustelina can be summarized as that of aspecies exhibiting slow growth and late ma­turation, low annual fecundity, large size atbirth, and a long reproductive life. Assumingthat this pattern evolved in an essentiallypredator-free situation, the character thatappears most obviously as the key to thepattern is the extremely large birth size. At4.5 mm in length, offspring of A. mustelinaare nearly one-quarter the size of adults.Such large birth size places severe limits onthe size of the maternal organism. Snails

PACIFIC SCIENCE, Volume 34, October 1980

reproducing at sizes much less than thoseseen could only do so by producing smalleroffspring.

If growth rate is restricted by nutritionallimitations and minimum adult size is lim­ited by juvenile size, then age at maturationmust come late. The compensation for lowfecundity, itself a consequence of large sizeof offspring, is an extended reproductive life.

If this interpretation is valid, it becomes ofinterest to explain the selective advantage oflarge offspring. A frequently cited factorleading to large birth size is predation fo­cused on small individuals (e.g., Spight 1976).We have no evidence for the existence of anabundance of microcarnivores specializingon snails. A more useful hypothesis favorsinterspecific competition as a selective forcefor large birth size in the achatinellas.Literally dozens of species of snails belong­ing to four families occupy the trees ofHawaii (Zimmerman 1948). Adults of manyof these species, in the Tornatellininae forinstance (Carlquist 1970), are smaller thanthe birth size of young of Achatinella mus­te/ina. Might not competition with well­developed, small, adult tornatellinins or suc­cineas for resources such as food and spacehave exerted strong selective pressure againstsmall young in the achatinellas?

The proposition that birth size sets thelimit on other life history characters inAchatinella mustelina is debatable. We dis­sected five dried specimens of an uniden­tifiable species of Achatinella and found eachto have a single large intrauterine embryo.The largest of these embryos measured 4.35mm and 4.43 mm in length and were thus inthe same size range as young of A. muste/inaat birth. The snails bearing these embryoshad shells 25 and 26 mm in length, contrast­ing sharply with the mean size of mature A.mustelina seen in the present study. Ourhypothesis, that extreme selection for largebirth size sets a minimum on adult repro­ductive size, does not explain why snails dem­onstrably capable of reproducing at 18 mmshould grow to 25 mm before reproducing,unless, of course, the large animals belong toa species whose offspring are significantlylarger at birth than those of A. mustelina.

Field Study of a Vanishing Species-HADFIELD AND MOUNTAIN 357

Perhaps reproductive maturity is age-specific;beyond some minimum size, animals all be­come reproductively functional at a set age.Size at the onset of reproduction is then afunction of growth rate, and that depends onfood availability and quality.

A long prereproductive life and low fecun­dity in species suddenly exposed to massiveand diverse predation by a multiplicity ofpredators (humans, rats, birds, snails) pre­sents a picture of imminent extinction. Thisis, in fact, the case. When the present in­vestigation was begun in 1974, the studypopulation of Achatinella mustelina appearedto be thriving, if not dense. During thecourse of the study, the population persisted,though numbers may have been declining.One of the native trees in which the snailswere found, an Osmanthus sandwicensis,died. A few dead snails showing evidence ofrat predation were found in the study area ateach visit. However, it was the appearanceof the introduced predatory snail Euglandinarosea that most clearly coincided with thedisappearance of all snails from the studysite and the ridge above and below it.Specimens of E. rosea were first seen onthese slopes, below the study area at eleva­tions of about 1000 ft, in December 1974.By 1977 the predatory snails were foundnear the study site. In August 1979 a recon­naissance of the area showed dead shells ofE. rosea to be abundant, and living ach­atinellids, as well as members of all othersnail taxa previously seen in the area, wereabsent. The study area was thoroughlysearched for dead shells of A. mustelina, and74 were found, of which only 14 showedbreakage similar to that inflicted by rats.It must be concluded that predation byE. rosea was the "final" cause of extinctionof the population of A. mustelina on theKanehoa trail.

ACKNOWLEDGMENTS

The authors gratefully acknowledge theassistance of Clifford Chun and CarolynHadfield in carrying out the field studies.The manuscript profited greatly from the

critical reading and suggestions of D. P.Abbott, E. A. Kay, J. Stimson, and F. E.Perron. Special thanks are due to HerbertKikukawa of the Hawaii State Division ofForestry for permission to pursue thesestudies on state forest lands.

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