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AMER. ZOOL., 33:610-622 (1993) The Decimation of Endemic Hawaiian Tree Snails by Alien Predators' MICHAEL G. HADFIELD, STEPHEN E. MILLER, AND ANNE H. CARWILE Kewalo Marine Laboratory, University of Hawaii, 41 Ahui St., Honolulu, Hawaii 96813 SYNOPSIS. Endemic terrestrial tree snails of the Hawai'ian Islands, like those of other oceanic islands and even some continental areas, are extremely sensitive to disturbance because of their low population numbers and small geographic ranges. Like many other plants and animals of oceanic islands, they have evolved no defenses against introduced predators and competitors. The range of Achatinella mustelina, a tree-snail species found only in a short mountain range on the island of O'ahu, typifies this problem. Mark-recapture studies at two field locations reveal that the snails exhibit slow growth and late maturity (3-5 years). Fecundity is estimated at about 7 offspring per adult per year. The young are born live at about 4.6 mm. Population growth typically depends on considerable longevity (> 10 years). Demographic effects of the depredations by alien predators, rats and a North American predatory snail, Euglandina rosea, were documented in two long-term study sites. The predatory snail eats all sizes of A. mustelina and can rapidly drive populations to extinction (less than one year). Rats tend to select larger snails as prey and may leave an area before destroying all of the prey snails present; while reproductive output is temporarily destroyed, populations may survive. Actions necessary to conserve Hawai'ian tree snails, or indeed any group of relatively sedentary invertebrates with small species ranges, must include predator abatement, but also preservation and restoration of sufficiently large and complex forest habitats that the invertebrates may find refuge from alien predators. reduction in range through conversion of habitat to agricultural uses. Especially birds and mammals have vanished in large numbers from Hawaii, New Zealand, Madagascar and Mauritius (Diamond, 19846; Atkinson, 1989). Tortoises have fared equally badly on the Galapagos Islands and islands of the Indian Ocean, and have become largely extinct on Madagascar, Although alarmingly less studied than the vertebrates, invertebrates are victims of the same annihilating forces on oceanic islands, Th ere are scattered references to various endangered groups in Hawai'i and elsewhere {e.g., Crowell, 1968; Gagne, 1981; Meads et al, 1984), but recognition of the threatened status of island invertebrates, much less their intensive study, has lagged • distantly behind that of vertebrates, 1 From the Symposium The Crisis in Invertebrate especially birds. This is not Surprising since A S S ' ^ ^ ^ C . ^ S X 2 £ & £ invertebrates are typically much smaller and INTRODUCTION The endemic terrestrial biotas of oceanic islands are arguably the most disturbance sensitive and extinction-prone biotas on earth. Two major characteristics of such island species, small geographic range and small populations, are believed to underlie their high extinction rates (Diamond, 1984a, 1989; Olson, 1989). Additionally, manyprobably most—oceanic-island species evolved in relative isolation from grazers and predators, often with little competition as well. For these reasons, island species are especially vulnerable to alien predators (including man) and aggressive competitors brought from the continents, as well as to ety of Zoologists, 27-30 December 1992, at Vancouver. British Columbia. less spectacular than birds. However, given the importance o f arthropods to the diets 610 EXTINCTION IN HAWAI'IAN TREE SNAILS 611 of many island birds, it is puzzling that avian biologists have devoted so little attention to these animals. Hawai'ian tree snails (Pulmonata; Achatinellidae; Achatinellinae) have been well known since the mid-1800s for their beautiful, highly variable shells and their spectacular evolutionary radiation (Gulick, 1905). Their high rate of extinction, recognized by their inclusion on the U.S. List of Federally Endangered Species in 1981, has been attributed to a typical set of threats: degradation and outright loss of habitat, introduced predators (principally rats and snails), and human shell collectors (Hadfield, 1986). The genus Achatinella as last revised (Pilsbry and Cooke, 1912-1914) included 41 species, each endemic to a small region of one of the two mountain ranges on the island of O'ahu. While species had begun to disappear before 1900, the rate of extinction accelerated greatly after the introduction of a predatory snail, Euglandina rosea. The Hawaii State Department of Agriculture introduced E. rosea in 1958 in an ill-conceived program of biological control of a garden pest, the giant African snail Achatina fulica. Fewer than 20 species of Achatinella are now believed to persist, and all are declining in numbers due to introduced predators (Hadfield, 1986). In addition, at the higher elevations where remaining Achatinella species are found, alien ungulates, principally goats and pigs, continue to degrade the habitat by destroying native vegetation and spreading noxious alien plants. bers of the genus) after an apparently lengthy gestation, slow growing, late maturing (ca. 6 yr), and low in fecundity. This paper presents the results of 10 years of field demographic studies, aimed at furthering our understanding of life-history patterns and long-term dynamics of residual populations of achatinelline snails. They were carried out at the northern and southern extremes of the current range of the species. The physical settings of the two study sites are sufficiently different to allow additional insight into the role played by tree type, forest cover and isolation on population dynamics. Because tree-snail populations at both sites were under pressure from both predatory snails and rats, we hoped to gain additional understanding of the effects of these predators and ways to control them. Ultimately, it is the goal of our investigations to provide the information necessary to plan a major conservation effort for the Hawai'ian tree snails. Such information should be useful in conservation strategies for other sedentary invertebrates under stress and facing extinction. In an effort to determine the best plan for conservation of the native Hawai'ian tree snails, we have carried out field studies on Achatinella mustelina, the most abundant of the remaining species in this genus. Achatinella mustelina is restricted to the Wai'anae Range on O'ahu, where it was once found almost continuously distributed at elevations at least as low as 350 m; today its range lies only above 550 m and is repeatedly broken. An earlier study documented the destruction of a population of this species by Euglandina rosea in the middle of the Wai'anae Range (Hadfield and Mountain, 1980). From those studies we learned that A. mustelina is live bearing (like all mem- Study sites Field studies were conducted on populations of Achatinella mustelina at two sites approximately 20 km apart. The Pahole population was located in a 5 by 5 m quadrate in dry forest at about 575 m elevation in the Pahole Natural Area Reserve, north Wai'anae Mountains, O'ahu. In the quadrate, most of the snails were found on the most abundant tree, Pisonia umbellifera. The second site was located near Pu'u Palikea in the southern Wai'anae Mountains, between 900 and 930 m elevation, in The Nature Conservancy's Hono'uli'uli Preserve. At this site, snails were studied in single small trees, two each at two separate MATERIALS AND METHODS The species studied here, Achatinella mustelina (Fig. 1), was and remains the dominant species of its genus in the Wai'anae Mountain Range on O'ahu. The distribution is broken into northern and southern segments. Variation and taxonomy of the species were monographed by Welch (1938). 612 M. G. HADFIELD ET AL. waterproof lacquer applied sparingly with a fine brush. The length and width of each snail was measured with calipers to 0.01 mm. Adult snails were noted by the thickened lip or callus on the aperture of the shell. After all of the snails from a tree or a subquadrate were marked and measured, they were returned into the subquadrate/ tree from which they were collected. Any snails that were crawling were placed directly onto leaves or branches of the trees (this typically included all smaller snails); snails that remained retracted into their shells were placed in fiberglass-screen baskets with wetted leaves from the host tree, and the baskets were hung within the shaded part of the tree. Repeated checks have shown that snails crawl from the baskets onto the trees during the ensuing evening hours. At all sites, the shells of dead snails were collected from the ground within the quadFIG. 1. Achatinella mustelina, adult and first-year rate or beneath the study trees (ground shells) juvenile from the Pahole site. Adult is approximately at the start of each visit. These shells were 21.5 mm long; juvenile is about 5.1 mm long. sorted into size classes, and damage due to rat predation (indicated by raggedly broken locations. Because there was no movement shells) was recorded. of snails between the trees, they are treated as four populations. Three of the trees were small Metrosideros polymorpha, and the Data analyses fourth was actually a pair of small trees An analysis of growth rate provided the intermingled, a Coprosma (longifolia?) and basis for estimating the age of a snail from a Dubautia sp. its shell length. Growth rate was analyzed following methods described by Kaufmann Data collection (1981). Briefly, the bestfittinggrowth model The Pahole site was visited once a month was selected from among five growth curves from November 1983 through November (exponential, power, Gompertz, logistic and 1987 and then quarterly through 1992. The von Bertalanffy) by regressing specific growth 25 m2 quadrate was subdivided into four rate (or its log) against size (or its log or subquadrates (A, B, C and D) and each sec- reciprocal). ¥ or Achatinella mustelina at the tion was searched by 3-4 persons for 50-60 Pahole study site, the best fit to the collected min. The Palikea sites were visited monthly data was obtained with the logistic growth from June 1988 through April 1989 and curve. Next, the logistic variation of the then quarterly through 1992. On each visit, Ford-Walford linear regression (Kaufmann, each of the four trees was searched for 50- 1981) was used to estimate a slope and 60 min by two persons. All live snails found intercept, the latter being an estimate of were removed from the trees and held in maximum size (Smax). These values, along screened boxes placed in damp shade. Snails with the mean time between visits (here we from each subsection of the quadrate at employed only data obtained at 2-month Pahole or from different trees at Palikea were recapture intervals), were used to estimate treated separately. Each new, unmarked b, the intrinsic growth rate. Smax and Sbirth snail was alphanumerically coded {e.g., (birth size) were determined from measureA108); a number was written on the shell ments on field populations. Smax, Sbirth, and with india ink and coated with a fast-drying, b were used in the logistic equation to esti- i EXTINCTION IN HAWAI'IAN TREE SNAILS 613 number of never-before-seen, year-class 0 snails of each visit by the proportional value determined for that visit. Similar estimates 1 were made for the "real number" of adult 1 + [(Smax - Sbirth)/Sbirth]e-bt snails present on each visit. Finally, the estiFor Smax = 21.96, Sbirth = 4.64, b = 0.003068, mated "real numbers" of newborn snails and t in days. This formula was used to per visit were summed over a 12-month establish the size ranges of each year class. period, and this sum was divided by the Mark-recapture analyses were used to similarly obtained "real number" of adult estimate the total number of snails in each snails present in the population over the population, and within each year class. Ani- same period. The result was an estimate of mal sizes, catalogued in the mark-recapture annual fecundity, that is, the number of studies, were converted to ages, and divided newborn snails per adult per year. Addiinto year classes that were then analyzed by tional estimates were calculated for all posthe Manly-Parr method and "spot checked" sible 12-month intervals between January by the application of Petersen indices (see 1984 and July 1986 and averaged to deterBegon [1979] for good directions to these mine a mean annual fecundity. An estimethods). The Manly-Parr method was mated mean annual fecundity was similarly selected because it makes the fewest calculated for snails at Palikea using data assumptions about the data, especially the collected between June 1988 and Novemdistribution of mortality across year classes. ber 1989. Survivorship between visits to the study Because growth is determinate in A. mussites, also estimated from the Manly-Parr telina, direct determination of age of lipped analyses, were converted to annual survi- shells is impossible; we can estimate only vorships for each year class. the age at which snails become mature. Size at birth was estimated as the average Using this estimate as a basis for age at first length of all snails less than 5.00 mm long sighting, the age of any snail seen repeatedly at first measure. Age at first reproduction during the study will be estimated as agewas estimated by determining the average at-maturity plus subsequent years over lengths of snails when they developed a lip which the snail has been recaptured. For on their shells and stopped growing (that is, example, if a snail was mature when first the mean length of all lipped shells), and marked, its age will he estimated at 4-5 yr; converting this value to age using the logis- recapture of the same snail three years later will provide a final estimate of 8 yr. Needtic formula given above. less to say, this is a conservative estimate Annual fecundity, the number of offspring live-born to each adult per year, was because many mature snails will be older determined by dividing an estimated num- than 4-5 yr when first captured. ber of new, year-class 0 snails by an estimated number of adult snails (i.e., those RESULTS with lipped shells) for each visit to the Pahole Demography site, and averaging across each year of visits. Small snails were not as easily seen as adults, From 1984 through 1986 the Pahole snail so the numbers of young and adults in the population was relatively large and growing. population were estimated separately, as For these reasons, mark-recapture data for follows. For year-class 0 snails, the total this period were analyzed to determine sizenumber actually seen on each visit was specific growth rates and, subsequently, to divided by the Manly-Parr estimate for year- integrate these numbers into a growth curve class 0 snails present on that visit. This pro- that allowed determination of the ages of vided a proportional value for the number snails from their shell lengths (Table 1). seen (e.g., we saw 0.47 of the number of Average size at birth, the mean length of snails estimated to be present). Next, a "real newly marked snails under 5 mm long, was number" of new, year-class 0 snails for a 4.61 ± 0.31 mm at Pahole (n = 139) and given visit was estimated by dividing the 4.45 ± 0.33 at Palikea (n = 24). At Pahole, mate size at any particular age (St): 614 M. G. HADFIELD ET AL. TABLE 1. Size-year class relationships in Achatinella mustelina at Pahole. Age (years) Year class Size range (mm) 0-1 1-2 2-3 3-4 4-5 0 1 2 3 4+ 3.6-10.0 10.1-16.0 16.1-19.6 19.7-21.2 >21.2 1 2 0 -i Manly-Parr estimates (1984-1986) X OS adults 60 - OH CO S 30 mean length of all snails with lips (i.e., those that had ceased growing and become reproductively mature) was 21.4 ± 0.96 mm (n = 1,804, including repeat measures of the same snails on different visits). The average age of snails at this mean length is 4 yr, and this is taken as the average age at first reproduction. The range of ages at first reproduction is 3 to 5 yr. A summary of lifehistory characteristics of Achatinella mustelina, as determined at the Pahole study site, is presented in Table 2. At Palikea, adult snails averaged 20.7 ± 1.03 mm in length (n = 319, including repeat measures from single snails in all trees). Growth may be slower or reproduction earlier in these populations; the data set is insufficient for a rigorous test of either hypothesis. Fecundity, determined from the annual production of new snails in the Pahole quadrate divided by the mean number of mature snails during the same period, was found to be seven offspring per adult per year. Estimated fecundity at Palikea was 23 offspring per year, but the robustness of this estimate is considerably less due to the low numbers of snails present and the nearly continuous early presence of predators that could have removed smaller snails before they were measured. Age-specific survivorships, estimated by the Manly-Parr analyses of mark-recapture data collected at Pahole between January TABLE 2. Life-history characters of Achatinella mustelina at Pahole. Birth size (length, mm) Mean maximum size (mm) Range Age at first reproduction (yrs) Annual fecundity Longevity (yrs) 4.6 21.4 18.6-23.1 4 7.4 10 + CO 1 2 3 YEAR CLASS FIG. 2. Year-class distribution of Achatinella mustelina in the Pahole study quadrate from early 1984 through 1986. Adult snails, those whose shells have a thickened apertural lip, are indicated by hatching. 1984 and December 1986 are presented in Table 3. By this analysis, survivorship is about 21% for the first year, 31% for the second year, and subsequently about 52% per year, and only 1-2% of snails survive long enough to reproduce. However, the distribution of age classes in the Pahole population between 1984 and 1986 (Fig. 2) indicates higher survivorship during the first two years, about 35% for the first year, 42% for the second, and subsequently at least 50%, probably through life. Thus as many as 8-9% of newly born snails may survive to reproduce. With an annual fecundity of seven, survivorship rates this high should support a growing population, as was indeed seen between 1984 and 1986 at Pahole (see below). Maximum age of A. mustelina at Pahole is at least 10 years. Many snails had lipped shells when the population was first marked in November 1983, and many of them were recaptured at least through 1988. Assuming TABLE 3. Annual survivorship of Achatinella mustelina at the Pahole site, estimated from mark-recapture data, January 1984-December 1986. Year class Survivorship 0 1 2 3 4+ 0.21 0.31 0.52 0.46 0.57 615 EXTINCTION IN HAWAI'IAN TREE SNAILS 320 -n ^ 240 - o 160 - • • estimated population size ground shells per month w PQ 80 - 0 1984 1986 1988 1990 1992 DATE OF VISIT FIG. 3. Top: estimate of population size of Achatinella mustelina in the Pahole study quadrate from 1984 through 1992. Population size was estimated from Manly-Parr evaluation of mark-recapture data. Bottom: monthly number of dead shells found on the ground in the Pahole quadrate from 1984 through 1992. that some of these snails developed shell lips at five years, we arrive at the conservative estimate. Because all large snails at Pahole were killed by alien predators during the 1987-1989 interval, we have no way of determining ultimate life span in the absence of predation. Ultimate lifespan in A. mustelina, as in other members of the subfamily, is clearly much greater than our conservative estimate. Population dynamics: Pahole Site From the beginning of 1984 until early 1987, the population of Achatinella mustelina within the 25 m2 quadrate at Pahole grew from about 120 to 300 snails (Fig. 3). Then, in April 1987, the population began a precipitous decline in numbers that continued until about October. An approximately two-month increase in snail numbers was followed by another rapid decline until mid-1988, when the population appeared to rebound again slightly, only to be followed by a more gradual decline in numbers until mid-1989. For the next year, the population was relatively stable at about 80 snails. In early 1991 the number of snails in the study quadrate increased, and currently fluctuates around a mean of about 150 snails, not greatly different from the density present when our study began in 1983. The density of dead shells within the quadrate accurately reflected the loss of live snails from the trees overhead (Fig. 3). Two to 20 (mean = 9.8) ground shells were found on each visit from the beginning of the study through 1986. In 1987, the number of dead snails increased greatly (mean 24.3; range: 13-65 per mo) as the number of live snails declined. All of the loss of live snails from the population was accounted for in the dead shell count. After the population of living snails hit its minimum density in late 1988, the number of ground shells remained low and relatively constant. 616 M. G. HADFIELD ET AL. 2 5 -. A 20 X o IB no predation (1-12/86) E. rosea predation (9-10/87) 15 10 - 5X, 0 - 1 S 25 -| ™ 20 - • _ D rat predation (1-4/88) recovering population (3-9/92) Q g 15 H § O 10- rat—killed snails 50 co in in CO m m m m d CM CO CO in CM in CO* CM in in in in d CM co CM CM SIZE CLASS (mm) FIG. 4. Size-frequency distribution of dead shells from the Pahole quadrate: A, during the maximum observed population density in 1986; B, during a period of rapid population decline due to intense predation by Euglandina rosea (open bars repeat graph A for comparison); C, during a later period of population decline caused mainly by rat predation; and, D, during a population-recovery period after rats had been removed from the study area. Examination of the ground shells provides important clues to causes of mortality, both in the size-frequency distribution of the dead-shell assemblage and in the condition of the shells. The alien predatory snail Euglandina rosea devours all snails it finds, and thus, during episodes of intense Euglandina predation, size frequencies of dead shells tend to reflect those of the live snails present, with an emphasis on smaller size classes. A slight bias away from the largest snails probably reflects a tendency for very large Achatinella mustelina to live in the tops of the trees, which are areas where E. rosea is less likely to venture during its nocturnal feeding forays above the ground. Shells of snails killed by E. rosea are generally very clean and undamaged due to the habit of this predator of extracting its prey through the shell aperture with its highly extendable proboscis. While E. rosea is mainly a nocturnal predator, on one occasion we observed an individual E. rosea feeding on a small A. mustelina about 1 m above the ground in a tree within the Pahole quadrate. Contrasting with the habits of Euglandina rosea, rats appear to choose larger snails as their prey. Thus the size-frequency distribution of dead shells during episodes of rat predation is biased toward those larger than 15 mm. Additionally, rats crush the shells when they feed upon them creating recognizable breakage patterns, although some small snails may be eaten whole. Rats are also nocturnal predators and have never been seen during daylight visits to the site. While shells of most rat-killed snails were 617 EXTINCTION IN HAWAI'IAN TREE SNAILS 125 -jA 100 75 X B E. rosea predation no predation (1-12/86) (9-10/87) estimated 222 seen 50 - EH S3 o 25 0 D rat predation (1-4/88) recovering population (3-9/92) - y////, 4+ 0 4-1- YEAR CLASS FIG. 5. Age-frequency distribution of living snails in the Pahole quadrate: A, prior to major predation; B, during intense predation by Euglandina rosea; C, during intense predation by rats; and, D, during the interval since rats were killed at the study site. Open bars represent class sizes estimated by Manly-Parr analyses of mark-recapture data. found on the ground, on one occasion rateaten shells were found on a tree branch about 3.5 m above the ground, indicating that these predators move high along the thick branches of the Pisonia umbellifera upon which the native snails live at this site. The size-frequency distributions for dead shells collected in the Pahole quadrate at different times during the study display the trend toward variation in pattern when different predators are present (Fig. 4). During the major decline in the Pahole population of A. mustelina in 1987, all sizes of snails were preyed upon, although juvenile shells were more frequent in the ground assemblage than larger ones, and the frequency of small shells in the death assemblage was greater than in the living population. We judge the huge mortality of A. mustelina in the Pahole quadrate in early 1987 to have been caused by E. rosea because of the size- frequency distribution of dead snails and the presence of shells of E. rosea in the quadrate. During the major population decline of 1988, large shells were more abundant on the ground, and nearly all of the medium and larger shells showed the breakage characteristic of rat predation. The abrupt stop in the decline of the population in 1989 occurred after a program of rat poisoning was instituted at the study site. Bait boxes were monitored bi-monthly from April 1989 through January 1990, when the rat bait stopped disappearing from the boxes between visits to the site. At this time, it was concluded that the major rat invasion to the site had been curtailed. Different predators have different effects on the demography of Achatinella mustelina, as illustrated when the age-frequency structures of the population are examined 618 24 M. G. HADFIELD ET AL. -i Si 22 -| PL, H 20 -| 18 20 -i Year—class 0 (per month) T M M J S N T M M J S'N'J'M M J S N 1985 1986 1984 DATE OF VISIT 1 FIG. 6. Juvenile mortality and climate at the Pahole site. Occurrence of dead (ground) shells of less-than one-year-old Achatinella mustelina is plotted at the bottom. Temperature (top) and rainfall (middle) are plotted for the same years when juvenile mortality was monitored. predation by rats and Euglandina rosea caused great increases in mortality, most snail deaths fell in the smallest size class (snails under 7 mm in length). Analyses of the temporal distribution of deaths among snails less than one year old (Fig. 6) showed that mortality from June through October, the hottest months in Hawai'i, was nearly double that during the rest of the year; an average of 8.4 small snails died per month during the summer months, compared to 4.6 per month during the cooler part of the year. Correlations between juvenile mortality and either rainfall or temperature (Fig. 6) were weak; Kendall's coefficient of rank correlation, T, was 0.19 between year-class 0 mortality and rainfall, and 0.33 between year-class 0 mortality and temperature. While the correlations are not strong, the combined effects of high temperatures (>21°C) and low rainfall (<5 cm month"1) are sufficient to account for the 1.5-2 fold increase in juvenile mortality observed during the warmer months (May or June through October or November). Warm drought periods at any time of year could lead to increased death among small snails at the Pahole site. Obviously, this natural mortality may render populations seasonally more sensitive to attack by alien predators. Population dynamics: Palikea sites Numbers of Achatinella mustelina in the during different time intervals of this study study trees at Palikea between 1988 and (Fig. 5). While the total population declined 1992 are graphed in Figure 7. Because of during the period of intense predation the small sizes of these trees, recapture was attributed to Euglandina rosea, a small always close to 100%. Trees A and B, origreproductive capacity remained. Under inally intertwined individuals of Dubautia intense rat predation, adult snails were sp. and Coprosma sp., changed dramatically selected so severely that nearly all repro- during the course of our study, in part, we ductive and near-reproductive snails were think, due to our activities. In an effort to eaten, leaving the population without repro- curb the continuous predation by Euglanductive potential for several years. Recov- dina rosea that we were recording at this ery of the population began only after the site, in 1989 we cleared a dense ground predators had been removed and remaining cover, the fern Dicranopterus sp., from the juvenile snails grew to adulthood in two area around the study trees. This appeared years or more, aided by a small immigration to cause the soil to dry out, possibly to the detriment of the sprawling specimen of of mature snails into the quadrate. At all times during this nearly 10-year Dubautia sp. which regressed and eventustudy there has been mortality in the study ally died. Many snails had died well before population of Achatinella mustelina (Fig. 2). the tree (probably victims of E. rosea which Other than the times noted above, when we repeatedly observed here), and remain- 619 EXTINCTION IN HAWAI'IAN TREE SNAILS 20 - _ trees A & B Jl 15 10 5 - o 20 -| tree D 15 10 5NUMBER ing live snails simply moved into the living parts of the Dubautia and eventually into the Coprosma. During 1992, upward growth of the Coprosma brought its branches and leaves into extensive contact with a large overhanging o'hia tree {Metrosideros polymorpha), and remaining snails (about five) probably dispersed into the larger tree. No ground shells were found to account for their disappearance. Ground shells occurred beneath Trees A and B during the first half of this study, and Euglandina rosea was common at the site. By clearing dense ground cover around trees A, B and D, and visiting the site twice per month from November 1988 to November 1989 to search for and collect specimens of the predatory snail (four were collected alive), its depredations were considerably reduced. This was apparent from the decline in numbers of dead shells of A mustelina, as well as the apparent stability of the population of snails in Tree D from at least mid1989 to the present. However, only four mature snails are currently present, and, with a reproductive population this small, any increased mortality caused either by rats or Euglandina could lead to rapid disappearance of snails at this site. It is worth noting that the distribution of Achatinella mustelina in the southern Wai'anae Mountains previously extended downslope from our study site to much lower elevations, and old ground shells can be found there. It appears that predation by E. rosea has progressed upward, annihilating nearly all native snails lower than the elevation where our study site lies. Palikea Tree J was one of a pair of small o'hia {Metrosideros polymorpha) atop a small peak at 930 m elevation. The other, originally designated 'Tree F,' harbored a small population of snails that declined to a single snail by August 1989. The population in Tree J (Fig. 7) has remained fairly constant throughout our study, and promises to continue in this state unless invaded by predators. Like Tree D, however, it harbors only about four mature snails, and this population could easily lose its reproductive capacity. If fecundity of these adults is as high as at Pahole, we would expect a treewide birth rate of about 30 snails per year. n 20 - tree F 15 10 - J \ 50 20 -, 15 - 1 1— •—•—i = » tree J 10 50- •V 1988'1989'l990'1991'l992' DATE OF VISIT FIG. 7. Population sizes in four study trees at the Palikea area. Numbers of snails seen in each tree are plotted against date of the monitoring visit to the sites. We cannot account for this many small snails, but the great exposure of this site to sunlight, heat and wind, should predispose it to high juvenile mortality for as many as 6-8 mo of the year. In addition, a ground cover of deep grass prevents efficient recovery of small, dead shells. Motility At both study sites, the same snails were recaptured repeatedly over many years. The isolation of some of the trees in the Palikea populations makes this less surprising than at Pahole where trees in the study quadrate extend across the quadrate boundaries. Additionally, branches of the trees within the quadrate intermingle with those of trees 620 M. G. HADFIELD ET AL. Partulina species have been studied on Molokai, and both found to have birth sizes of 4-5 mm, and growth rates that predict sexual maturity (at 19-22 mm) in the 4th to 7th year. Fecundities for all populations studied so far range from 4 to 7 offspring per year. This pattern thus appears to be conserved across the subfamily from a common ancestor that itself evolved in Hawai'i. Late age at maturation and low fecundity have particularly predisposed this large group of endemic snails to extinction when exposed to alien predators such as rats, snails and human shell collectors, especially after their original ranges were drastically reduced by the land-clearing of early Hawai'ians and later European farmers. Populations of A. mustelina in the study trees at Palikea in the southern Wai'anae DISCUSSION Range were small at the beginning of this Life-history characteristics of Achatinella study, and only predator-control efforts have mustelina were determined previously at a allowed at least some of these populations different study site, Kanehoa, near the mid- to persist. Because of the precariousness of dle of the Wai'anae Range (Hadfield and these populations and the unique shell patMountain 1980). The Kanehoa site, also a terns found at Palikea, adult snails have been 25 m2 quadrate, differed from the Pahole brought to the laboratory as part of a capquadrate in number and species of trees, and tive-rearing program. in the general density of foliage, but the snail The multi-year study of population populations at the two locations were ini- dynamics at Pahole has revealed that poptially similar. Birth size at Kanehoa was ulations of Achatinella mustelina have the essentially the same as found at Pahole, but capacity to grow when not under predation growth rate was slower, and reproductive pressure; the population doubled in about maturity was estimated to occur at the end three years. However, the apparent plateau of the 6th year. Fecundity at Kanehoa was in snail numbers that persisted through estimated at less than one offspring per adult 1986, with a density of about 300 snails in per year, undoubtedly a significant under- a 25 m2 quadrate, was quickly reduced by estimate due to the low frequency of capture 80% when predators of two different types of small snails at that site; the structure of invaded the site. We suspect that only rapid the trees at Kanehoa made searching their rat-control efforts prevented the total extirhigher branches impossible. Given the pation of snails at this site. robust sample size and great duration of the We have attributed the rapid decline in study at Pahole, there is no reason to ques- snail numbers at Pahole in 1987 to a bout tion the life-history characteristics of A. of predation by Euglandina rosea, based on mustelina as determined there. In addition, the size-specific distribution of snail deaths. devastating predation by Euglandina rosea Mortality during the population crash difwas seen at both sites. At Kanehoa, the fered from typical "background" in both the native snail population was eventually com- numbers of snails dying and the sudden pletely destroyed. inclusion of much larger snails among the The life history pattern presented here for fatalities. The question arises, why didn't A. mustelina is consistent across species in this trend continue until the population was two genera of the subfamily Achatinellinae extinct? There are at least two possible on two islands, O'ahu and Molokai (Had- answers, the first being the most obvious. field, 1986, Hadfield and Miller, 1989). Two Euglandina rosea is as susceptible to rat preoutside. Occasionally, marked snails were found outside the quadrate, and new, large snails were found within, indicating the sitefidelity is not absolute. Still, extremely low motility is the rule for A. mustelina in both locations. We observed one time during this study an event that probably represents a major dispersal event for these snails. A violent windstorm in January 1985 knocked many snails from their trees, and at the next visit to the site we found marked snails up to 20 m outside the quadrate boundaries and some large unmarked snails within the quadrate. It appeared that snails blown from the trees, probably with the leaves upon which they were resting, crawled across the ground until they encountered a tree trunk which they then climbed. EXTINCTION IN HAWAI'IAN TREE SNAILS dation as A. mustelina, and perhaps even more so given its typical ground-dwelling, nocturnal habits. Thus the rat invasion that eventually destroyed nearly all of the larger A. mustelina in the quadrate, may have also annihilated the predatory snails at the site. A second possibility is that the predatory snails simply moved out of the area as prey became less dense and hunting effort less effective. It must be concluded that, of the two predators currently responsible for most mortality in Achatinella spp., Euglandina rosea is the far more serious. It preys on snails from all size classes, and, if it remains in an area, it will eventually destroy a prey population. This has undoubtedly happened repeatedly on O'ahu with a number of species. Secondly, E. rosea may attack an area in waves, so that a prey population decimated at one time, may experience a new bout of predation just as, or even before, it begins to recover. Rats tend to be size selective and probably leave an area before completely destroying a prey-snail population; while reproductive capacity of the prey population will be significantly negatively affected, the population may survive and in time begin to grow again. Because Rattus rattus and R. norvegicus were introduced soon after European contact with the Hawai'ian Islands, we must assume that Hawai'ian tree snails have survived nearly 200 years of rat depredations (more than 1,000 years of predation by the Polynesian rat, Rattus exulans, appears not to have significantly reduced snail numbers; see Hadfield, 1986). By contrast, Euglandina rosea was introduced to Hawai'i in 1958, and its destructive effects on native snails were almost immediately noticed. However, epidemic invasions by either predator contributes significantly to extinction in terrestrial Hawai'ian snails. It is particularly enlightening to learn that demographic patterns allow an investigator to determine the nature of pressures on a population. For A. mustelina, increased mortality weighted toward smaller size classes appears to signal predation by the snail Euglandina rosea, while increased mortality among largest size classes is indicative of rat predation, confirmed by the 621 sharply broken shells of the prey snails. Because predator-control efforts are typically predator specific, a means for quickly determining the nature of the threat to a population is invaluable. For example, with this new knowledge of predation patterns on A. mustelina, we can determine if a population is currently under predation pressure and which predator is acting upon it from only a single pair of visits, one to clear the ground of dead shells and a second to record the distribution of mortality by size and presence of broken shells. Population monitoring at the Palikea site has been important for several reasons. Those populations of Achatinella mustelina have different and more variable shell-color patterns than are present in the Pahole population. The Palikea populations occupy different types of vegetation, and some of the trees are isolated from all others. In addition, the populations are very small. At this time, snails appear to have vanished from two of the small trees and remained relatively stable at two others, even though there are only 7-14 snails per tree. Continued monitoring of these trees, if predation can be forestalled, may clarify what happens when snail populations become very dense in the small trees; does reproduction decline, do snails die, or does out-migration occur? Such knowledge is essential for long-range management planning for the conservation of Hawai'ian tree snails. If comparison of the results of studies of Achatinella mustelina at three different sites (two in the present study, plus the midWai'anae Range site studied by Hadfield and Mountain [1980]) has a particular lesson, it is probably that snail populations in dense and continuous forest, as observed at the Pahole site, have a better chance of survival than those in single isolated trees or even those in more open forest such as at the Kanehoa location. The exceedingly low motility of these snails, a fact that makes their study much easier, contributes greatly to a vulnerability that is only somewhat reduced by greater habitat complexity. Clearly, conservation efforts for endemic Hawai'ian arboreal snails must include habitat conservation and restoration, and preserved habitats must be of dimensions large 622 M. G. HADFIELD ET AL. enough to provide refuges for the snails from localized onslaughts of predatory snails and rats. The lessons learned here have broader application than just to the tree snails of O'ahu. They probably hold for the numerous endemic snails of other families, as well as other invertebrates of the tropical Pacific oceanic islands (e.g., Partula spp. in French Polynesia, [Murray et al, 1988]; Powelliphanta spp. of New Zealand, [Meads et al, 1984]); these islands are home to thousands of species with low motility and highly restricted ranges. However, such species are not limited to oceanic islands; continental snail species, or those inhabiting continental islands (e.g., the snail Orthalicus reses reses of Florida, [Franz 1982]), may have small ranges and the same vulnerabilities to new predators as Achatinella mustelina. Other characters that are encountered more often among the biotas of oceanic islands are absence of protective devices and behaviors, and life histories that are illadapted to predator harvesting. The same will be true of soil arthropods, worms and other non-flying invertebrates. ACKNOWLEDGMENTS The authors gratefully acknowledge generous financial assistance from the Department of Forestry and Wildlife, State of Hawaii (DOFAW), the U.S. Fish and Wildlife Service, and the Cooke Foundation. Access to the Pahole site was made possible by DOFAW, and access to the Palikea sites was assisted by the Campbell Estate and The Nature Conservancy of Hawaii. Volunteers from The Nature Conservancy greatly assisted the efforts to control predators at the Palikea sites. Rat control efforts at Pahole would have been impossible without the support of DOFAW staff, especially David Smith. Literally hundreds of colleagues, friends, and family members have provided excellent and generous assistance to our field studies over the last 10 years. Our most sincere thanks to all of the above. REFERENCES Atkinson, I. 1989. Introduced animals and extinctions. In: D. Western and M. C. 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