Download The Decimation of Endemic Hawaiian Tree

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. Pearl, (eds.), Conservation for the twenty-first century, pp. 54-75.
Oxford Univ. Press, New York.
Begon, M. 1979. Investigating animal abundance:
Capture-recapture for biologists. University Park
Press, Baltimore.
Crowell, K. L. 1968. Rates of competitive exclusion
by the argentine ant in Bermuda. Ecology 49:551555.
Diamond, J. M. 1984a. "Normal" extinctions of isolated populations. In: M. H. Nitecki, (ed.), Extinctions, pp. 191-246. Univ. Chicago Press.
Diamond, J. M. 19846. Historic extinctions: A rosetta
stone for understanding prehistoric extinctions. In:
P. S. Martin and R. G. Klein (eds.), Quaternary
extinctions: A prehistoric revolution, pp. 824-862.
Univ. Arizona Press, Tucson.
Diamond, J. 1989. Overview of recent extinctions.
In: D. Western and M. C. Pearl (eds.), Conservationfor the twenty-first century, pp. 37-41. Oxford
Univ. Press, New York.
Franz, R., (ed.) 1982. Rare and endangered biota of
Florida, Vol. 6, Invertebrates.
Gagne, W. C. 1981. Status of Hawaii's endangered
species: Insects and land snails. 'Elepaio 42:3136.
Gulick, J. G. 1905. Evolution, racial and habitudinal.
Carnegie Inst., Washington.
Hadfield, M. G. 1986. Extinction in Hawaiian achatinelline snails. Malacologia 27:67-81.
Hadfield, M. G. and S. E. Miller. 1989. Demographic
studies on Hawai'i's endangered tree snails: Partulina proxima. Pac. Sci. 43:1-16.
Hadfield, M. G. and B. S. Mountain. 1980. A field
study of a vanishing species, Achatinella mustelina
(Gastropoda, Pulmonata), in the Waianae Mountains of Oahu., Pac. Sci. 34:345-358.
Kaufmann, K. W. 1981. Fitting and using growth
curves. Oecologia 49:293-299.
Meads, M. J., K. J. Walker, and G. P. Elliott. 1984.
Status, conservation, and management of the land
snails of the genus Powelliphanta (Mollusca: Pulmonata). New Zealand J. Zoology 11:277-306.
Murray, J.,E. Murray, and M. S. Johnson. 1988. The
extinction of Partula on Moorea. Pac. Sci. 42:150153.
Olson, S. L. 1989. Extinction on islands: Man as a
catastrophe. In: D. Western and M. C. Pearl, (eds.),
Conservation for the twenty-first century, pp. 5052. Oxford Univ. Press, New York.
Pilsbry, H. A. and C. M. Cooke, Jr. 1912-1914.
Achatinellidae. Manual of conchology, 2nd ser.,
Vol.21.
Welch, D'A. 1938. Distribution and variation of
Achatinella mustelina Mighels in the Waianae
Mountains, Oahu. B. P. Bishop Museum Bulletin
152.